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The Bulletin of BISMiS Published by Bergey’s International Society for Microbial Systematics Volume 2, part 2 – December 2011

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Page 1: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

The Bulletin of BISMiSPublished by Bergey’s International Society for Microbial Systematics

Volume 2, part 2 – December 2011

Page 2: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

Published by Bergey’s International Society for Microbial Systematics

ISSN 2159-287X

On the cover

Oscillatoria cf. boryana from a tepid S-rich pool in New Zealand. Photograph supplied by Richard W. Castenholz – see his autobiography in this issue.

Editorial Board

'LUHFWRU�RI�WKH�(GLWRULDO�2IÀFH� William B. Whitman, Athens, GA, USA

(GLWRU� James T. Staley, Seattle, WA, USA

$VVRFLDWH�(GLWRU� Paul A. Lawson, Norman, OK, USA

(GLWRULDO�%RDUG�0HPEHUV� Hans-Jürgen Busse, Jongsik Chun, Paul De Vos, Michael Goodfellow, Brian P. Hedlund, Peter Kämpfer, Wen-Jun Li, Wolfgang Ludwig, Bruce J. Paster, Fred A. Rainey, Ken-ichiro Suzuki, Martha E. Tujillo, William G. Wade, Naomi L. Ward and William B. Whitman

0DQDJLQJ�(GLWRU� Aidan C. Parte, Sudbury, MA, USA

Copyright

The copyright in this publications belongs to Bergey’s International Society for Microbial Systematics (BISMiS). All rights reserved. This work may not be translated or copied in whole or in part without the written permis-sion of the publisher (BISMiS), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publica-WLRQ�RI�WUDGH�QDPHV��WUDGHPDUNV��VHUYLFH�PDUNV��DQG�VLPLODU�WHUPV��HYHQ�LI�WKH\�DUH�QRW�LGHQWLÀHG�DV�VXFK��LV�not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights.

© 2011 Bergey’s International Society for Microbial Systematics

3XEOLVKHU�DQG�(GLWRULDO�2IÀFH

Bergey’s International Society for Microbial SystematicsDepartment of Microbiology527 Biological Sciences BuildingUniversity of GeorgiaAthens, GA 30602-2605USA

email: [email protected]

The Bulletin of BISMiS

Page 3: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

Contents of Volume 2, part 2

ReviewA century of systematics of the genus Bacteroides��IURP�D�VLQJOH�JHQXV�XS�WR� the 1980s to an explosion of assemblages and the dawn of MALDI-TOF-Mass Spectrometry 87Haroun N. Shah and Saheer E. Gharbia

OpinionFunctional gene sequence studies of pure cultures are the basis of systematic studies of environmental communities of phototrophic bacteria and their VSHFLHV�VSHFLÀF�DQDO\VHV� � ���Johannes F. Imhoff

The importance of cultured representatives of the human intestinal microbiota in the metagenomic era 117Harry J. Flint and Sylvia H. Duncan

:RUNLQJ�WRZDUGV�D�0ROHFXODU�6\VWHPDWLFV�/LEUDU\�IRU�3URNDU\RWHV��D�SHUVSHFWLYH� � ���Xiao-Yang Zhi, Wei Zhao, Wen-Jun Li and Guo-Ping Zhao

Intent of the nomenclatural Code and recommendations about naming new species based on genomic sequences 135William B. Whitman

Biography3URIHVVRU�'U�'U�K�F��PXOW��2WWR�.DQGOHU��GLVWLQJXLVKHG� botanist and microbiologist 141Karl-Heinz Schleifer

AutobiographiesMy life as a microbiologist and naturalist 149Richard W. Castenholz

A little kid from Far Rockaway grows up 165Sydney M. Finegold

Papers from the Inaugural Meeting of BISMiS, Beijing, May 2011Isolation of novel natural products from un- or underexplored marine actinomycetes 181Na Yang, Biao Ren, Jian Wang and Li-Xin Zhang

CVTrees support the Bergey’s Systematics and provide high resolution at species levels and below 189Bailin Hao

The Bulletin of BISMiS

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Page 5: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

87© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 87–106

*The name “Bacteroides” used here initially is all-encompassing to illustrate their early history.

Contact detailsHealth Protection Agency Department for Bioanalysis and Horizon Technologies, 61 Colindale Avenue, London, NW9 5EQ, UK.

Corresponding author: Haroun Shah – [email protected]

Introduction

Few microbiologists are taxonomists by training, most de-velop their interest and acquire their skills from sustained studies of a particular habitat. The overwhelming range of inter- and intra-species diversity together with the problems RI�DVVLJQLQJ�XQNQRZQ�LVRODWHV�WR�D�SULRU�FODVVL¿FDWLRQ�RIWHQ�provides the impetus for in-depth analysis of an ecosystem and fuels an interest in systematics. Developments in the ¿HOG�RI�WD[RQRP\�RI�WKH�Bacteroides provide a poignant ex-ample in which huge debates were contested between those who were intransigent to taxonomic change and those who argued vehemently for modernization. Recognized very early on as a major component of the colon of man, workers LQ� WKH�¿HOG�RI�YHWHULQDU\��H�J��7��0LWVXRND��'��/RYH��(�0��

%DUQHV��5�(��+XQJDWH��0�3��%U\DQW��0��6HEDOG��0��/DWKDP��&��,PSH\��HW�DO���DQG�KXPDQ�VFLHQFHV��H�J��/�9��+ROGHPDQ��:�(�&��0RRUH��6�0��)LQHJROG��%��'UDVDU��-�*��&ROOHH��'�:��/DPEH��%�,��'XHUGHQ��:�3��+ROEURRN��+��%HHUHQV��+��:HU-QHU��6��/��*RUEDFN��)�3��7DOO\��9��5��'RZHOO��(��3��&DWR��9�/��6XWWHU��7��+RIVWDG��'�/��.DVSHU��6�6��6RFUDQVN\��.��2NXGD��6��7DEDTFKDOL��3��%RUULHOOR��0��+LOO��+��:HUQHU��5�-��*LEERQV��-�%��0DF'RQDOG��'��0D\UDQG��7�-�0��YDQ�6WHHQEHUJHQ��*�.��6XQGTYLVW��$�0��<RVKLPXUD�� ,��2OVHQ��(��1DJ\��HW�DO���SUR-duced voluminous literature in reference books, conference proceedings, original papers and were encapsulated in edi-tions of Bergey’s Manual, highlighting the ubiquitous pres-ence of a continuum of species that were compatible with the general description of “Bacteroides”.

)URP�WKH�RQVHW��WKH�EURDG�GHVFULSWLRQ�RI�WKH�JURXS��DV�*UDP�stain-negative, non-spore-forming, nonmotile, obligatory anaerobic rods that may or may not ferment carbohydrates prevailed through all editions of Bergey’s Manual of Deter-minative Bacteriology. This all-encompassing description of “Bacteroides”, together with a paucity of reliable char-acters for species’ descriptions resulted in the accumulation

Haroun N. Shah and Saheer E. Gharbia

A century of systematics of the genus Bacteroides��IURP�D�single genus up to the 1980s to an explosion of assemblages and the dawn of MALDI-TOF-Mass Spectrometry

The genus “Bacteroides” comprises the predominant group of micro-organism of the alimentary tract ZKHUH�WKH\�FRH[LVW�WR�WKH�PXWXDO�EHQHÀW�RI�WKH�KRVW��5HFHQW�VWXGLHV�RI�WKH�KXPDQ�JXW�PLFURELRPH�LV�revealing the emergence of universal dominant clusters (or enterotypes) of which Bacteroides, Pre-votella and Ruminococus are the dominant enterotypes (Arumugam et al., 2011). Perturbations in the local habitat are believed to trigger their translocation to new sites from where they cause numerous infections. The original “Bacteroides”* species were studied extensively in the rumen for nearly half a century and much of the fundamental science including anaerobic techniques were emulated to study LQIHFWLRQV�LQ�PDQ��VHH�H�J��+XQJDWH���������7RGD\�WKHLU�SK\VLRORJLFDO�IXQFWLRQV�DQG�VLJQLÀFDQFH�DUH�intensively studied in parallel with their phylogenetic relationships (see e.g. Karlsson et al., 2011) but this would not have been possible without painstaking work on their systematics from the mid-1970s. Once their heterogeneity had been ordered into coherent groups of species, more focused studies became possible and with the current interest in the human microbiome, their functional roles in vivo are becoming clearer. However, many taxa are non-fermentative and poorly circumscribed and new techniques are being explored to elucidate differential characters. This latter group has been one of the driving forces for the development of MALDI-TOF and LC-tandem mass spectrometry. This review charts the history of these taxonomic changes against the intransigence of established microbiologists DQG��WKH�RSSRVLQJ�YLHZV�RI�QHZFRPHUV�WR�WKH�ÀHOG�ZKR�V\VWHPDWLFDOO\�SHUVHYHUHG�WR�RYHUWXUQ�WKH�GRJPD�RI�PDQ\�GHFDGHV�LQWR�DQ�DFFHSWHG�FODVVLÀFDWLRQ�WKDW�WRGD\�FRQFXUV�ZLWK�WKHLU�SK\ORJHQ\�

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88 The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

of a large and heterogeneous collection of species that could QRW�EH�DFFRPPRGDWHG�HOVHZKHUH��%U\DQW�HW�DO���������0LW-VXRND� HW� DO��� ������+DUULVRQ� DQG�+DQVHQ�� ������&DWR� DQG�%DUQHV��������

The number of species varied periodically between editions of Bergey’s Manuals, however, the type species, Bacteroi-des fragilis, remained unchanged at the center of variation as the intrageneric structure of this group transformed over WKH�\HDUV��7KH� LQVSLUHG�ZRUN�RI�9HLOORQ�DQG�=XEHU� ��������ZKLFK�UHVXOWHG�LQ�WKH�LVRODWLRQ�RI�*UDP�VWDLQ�QHJDWLYH��QRQ�sporing, obligately anaerobic bacteria from various infec-tious sites, stimulated other workers around the turn of the FHQWXU\�� 1RWDEOH� H[DPSOHV� LQFOXGHG� WKH� ZRUN� RI� 7LVVLHU��������ZKR�UHSRUWHG�WKDW�WKH�SUHGRPLQDQW�PLFUR�RUJDQLVPV�RI� WKH� KXPDQ� FRORQ� ZHUH� DQDHUREHV� DQG� GHVFULEHG� ¿YH�³W\SHV´�ZKLOH�.UXPZLHGH� DQG� 3UDWW� ������� DQG�7XQQLFOLII��������UHSRUWHG�YDULRXV�DQDHURELF�IXVLIRUP�EDFWHULD��&DVWHO-ODQL�DQG�&KDOPHUV������DVVLPLODWHG�GHVFULSWLRQV�IURP�VHY-HUDO�RI�WKHVH�VWXGLHV��SDUWLFXODUO\�WKDW�RI�9HLOORQ�DQG�=XEHU��������IRU�WKH��VW�HGLWLRQ�RI�Bergey’s Manual��%HUJH\�HW�DO����������7KLV�ZDV�UHLQIRUFHG�E\�3ULPEUDP��������������ZKR�UHSRUWHG�VWXGLHV�RQ�WKH�FODVVL¿FDWLRQ�RI� WKHVH�PLFUR�RUJDQ-LVPV�EXW�ZDV�QRW�FLWHG�DV�WKHLU�VRXUFH�XQWLO�WKH��WK�HGLWLRQ�RI�Bergey’s Manual��������

7KH�¿UVW�UDGLFDO�FKDQJH�ZDV�ZLWQHVVHG�LQ�WKH��WK�HGLWLRQ�RI�the Manual��%HUJH\�HW�DO���������ZKHQ�DQ�DWWHPSW�ZDV�PDGH�to construct a combined schema incorporating the extensive ZRUN�RI�3UpYRW��������DQG�(JJHUWK�DQG�*DQQRQ���������7KH�QHZ�GH¿QLWLRQ�QRZ�HQFRPSDVVHG�RQO\�*UDP�VWDLQ�QHJDWLYH�species and the black pigment of colonies grown on blood agar was introduced as a new determinative character to identify Bacteroides melaninogenicus. /DUJHO\�EHFDXVH�RI�3UpYRW¶V�ZRUN��GDWD�RQ�DQLPDO�SDWKRJHQLFLW\� WHVWV�ZHUH� LQ-FOXGHG�IRU�WKH�¿UVW�WLPH�LQ�Bergey’s Manual��+RZHYHU��WKH�schema produced in the following edition of the Manual �%UHHG�HW�DO���������ZDV�FRQIXVLQJ�DV�LW�DOVR�LQFOXGHG�3UpY-RW¶V�ZRUN��������LQ�WKH�VDPH�FKDSWHU�WKDW�SURYLGHG�D�³NH\�WR�the species of the genus “Bacteroides”. Bacteroides species were described under the generic names “Ristella”, “Bacte-rium”, “Bacillus”, “Zuberella” or “Coccobacillus´��%HUJH\�HW� DO��� ������� 7KXV��Bacteroides fragilis and Bacteroides melaninogenicus were synonyms of Ristella fragilis and Ristella melaninogenica respectively.

The arrival of compact, largely automated gas-liquid chro-matographs facilitated the rapid analysis of volatile, short-chained fatty acid end products of metabolism such as for-mic, acetic, propionic, n-butyric, iso-butyric, and iso-valeric acids, etc., in microbiology laboratories. The diagnostic SUR¿OHV�RI�VSHFLHV�ZHUH�HIIHFWLYHO\�XVHG�E\�+ROGHPDQ�DQG�

0RRUH�WR�DJDLQ�IXQGDPHQWDOO\�UHVWUXFWXUH�WKH�JHQXV�Bacte-roides� ��������7KH� IDPLO\�Bacteroidaceae now comprised WKUHH�JHQHUD�EDVHG�RQ� WKH�SUR¿OH�RI� WKHLU� HQG�SURGXFWV�RI�PHWDEROLVP�� *HQXV� ��� Bacteroides, produced a complex PL[WXUH�RI�VKRUW�FKDLQHG�YRODWLOH� IDWW\�DFLGV��*HQXV����Fu-sobacterium, produced butyric acid as a major end product DQG� JHQHUDOO\� KDG� D� VLPSOHU� SUR¿OH�� ZKLOH� *HQXV� ��� Lep-totrichia, yielded lactic acid as its only major end product. While Fusobacterium and Leptotrichia were fairly well GH¿QHG�� WKH�Bacteroides were often deduced by failure to PDWFK� SUR¿OHV� WR� WKH� WZR� IRUPHU� JHQHUD�� :LWKLQ� WKH� JH-nus Bacteroides��VSHFLHV�SUR¿OHV�RI�DFLGV�ZHUH�GLYHUVH�DQG�PDWFKLQJ�DQ�XQNQRZQ�WR�D�JLYHQ�SDWWHUQ�IRU� LGHQWL¿FDWLRQ�was often subjective. Thus, although Bacteroides, moved WR�D�DQRWKHU�VWDJH�RI�FODVVL¿FDWLRQ��LW�ZDV�HYLGHQW�WKDW�VSH-FLHV�VWLOO�UHWDLQHG�FRQVLGHUDEOH�LQKHUHQW�KHWHURJHQHLW\��6HY-eral subspecies were conveniently created to minimize the number of species but these only served to obscure their intra-species diversity. The newly described genus Bacte-roides� H[FOXGHG����RI� WKH���� VSHFLHV�GHVFULEHG� LQ� WKH��WK�edition of the Manual��������ZKLOH�IRXU�VSHFLHV�FRPSULVHG�subspecies. Thus, Bacteroides melaninogenicus was listed as three subspecies, viz. Bacteroides melaninogenicus subsp. melaninogenicus for the highy saccharolytic strains, Bacte-roides melaninogenicus subsp. intermedius for moderately fermentative strains, and Bacteroides melaninogenicus sub-sp. asaccharolyticus for strains that were non-fermemtative. The species, Bacteroides fragilis, Bacteroides ruminicola, and Bacteroides clostridiiformis�ZHUH�DOVR�QRZ�UHGH¿QHG�WR�include subspecies.

,Q� WKH�����V� WR�����V��FKHPRWD[RQRPLF�DQDO\VHV�ZHUH�H[-tensively reported on members of the genus of Bacteroides. 7KH�KHWHURJHQHLW\�RI�WKLV�JURXS�ZDV�UHÀHFWHG�LQ�WKHLU�'1$�EDVH� FRPSRVLWLRQV�ZKLFK� UDQJHG� IURP���±���PRO��*�&��while large differences in long-chained cellular fatty ac-ids, menaquinone composition, polar lipids, peptidoglycan FKHPRW\SHV��6'6�3$*(�SDWWHUQV��DQG�PHWDEROLF�HQ]\PHV�ZHUH� UHSRUWHG� �IRU� UHYLHZV�� VHH�6KDK�����D������E���&RQ-VHTXHQWO\�� WKH�GLYHUVLW\�DPRQJ�VSHFL¿F�WD[D�ZDV�VXFK�WKDW�VHYHUDO� ZHUH� UHFODVVL¿HG� DQG� LQ� VRPH� FDVHV� QHZ� VSHFLHV�ZHUH�SURSRVHG��VHH�7DEOH�����,Q�WKH��VW�HGLWLRQ�RI�Bergey’s Manual of Systematic Bacteriology��+ROGHPDQ�HW�DO����������WKH�QXPEHU�RI�VSHFLHV�LQFUHDVHG�E\������7DEOH����RYHU�WKH�SUHYLRXV���WK��HGLWLRQ�RI�Bergey’s Manual of Determinative Bacteriology ������� E\� YLUWXH� RI� PDQ\� EHLQJ� HOHYDWHG� WR�species rank but mainly due to the large numbers reported IURP�WKH�RUDO�FDYLW\��+RZHYHU��WKH�FULWHULD�DQG�VWUXFWXUH�RI�WKH�JHQXV�IROORZHG�DORQJ�WKH�VDPH�OLQHV�DV�WKH��WK�HGLWLRQ�of the Manual��������DQG�WKH�WUHPHQGRXV�GLYHUVLW\�UHSRUWHG�within the genus was merely highlighted as footnotes to the chapter. This was echoed by the International Committee on

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89

Haroun N. Shah and Saheer E. Gharbia

The Bulletin of BISMiS

6\VWHPDWLF� %DFWHULRORJ\� 6XEFRPPLWWHH� RQ� WKH� 7D[RQRP\�RI�*UDP�QHJDWLYH�$QDHURELF�5RGV��ZKLFK�SHUVLVWHG�LQ�PDN-ing minimal changes to improve the taxonomy of the genus �VHH�H�J�� ,QWHUQDWLRQDO�&RPPLWWHH�RQ�6\VWHPDWLF�%DFWHULRO-RJ\���������7DEOH���SURYLGHV�D�VXPPDU\�RI� WKH�VHTXHQWLDO�FKDQJHV� UHSRUWHG� IURP�WKH��VW�HGLWLRQ�RI�Bergey’s Manual �%HUJH\�HW�DO���������WR�WKH��VW�HGLWLRQ�RI�Bergey’s Manual of Systematic Bacteriology��������

Bacteroides melaninogenicus, focus of WKH�ÀUVW�FKDQJH

This broad acceptance of heterogeneity permeated to the spe-cies level. Thus, the species Bacteroides melaninogenicus encompassed strains that were metabolically very diverse but resided in juxtaposition to each other as “subspecies” to avoid taxonomic change. In any other branch of taxonomy it would be irreconcilable that a species could encompass VDFFKDURO\WLF� �Bacteroides melaninogenicus subsp. mela-ninogenicus���PRGHUDWHO\� VDFFKDURO\WLF� �Bacteroides mela-ninogenicus subsp. intermedius) and also non-fermentative Bacteroides melaninogenicus subsp. asaccharolyticus) strains into a single species. The overriding property of the black pigment, observed after growth on blood agar plates by Bacteroides melaninogenicus was the basis in which the KHWHURJHQHLW\� RI� WKLV� VSHFLHV�ZDV� DFFHSWHG��7KH� VFLHQWL¿F�community held steadfastly to the accepted dogma and was so refractory to change, it would seem prudent that detailed characterization of the pigment of Bacteroides melanino-genicus, its most weighted yet contentious character, might provide the momentum for change.

7KLV� VSHFLHV� ZDV� ¿UVW� GHVFULEHG� LQ� ����� E\� 2OLYHU� DQG�Wherry as Bacteroides melaninogenicum because it was thought that the distinctive black pigment produced by FHOOV�JURZQ�RQ�EORRG�DJDU�SODWHV�ZDV�PHODQLQ��2OLYHU�DQG�:KHUU\���������$OWKRXJK�WKH�SLJPHQW�ZDV�LQFRUUHFWO\�LGHQ-WL¿HG��6FKZDEDFKHU�HW�DO����������WKH�DFFHSWHG�UXOHV�RI�QR-PHQFODWXUH�RYHUUXOHG� WKH�VXJJHVWHG�FKDQJH�RI� WKH�VSHFL¿F�epithet to Bacteroides nigrescens, and “melaninogenicus” was retained. The nature of the pigment was contested by 7UDF\� �������ZKR� UHSRUWHG� WKDW� WKH� SLJPHQW�ZDV� QRW� VSH-FL¿F�IRU�Bacteroides melaninogenicus and could be induced in other non-pigmented species such as Bacteroides fragi-lis. 7UDF\� �������VWDWHG� WKDW� WKH�SLJPHQW�ZDV�H[WUDFHOOXODU�DQG�LGHQWL¿HG�LW�DV�FROORLGDO�IHUURXV�VXO¿GH��+RZHYHU��PRVW�studies demonstrated that the pigment was only produced ZKHQ�FHOOV�ZHUH�FXOWXUHG�RQ�EORRG�DJDU�DQG�ZDV�VSHFL¿F�IRU�Bacteroides melaninogenicus �'XHUGHQ���������2XU�VWXGLHV��6KDK�HW� DO��� ������ VKRZHG� WKDW� WKH�GHSWK�DQG�GXUDWLRQ�RI�SLJPHQWDWLRQ� YDULHG� DPRQJ� VWUDLQV� DQG� ORQJ�ZDYH�89� UD-diation was pronounced before the characteristic jet-black

SLJPHQWDWLRQ� DURVH�� /DUJH�VFDOH� H[WUDFWLRQ�� FU\VWDOOL]DWLRQ�and mass spectral determination of the pigments eventually FRQ¿UPHG�WKHP�WR�EH�SURWRKDHPLQ��QRQ�ÀXRUHVFHQW��ZKLOH�WKH�EULJKW�ÀXRUHVFHQW�FRPSRXQG�ZDV�VKRZQ�WR�EH�SURWRSRU-SK\ULQ��6KDK�HW�DO���������2I�WKH�WKUHH��VXEVSHFLHV�³melanin-ogenicus” produced mainly protoporphyrin hence colonies on blood agar were often light brown to beige rather than EODFN� �)LJXUH� ���� 6RPH� ODERUDWRULHV� UHSRUWHG� WKDW� VWUDLQV�of Bacteroides melaninogenicus showed no pigmentation while conversely isolates of the non-pigmented species Bac-teroides oralis were found to pigment so consistently that extensive re-examination of this equally contentious group began.

$� NH\� SURSHUW\� RI Bacteroides oralis was its inability to form black-pigmented colonies on blood agar or to ferment WKH� SHQWRVH� VXJDUV�� [\ORVH� DQG� DUDELQRVH�� �/RHVFKH� HW� DO����������7KH�ODWWHU�ZDV�GHVFULEHG�DV�D�VLJQL¿FDQW�GLIIHUHQWLDO�property of the rumen spcies, Bacteroides ruminicola �%HU-JH\¶V��������+RZHYHU��VWUDLQV�GHVLJQDWHG�Bacteroides oralis �LQFOXGLQJ� WKH�7\SH�VWUDLQ��&0��ZHUH�YHU\�KHWHURJHQHRXV�and found to be incompatible with its original description.

Figure 1. Variation in colonial morphology and depth of pigmentation among strains of “Bacteroides mela-ninogenicus” grown on blood agar plates. Strain VPI 9085 was a reference strain of “Bacteroides oralis that pigmented, albeit light brown and was eventually used to create the new species “Bacteroides loescheii” after Loesche et al. (1964) who proposed the species, Bac-teroides oralis. Strain W83 showed mucoid dark brown colonies, characteristic of the asaccharolytic strains. T588, a representative of the moderately saccharolytic group formed very small, jet-black, pigmented colonies.

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90 The Bulletin of BISMiS

A century of systematics of the genus BacteroidesTa

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s ba

sed

on m

orph

olog

ical

and

bio

chem

ical

dat

a, la

ter

edit

ions

of

Berg

ey’s

(fr

om 4

th e

diti

on)

bega

n in

corp

orat

ing

them

in a

sin

gle

syst

em w

ith

the

genu

s na

me

Bact

eroi

des

taki

ng p

rece

denc

e.

Edit

ion

deta

ils,

cont

ribu

tors

, an

d no

tes

Fam

ily/t

ribe

/gen

us/s

peci

esSa

lient

phe

noty

pic

test

sH

abit

at

1st

edit

ion

of B

erge

y’s

Man

ual o

f De

term

inat

ive

Bact

erio

logy

(19

23),

pp

. 25

5–26

4.

D.H

. Be

rgey

, F.

C. H

arri

son,

R.S

. Br

eed,

B.W

. H

amm

er a

nd F

. M

. H

unto

on.

Fam

ily IV

: Ba

cter

iace

ae

Trib

e IX

: Ba

cter

oide

ae

Gen

us X

VIII:

Bac

tero

ides

Cas

tella

ni a

nd C

halm

ers.

Sp

ecie

s: 1

7 w

ere

desc

ribe

d as

fol

low

s:

(1)

B. f

ragi

lis

(Typ

e);

(2)

B. c

ornu

tus;

(3)

B.

vari

abil

is;

(4)

B. d

imor

-ph

us;

(5)

B. la

evis

; (6

) B.

pse

udor

amos

us;

(7)

B. t

ortu

osus

; (8

) B.

an

gulo

sus;

(9)

B.

acum

icat

us;

(10)�%��ELÀGX

V; (

11)

B. b

ullo

sus;

(12

) B.

var

iega

tus;

(13

) B.

the

taio

taom

icro

n; (

14)

B. li

quef

acie

ns;

(15)

B.

rig

idus

; (1

6) B

. te

nuis

; (1

7) B

. m

ulti

form

is.

Even

tho

ugh

Oliv

er a

nd W

herr

y ha

d de

scri

bed

the

blac

k-pi

gmen

ted

spec

ies

B. m

elan

inog

encu

s in

192

1, it

was

not

incl

uded

in B

erge

y’s

Man

ual u

ntil

the

5th

edit

ion

(193

9).

'HÀQ

LWLRQ�WDNHQ�IURP

�&DVWHOOD

QL�DQG

�Ch

alm

ers

1919

; m

otile

and

non

-mo-

tile

rod

s, w

itho

ut e

ndos

pore

s. S

how

s go

od g

row

th o

n or

dina

ry c

ultu

re

med

ia;

wit

hout

pig

men

t fo

rmat

ion.

Al

l obl

igat

e an

aero

bes.

Key

tes

ts

wer

e: m

otili

ty,

coag

ulat

ion

of m

ilk,

indo

le a

nd a

cid

from

glu

cose

. Ab

out

half

of

the

spec

ies

liste

d in

-cl

udin

g th

e ty

pe s

peci

es,

B. f

ragi

lis

wer

e de

scri

bed

as G

ram

-pos

itiv

e.

All i

sola

tes

wer

e fr

om t

he in

test

i-na

l tra

ck o

f m

an

and

anim

als;

B.

frag

ilis

isol

ated

fr

om a

gan

gre-

nous

app

endi

x.

A fe

w s

peci

es

wer

e fa

cult

ativ

ely

anae

robi

c.

2nd

edn

(192

6),

pp.

271–

279.

D.H

. Be

rgey

, F.

C. H

arri

son,

R.S

. Br

eed,

B.W

. H

amm

er a

nd F

. M

. H

unto

on.

Fam

ily IV

: Ba

cter

iace

ae

Trib

e XI

: Ba

cter

oide

ae

Gen

us X

XI:

Bact

eroi

des

Cast

ella

ni a

nd C

halm

ers

1919

.

Unc

hang

ed f

rom

the

1st

edi

tion

. Se

vera

l spe

cies

con

tinu

e to

be

liste

d as

“G

ram

-pos

itiv

e”.

Unc

hang

ed f

rom

th

e 1s

t ed

itio

n.

3rd

edn

(193

0),

pp.

369–

378.

D.H

. Be

rgey

, F.

C. H

arri

son,

R.S

. Br

eed,

B.W

. H

amm

er a

nd F

. M

. H

unto

on.

Fam

ily IV

: Ba

cter

iace

ae

Trib

e XI

II: B

acte

roid

eae

Gen

us X

XIV:

Bac

tero

ides

Cas

tella

ni a

nd C

halm

ers

1919

. Sp

ecie

s: 1

9: T

wo

new

spe

cies

, B.

ovi

form

is a

nd B

. fu

ndib

ulif

orm

is

wer

e ad

ded.

Unc

hang

ed f

rom

the

pre

viou

s ed

i-ti

ons.

Indo

le p

rodu

ctio

n an

d ac

id in

m

ilk w

ere

key

char

acte

rs.

Mor

phol

-og

y an

d lim

ited

ran

ge o

f ca

rboh

y-dr

ate

ferm

enta

tion

rea

ctio

ns u

sed

for

spec

iati

on.

All s

peci

es w

ere

inte

stin

al e

xcep

t B.

fun

dibu

lifo

r-m

is w

hich

was

is

olat

ed f

rom

a

vagi

nal a

bsce

ss.

4th

edn

(193

4),

pp.

404–

413.

D.

H.

Berg

ey,

R.S.

Bre

ed,

B.W

. H

am-

mer

, F.

M.

Hun

toon

, E,

G.D

.Mur

ray

and

F.C.

Har

riso

n.

Fam

ily IV

: Ba

cter

iace

ae

Trib

e XI

II: B

acte

roid

eae

Gen

us X

XVI:

Bac

tero

ides

Cas

tella

ni a

nd C

halm

ers

1919

. Sp

ecie

s: a

ll 19

spe

cies

des

crib

ed b

efor

e w

ere

reta

ined

.

B. f

ragi

lis ZDV�OLVWHG

�IRU�WKH

�ÀUVW�

tim

e as

“G

ram

-var

iabl

e”.

Unc

hang

ed f

rom

th

e 3r

d ed

itio

n.

Page 9: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

91

Haroun N. Shah and Saheer E. Gharbia

The Bulletin of BISMiS

Edit

ion

deta

ils,

cont

ribu

tors

, an

d no

tes

Fam

ily/t

ribe

/gen

us/s

peci

esSa

lient

phe

noty

pic

test

sH

abit

at

5th

edn

(193

9),

pp.

556–

586.

D.H

. Be

rgey

, R.

S. B

reed

, E,

G.D

. M

urra

y an

d A.

P.

Hit

chen

s.

7KH�H[WHQVLYH�ZRUN�RI�3UpYRW�

(193

8) a

nd E

gger

th a

nd G

anno

n (1

933)

wer

e no

w in

corp

orat

ed.

3UpYRW·V�FODVVLÀFDWLRQ

�SODFHG�

Bac-

tero

ides

in t

wo

Ord

ers

com

pris

ing

eigh

t ge

nera

.

Fam

ily X

I: B

acte

riac

eae

Trib

e: (

Nil)

G

enus

VIII

: Ba

cter

oide

s Ca

stel

lani

and

Cha

lmer

s 19

19.

Spec

ies:

21

liste

d bu

t on

ly f

our,

B. f

ragi

lis,

B.

vari

abil

is,

B. f

un-

dibu

lifo

rmis

and

B.

thet

aiot

aom

icro

n w

ere

reta

ined

fro

m t

he 4

th

edit

ion.

19

new

spe

cies

wer

e lis

ted:

B.

ser

pens

; B.

sic

cus;

B.

coag

ulan

s; B

. va

rius

; B.

inae

qual

is;

B. in

-so

litu

s; B

. ve

scus

; B.

exi

guus

; B.

unc

atus

; B.

vul

gatu

s; B

. in

com

mu-

nis;

B.

dist

ason

is;

B. t

umid

us;

B. c

onve

xus;

B.

ovat

us;

B. u

nifo

rmis

; B.

gul

osus

; B.

cav

iae

and

B. m

elan

inog

enic

us.

A m

ore

exte

nsiv

e lis

t of

fer

men

ta-

tion

tes

ts w

ere

now

incl

uded

. So

me

that

wer

e hi

ther

to c

onsi

dere

d G

ram

-pos

itiv

e (e

.g.

B. f

ragi

lis)

, w

ere

reas

sess

ed a

nd e

xclu

ded

if t

hey

Gra

m-p

osit

ive.

A nu

mbe

r of

hu-

man

sit

es w

ere

now

incl

uded

; e.

g. u

rina

ry t

ract

, ge

nita

lia,

surg

ical

w

ound

s pu

lmo-

nary

infe

ctio

ns,

sept

icem

ias,

ab

sces

ses.

For

WKH�ÀUVW�WLP

H��WKH

�or

al c

avit

y w

as

cite

d as

a h

abit

at

for

B. m

elan

ino-

geni

cus.

6th

edn

(194

8),

pp.

564–

581.

I. H

uddl

eson

, F.

Joh

nson

, F.

H.

Kauf

fman

n an

d C.

D. K

elly

.

%RWK�V\VWHPV�>3UpYRW��������DQG

�Eg

gert

h an

d G

anno

n (1

933)

] w

ere

not

test

ed in

par

alle

l hen

ce t

he

VFKH

PD�GUDZ

Q�XS

�IRU�WKH

LU�LG

HQWLÀ-

cati

on w

as c

onsi

dere

d “t

enta

tive

” at

tha

t st

age.

Fam

ily X

I: P

arvo

bact

eria

ceae

Tr

ibe

III:

Bact

eroi

deae

G

enus

I: B

acte

roid

es C

aste

llani

and

Cha

lmer

s. 1

919.

(re

vise

d by

T.

E. R

oy a

nd C

.D.

Kelly

).

Spec

ies:

the

23

spec

ies

liste

d in

the

5th

edi

tion

wer

e re

tain

ed

unch

ange

d.

Phen

otyp

ic p

rope

rtie

s w

ere

reta

ined

fr

om t

he 5

th e

diti

on b

ut t

here

wer

e se

vera

l nom

encl

ator

ial c

hang

es.

Unc

hang

ed f

rom

th

e 5t

h ed

itio

n.

7th

edn

(195

7),

pp.

423–

436.

N.R

. Sm

ith.

The

unce

rtai

nty

of t

he p

revi

ous

edit

ion

was

rep

lace

d by

a m

ore

GHÀQ

LWLYH��FRQ

FLVH�VFKHP

H�

Fam

ily V

I: B

acte

roid

acea

e Tr

ibe:

Nil

Gen

us I:

Bac

tero

ides

Cas

tella

ni a

nd C

halm

ers

1919

. Sp

ecie

s: 3

0 sp

ecie

s. 14

new

spe

cies

wer

e lis

ted:

B.

fur

cosu

s;B.

per

foet

ens;

B.

tric

hoid

es;

B. t

ereb

ans;

B.

halo

s-m

ophi

lus;

B.

puti

dus;

B.

putr

edin

is;

B. c

apil

losu

s; B

. cy

lind

roid

es;

B. s

ucci

noge

nes;

B.

glut

inos

us;

B. d

esti

llat

ioni

s: B

. vi

scos

us;

B.

vari

egat

es.

7 sp

ecie

s lis

ted

in t

he 6

th e

diti

on w

ere

excl

uded

: B.

fun

dibu

lifo

r-m

is,

B. s

iccu

s, B

. va

rius

, B.

gul

osus

and

B.

cavi

ae,

B. in

aequ

alis

an

d B.

ves

cus.

Key

hier

arch

al t

ests

incl

uded

: m

otili

ty,

enca

psul

atio

n, g

elat

in

lique

fact

ion,

req

uire

men

t fo

r se

rum

or

asc

itic

, ca

rboh

ydra

te f

erm

enta

-ti

on t

ests

and

cel

lula

r m

orph

olog

y.

Cellu

lose

was

incl

uded

to

iden

tify

sp

ecie

s su

ch a

s B.

suc

cino

gene

s WKDW�FDQ

�GLJHVW�LW�ZKLOH�UXP

HQ�ÁXLG�

was

add

ed t

o im

prov

e th

e gr

own

of

mic

ro-o

rgan

ism

s fr

om t

his

site

.

The

habi

tat

of

the

grou

p w

as d

e-sc

ribe

d as

“fo

und

in t

he a

limen

tary

an

d ur

ogen

tica

l tr

acts

of

man

and

ot

her

anim

als”

. W

ork

on r

umen

sp

ecie

s by

Bry

ant

et a

l. (

1958

) an

d H

unga

te (

1966

) w

ere

wid

ely

re-

port

ed.

Page 10: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

92 The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

Edit

ion

deta

ils,

cont

ribu

tors

, an

d no

tes

Fam

ily/t

ribe

/gen

us/s

peci

esSa

lient

phe

noty

pic

test

sH

abit

at

8th

edn

(197

4),

pp.

384–

404

L.V.

Hol

dem

an a

nd W

.E.C

. M

oore

. (B

ased

on

“The

Vir

gini

a Po

lyte

ch-

nic

Inst

itut

e an

d St

ate

Uni

vers

ity

Anae

robe

Lab

orat

ory”

, Bl

acks

burg

, VA

, 1s

t ed

itio

n, 1

972)

. It

incl

uded

H[WHQVLYH�ZRUN�IURP

�3UpYRW��������

and

Seba

ld (

1962

) w

here

met

abol

ic

end

prod

ucts

and

DN

A ba

se c

ompo

-si

tion

s w

ere

alre

ady

bein

g us

ed f

or

FODVVLÀF

DWLRQ��

Fam

ily 1

: Ba

cter

oida

ceae

Pri

bram

193

3, 1

0.

Gen

us 1

: Ba

cter

oide

s Ca

stel

lani

and

Cha

lmer

s 19

19.

Spec

ies:

22

liste

d w

ith

a nu

mbe

r of

sub

spec

ies.

B.

fra

gili

s w

as r

etai

ned

as t

he t

ype

spec

ies

but

5 ph

enot

ypic

ally

cl

osel

y re

late

d sp

ecie

s w

ere

redu

ced

to s

ubsp

ecie

s ra

nk a

s fo

llow

s:

B. f

ragi

lis

subs

p. f

ragi

lis;

B.

frag

ilis

sub

sp.

vulg

atus

; B.

fra

gili

s su

bsp.

dis

taso

nis;

B.

frag

ilis

sub

sp.

ovat

us;

B. f

ragi

lis

subs

p. t

he-

taio

atom

icro

n.

In a

ddit

ion

to t

he a

bove

, th

e fo

llow

ing

7 sp

ecie

s in

7th

edi

tion

w

ere

reta

ined

: B.

put

redi

nis;

B.

furc

osus

; B.

suc

cino

gene

s; B

. se

rpen

s an

d B.

m

elan

inog

enic

us.

18 s

peci

es li

sted

in p

revi

ous

edit

ion

wer

e ex

clud

ed.

14 n

ew s

peci

es w

ere

liste

d: B

. ru

min

icol

a (2

sub

spec

ies)

; B.

oc

hrac

eus;

B.

oral

is;

B. a

myl

ophi

lus;

B.

hype

rmeg

as;

B. t

erm

itid

is;

B. b

iacu

tus;

B.

clos

trid

iifor

mis

(2

subs

peci

es);

B.

cons

tell

atus

; B.

pra

eacu

tus;

B.

corr

oden

s; B

. no

dosu

s; B

. pn

eum

osin

tes

and

B.

nige

r.

The

key

to d

elin

eati

on o

f sp

ecie

s pl

aced

hea

vy r

elia

nce

on p

igm

ent

form

atio

n on

blo

od a

gar

plat

es.

Cel-

lula

r m

orph

olog

ies

base

d on

mic

ros-

copy

wer

e sk

etch

ed. A

n ex

tens

ive

list

of c

arbo

hydr

ates

wer

e us

ed t

o di

ffer

enti

ate

spec

ies

alon

g w

ith

thei

r m

ajor

aci

d en

d pr

oduc

t/s.

Whe

re

know

n th

e m

ol%

G+C

con

tent

for

sp

ecie

s w

ere

give

n an

d fe

ll w

ithi

n th

e ra

nge

40–5

5%.

Oth

er t

ests

wer

e gi

ven

by D

owel

l an

d H

awki

ns (

1968

) an

d Su

tter

et

al.

(197

5)

Stra

in f

rom

an

imal

s ex

tend

ed

and

incl

uded

one

sp

ecie

s fr

om t

he

inte

stin

al c

on-

tent

s of

ter

mit

es

(B.

term

itid

is)

whi

ch h

ad a

low

G

+C c

onte

nt o

f 34

m

ol%.

1st

edit

ion

(198

4) o

f Be

rgey

’s

Man

ual o

f Sy

stem

atic

Bac

teri

olog

y,

pp.

602–

631

L.V.

Hol

dem

an,

R. W

. Ke

lley

and

W.E

.C.

Moo

re.

(Bas

ed o

n ‘T

he V

irgi

nia

Poly

tech

-ni

c In

stit

ute

and

Stat

e U

nive

rsit

y An

aero

be L

abor

ator

y’,

Blac

ksbu

rg,

Virg

inia

, 4t

h Ed

. 19

77).

Fam

ily 1

: Ba

cter

oida

ceae

Pri

bram

193

3, 1

0.

Gen

us 1

: Ba

cter

oide

s Ca

stel

lani

and

Cha

lmer

s 19

19.

Spec

ies:

39

desc

ribe

d.

A nu

mbe

r pr

evio

usly

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)LJXUH���VKRZV�WKH�,()�SURWHLQ�SDWWHUV��LQ�D�QDUURZ�S+�JUD-GLHQW�RI����±�����RI����VWUDLQV� WKDW�ZHUH�ZLGHO\�FLUFXODWHG�as authentic cultures of Bacteroides oralis and highlights this incongruity. Four groups were resolved and shown by '1$±'1$� UHDVVRFLDWLRQ� WR� FRPSULVH� WKH� QXFOHXV� RI� ¿YH�distinct species that were eventually proposed as Bacteroi-des buccalis, Bacteroides denticola and Bacteroides pento-saceus �WKH�ODWWHU�ZDV�VXEVHTXHQWO\�FKDQJHG�WR�Bacteroides buccae��%HUJH\¶V�������+ROGHPDQ�DQG�-RKQVRQ��������6KDK�DQG�&ROOLQV���������5HODWHG�VSHFLHV�Bacteroides veroralis sp. QRY��ZDV�SURSRVHG�E\�:DWDEH�HW�DO���������DQG�Bacteroides oulorum VS��QRY��E\�6KDK�HW�DO���������

7KH�XQDPELJXRXV�LGHQWL¿FDWLRQ�RI�WKH�SLJPHQWV�RI�Bacteroi-des melaninogenicus OHG�WR�VWXGLHV�RI�WKHLU�IXQFWLRQ��3RUSK\-rins are often present as the prosthetic group of cytochromes and cell extracts of both pigmented and non-pigmented spe-cies were found to have cytochrome c and cytochrome b �6KDK������E���$W�WKDW�WLPH��DQDHURELF�EDFWHULD�ZHUH�WKRXJKW�to utilize ferrodoxin-type mechanisms for energy conserva-tion. The presence of porphyrins supported the view of an DQDHURELF� HOHFWURQ� WUDQVSRUW� FKDLQ� LQ�*UDP�VWDLQ�QHJDWLYH�anaerobes and represented a major divergence from other anaerobic species. The electron-transport complex was shown to consist of another electron transport carrier, mena-quinone, derived from its growth requirement for vitamin .���6KDK�DQG�&ROOLQV���������7KH�SUHVHQFH�RI�HQ]\PHV�VXFK�as malate dehydrogenase and fumarate reductase with suc-cinate as an end product, together with radiolabeling studies, FRQ¿UPHG�WKH�SUHVHQFH�RI�RQO\�D�SDUWLDO�7&$�F\FOH��RIWHQ�referred to as the succinate pathway). Furthermore, the abo-lition of fumarate reductase activity by inhibitors such as ��Q�KHSW\O���K\GUR[\TXLQROLQH�N-oxide, and the concomi-tant reduction in cytochrome, suggested that fumarate acted as an electron sink in accepting reducing equivalents from 1$'+�JHQHUDWHG� GXULQJ� FDWDEROLVP� E\�Bacteroides mela-ninogenicus �6KDK� DQG�:LOOLDPV�� ����D�� ����E��$O�-DOLOL�DQG�6KDK�������� 7KHVH�UHVXOWV�FRQ¿UPHG�EH\RQG�GRXEW�WKDW�more than one mechanism of energy conservation existed in anaerobic bacteria and helped to explain its dependence on KHPH� �IRU� WKH�SURVWKHWLF�SRUSK\ULQV�� DQG�PHQDGLRQH� �YLWD-PLQ�.�) for menaquinones biosynthesis which are naturally DFTXLUHG�LQ�WKH�LQWHVWLQDO�WUDFW��'LIIHUHQFHV�LQ�S+�RSWLPD�DQG�enzyme stabilities of the Bacteroides melaninogenicus sub-species further emphasized the heterogeneity of this group �6KDK�DQG�:LOOLDPV��������6KDK��������

6WXGLHV�RI� WKH�PRO��*�&�FRQWHQW�DQG�PXOWLORFXV�HQ]\PH�electrophoresis of these groups revealed considerable het-HURJHQHLW\�ZLWK�WKLV�WD[RQ��7KH�VDFFKDURO\WLF��Bacteroides melaninogenicus subsp. melaninogenicus) resolved into WKUHH� JURXSV�� WKH� PRGHUDWHO\� VDFFKDURO\WLF� �Bacteroides

melaninogenicus subsp. intermedius) into two clusters while the nonfermentative strains were delineated into three DGGLWLRQDO�JURXSV�LQ�DFFRUG�ZLWK�WKHLU�PHQDTXLQRQH�SUR¿OHV��)LJXUH����DQG�'1$±'1$�UHDVVRFLDWLRQ�VWXGLHV�HYHQWXDOO\�led to establishment of these clusters as eight distinct spe-FLHV��%HUJH\¶V��������

&ODUL¿FDWLRQ� RI� WKH� WD[RQRP\� RI� WKLV� JURXS� UHSUHVHQWV� DQ�excellent example of the immense value of systematics in UHYHDOLQJ�WKH�VLWH�VSHFL¿FLW\�DQG�KHQFH�WKH�SRWHQWLDO�FRQWUL-EXWLRQ�RI�D�SDUWLFXODU�VSHFLHV�WR�GLVHDVH��(DUOLHU��0DF'RQDOG�HW� DO�� ������� DQG� 6RFUDQVN\� DQG� *LEERQV� ������� GHPRQ-strated that “Bacteroides melaninogenicus” was an essential FRPSRQHQW�RI�WKH�ÀRUD�RI�PL[HG�LQIHFWLRQV�XVLQJ�D�JXLQHD�SLJ�PRGHO��6LPLODU�H[SHULPHQWV�ZHUH�QRW�UHSURGXFLEOH�VXE-sequently and were attributed to differences in strains used. 2YHU� WKH� \HDUV�� LW� EHFDPH� DSSDUHQW� WKDW� WKH� VDFFKDURO\WLF�strains appear to be less virulent and more associated with WKH� QRUPDO� ÀRUD�� %\� FRQWUDVW�� WKH� DVDFFKDURO\WLF� VSHFLHV�such as Porphyromonas gingivalis, Porphyromonas asac-charolytica, and Porphyromonas endodontalis possess a large number of virulence determinants and were reported

������������������������� �������������������������������������� �����������������������������������

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Figure 2. DNA base composition against the electro-phorectic mobility of malate dehydrogenase of the Bacteroides melaninogenicus” complex. (Adapted from Shah et al., 1976.) Red – saccharolytic strains that were eventually assigned to (1) Bacteroides melaninogenicus, (2) Bacteroides denticola, and (3) Bacteroides loescheii. Purple – moderately saccharolytic strains that were later proposed as two distinct species, (4) Bacteroides intermedius and (5) Bacteroides nigrescens. Green – non-fermentative strains that subsequently became (6) Bacteroides gingivalis, (7) Bacteroides asaccharolyticus, and (8) Bacteroides endodontalis.

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94 The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

more widely from infections. Today as direct molecular analysis of mixed infections are undertaken, combinations involving nonfermentative strains appear to substantiate the ZRUN�RI�0DF'RQDOG�HW� DO�� �������DQG�6RFUDQVN\�DQG�*LE-ERQV��������DQG�VXJJHVW�WKDW�WKHLU�VWUDLQ�PD\�KDYH�EHHQ�DQ�DVDFFKDURO\WLF�LVRODWH��0RUH�GLUHFWO\�Porphyromonas gingi-valis��GHOLQHDWHG�IURP�WKLV�FRPSOH[��)LJXUH�����LV�VSHFL¿F�WR�the oral cavity and considered a key component of periodon-tal disease and this facilitated detailed studies into its patho-genic mechanisms. For example, the vesicle-bound cysteine proteinase of Porphyromonas gingivalis�³JLQJLYDLQ´��6KDK�HW�DO���������ZDV�VKRZQ�WR�EH�D�SRWHQW�WLVVXH�DQG�FHOOXODU�GH-structive enzyme and considerable work has been devoted to elucidating its biological role. Porphyromonas gingivalis is a nonfermentative species whose growth requirements DUH�PDUNHGO\�LQÀXHQFHG�E\�WKH�SUHVHQFH�RI�SHSWLGHV��6KDK��������� ,W� VHHPV� OLNHO\� WKDW� in vivo these micro-vesicles, which are drawn into the interstitial spaces of the tissues, hydrolyze native proteins to release peptides/amino acids to maintain the growth of cells. Consequently, current thera-peutic strategies are being focused on inhibiting proteolysis.

Bacteroides fragilis, the type species and other non-pigmented “bacteroides”

$URXQG� WKH�SHULRG� IURP������ WR�������ZKLOH�RUDO�PLFUREL-ologists worked almost exclusively on pigmented species, intestinal and rumen scientists focused largely on Bacteroi-des fragils and Bacteroides ruminicola, respectively. Com-parative studies of the Bacteroides melaninogenicus, Bacte-roides fragilis, and Bacteroides ruminicola groups revealed YDVW�GLIIHUHQFHV�LQ�ELRFKHPLFDO�DQG�FKHPLFDO�SURSHUWLHV��VHH�6KDK������������D���7KH�PRVW�VWULNLQJ�GLIIHUHQFHV�ZHUH�LQ�WKHLU�'1$�EDVH�FRPSRVLWLRQV��DSSUR[����±���PRO��*�&��ZKLFK�LV�DOPRVW�DV�GLYHUVH�DV�WKH�EDFWHULDO�NLQJGRP��+RZHY-er, the majority, including the type species Bacteroides fra-gilis��KDG�'1$�EDVH�FRPSRVLWLRQV�ZLWKLQ� WKH�DSSUR[LPDWH�OLPLWLQJ�UDQJH�RI���±���PRO��DQG�DSSHDUHG�WR�FRPSULVH�WKH�QXFOHXV�RI� WKH�JHQXV��2WKHUV�VXFK�DV�Bacteroides praeacu-tus, Bacteroides hypermegas, Bacteroides furcosus, and Bacteroides ureolyticus, etc., were similar to fusobacteria in SRVVHVVLQJ�'1$�EDVH�FRPSRVLWLRQV�RI�a���PRO��*�&��$W�the extreme limits were other species such as Bacteroides capillosus, Bacteroides multiacidus, and Bacteroides micro-fusus�WKDW�SRVVHVVHG�EDVH�FRPSRVLWLRQV�RI�a���PRO��*�&�

Figure 3. Narrow range (pH 4.5–6.0) isoelectric-focusing of proteins of strains designated “Bacteroides oralis” and their relatedness by DNA–DNA reassociation (given above each lane). (From Shah et al., 1982.) The lane without a number is 3+�ODEHOHG�'1$�UHIHUHQFH�SUREH��7KHVH�UHVROYHG�LQWR�ÀYH�JURXSV�D�VKRZQ�DERYH��IURP�OHIW�WR�ULJKW������Oral isolates that were phenotypically similar to Bacteroides ruminicola – subsequently proposed as Bacteroides pentosaceus (=Bacteroides buccae). (2). Two strains designated Bacteroides oralis that shared 94% reassociation; eventually proposed as Bacteroides buccalis. (3). Saccharolytic strains of Bacteroides melaninogenicus, one of which had only 10% DNA–DNA reassociation and became Bacteroides loescheii. 4. Strains that were also phenotypi-cally similar to Bacteroides oralis (in group 2) but did not hybridize with these strains; a new species Bacteroides oulorum was created for these. (5). The 3H-labeled reference DNA of the type strain of Bacteroides oralis, strain �&0�VKRZHG�KLJK�DIÀQLW\�ZLWK�Bacteroides vulgatus and was transferred to this species.

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Haroun N. Shah and Saheer E. Gharbia

The Bulletin of BISMiS

To further study their diversity, systematic analysis of these groups were undertaken with particular emphasis on the analysis of their long-chained cellular fatty acids and respi-UDWRU\�TXLQRQHV��VHH�H�J��6KDK�DQG�&ROOLQV���������7KH�QRQ�K\GUR[\ODWHG�IDWW\�DFLGV�RI�VSHFLHV�ZLWK�PRO��*�&�FRQWHQWV�RI���±���PRO��FRQVLVWHG�SUHGRPLQDQWO\�RI� VWUDLJKW�FKDLQ��anteiso- and iso-PHWK\O� EUDQFKHG�FKDLQ� DFLGV��PRQRXQVDW-urated fatty acids were found in only small amounts. The major fatty acids of species such as Bacteroides ochraceus, Bacteroides distasonis, and Bacteroides splanchnicus and the asaccharolytic subspecies of Bacteroides melaninogeni-cus ZDV����PHWK\OWHWUDGHFDQRLF�DFLG��&�� iso) whereas the saccharolytic subspecies of Bacteroides melaninogenicus and oral isolates that were phenotypically similar to the Bacteroides ruminicola and Bacteroides fragilis groups pos-VHVVHG� PDLQO\� ���PHWK\O�WHWUDGHFDQRLF� DFLG� �&�� anteiso). Interestingly, the rumen strains of “Bacteroides” �viz. Bacte-roides ruminicola subsp. ruminicola and Bacteroides rumi-nicola subsp. brevis) were characterized by major levels of C���DQWHLVR�DQG�SHQWDGHFDQRLF��&����) fatty acids.

0HQDTXLQRQHV�ZHUH� WKH� RQO\� LVRSUHQRLG� TXLQRQHV� SUHVHQW�among all taxa with most species possessing menaquinones ZLWK�EHWZHHQ����DQG���� LVRSUHQH�XQLWV� �6KDK�DQG�&ROOLQV���������������7KH�PRVW�XQXVXDO�ZDV�WKH�FDSQRSKLOLF�VSHFLHV��Bacteroides ochraceus which contained menaquinones with VL[�LVRSUHQH�XQLWV�DQG�ZDV�VXEVHTXHQWO\�UHFODVVL¿HG�LQ�WKH�genus Capnocytophaga �/HDGEHWWHU�HW�DO���������&ROOLQV�HW�DO��� �������7KH�Bacteroides fragilis group of species was characterized by comparable amounts of menaquinones ZLWK���� DQG���� LVRSUHQH�XQLWV�ZKHUHDV� WKH� UXPHQ� VSHFLHV��Bacteroides ruminicola subsp. ruminicola and Bacteroides ruminicola subsp. brevis� KDG� PDLQO\� ��� DQG� ��� LVRSUHQH�XQLWV�� 2UDO� LVRODWHV� WKDW� ZHUH� SKHQRW\SLFDOO\� VLPLODU� WR�Bacteroides ruminicola possessed high amounts of mena-TXLQRQHV�ZLWK����DQG����LVRSUHQH�XQLWV��6KDK�DQG�&ROOLQV��������'1$�EDVH� FRPSRVLWLRQV� VXEGLYLGHG� WKH� JHQXV� LQWR�D� ORZ�*�&� JURXS� �a���PRO���� D� KLJK�*�&� JURXS� RI� ���PRO��� DQG�� D� WKLUG� LQWHUPHGLDWH� JURXS� RI� DSSUR[LPDWHO\���±���PRO��*�&��PDQ\�RI�ZKLFK�DSSHDU�WR�SRVVHVV�FRQVLG-erable biochemical and chemical heterogeneity. The latter contained the type species, Bacteroides fragilis hence taxo-nomic studies focussed largely on this group.

5HGHÀQLWLRQ�DQG�LWV�LPSDFW�RQ�WKH�ELRORJ\�of the group with particular reference to mid-range mol% G+C group

3K\VLRORJLFDOO\�� ³Bacteroides” species are metabolically versatile, being able to utilize nitrogenous substrates such as aspartate and glutamate but vary in their capacity to metabo-lize carbohydrates. They appear to lack functional enzymes

IRU�D�FRPSOHWH�7ULFDUER[\OLF�$FLG�&\FOH�EXW�KDYH�D�SDUWLDO�system that leads to succinate as an end product of metabo-OLVP��0DODWH�LV�DQ�LQWHUPHGLDWH�RI�WKLV�SDWKZD\�KHQFH�PDODWH�dehydrogenase is universally detected as is glutamate dehy-GURJHQDVH�IURP�JOXWDPDWH�PHWDEROLVP��6KDK�DQG�:LOOLDPV���������6XFK�GLYHUVH�SK\VLRORJLFDO�GLIIHUHQFHV��WRJHWKHU�ZLWK�supporting genomic and phenotypic data made it increas-LQJO\�GLI¿FXOW�WR�UHWDLQ�WKLV�GLYHUVH�JURXS�DV�D�VLQJOH�JHQXV��Thus, taxonomic changes, resisted so long and retained up WR�WKH��VW�HGLWLRQ�RI�WKH�QHZ�Bergey’s Manual of Systematic Bacteriology���������ZHUH�LQHYLWDEOH��,Q�������D�UHYLHZ�RI�WKH�JHQXV�ZDV�XQGHUWDNHQ�DQG�D�QHZ�GH¿QLWLRQ�ZDV�SURSRVHG�that recognized only species that were biochemically close-ly related to Bacteroides fragilis��WKH�W\SH�VSHFLHV��6KDK�DQG�&ROOLQV���������$�FRPSLODWLRQ�RI�WKH�NQRZQ�SURSHUWLHV�RI�WKH�JURXS�OHG�WR� WKH�IROORZLQJ�UHGH¿QLWLRQ�RI� WKH�JHQXV�Bacte-roides EDVHG�XSRQ�WKH�IROORZLQJ�FULWHULD�

�� 3URGXFH�PDMRU�DPRXQWV�RI�VXFFLQLF�DQG�RU��EXW\ULF�DFLGV��WRJHWKHU�ZLWK�VXEVWDQWLDO�OHYHOV�RI�DFHWLF�DQG�RF-FDVLRQDOO\�RWKHU�VKRUW�FKDLQ�DFLGV�

�� Contain malate dehydrogenase and glutamate GHK\GURJHQDVH�

�� 3RVVHVV�'1$�EDVH�FRPSRVLWLRQ�ZLWKLQ�WKH�DSSUR[LPDWH�OLPLWLQJ�UDQJH�RI���±���PRO��*�&�

�� 3RVVHVV�VSKLQJROLSLGV�

�� 3URGXFH�PDMRU�DPRXQWV�RI�VWUDLJKW�FKDLQ�VDWXUDWHG��LVR�DQG�DQWHLVR�PHWK\O�EUDQFKHG�ORQJ�FKDLQ�IDWW\�DFLGV�

�� Contain menaquinones as the sole respiratory quinones.

7KLV�QHZ�GH¿QLWLRQ�DOORZHG�WKH�UHWHQWLRQ�RI�WKH�Bacteroides fragilis group of species and the pigmented/non-pigmented species that are biochemically related to Bacteroides mela-ninogenicus��+RZHYHU��ZLWKLQ�WKLV�PRUH�UHVWULFWHG�GH¿QLWLRQ��WKUHH�JURXSV�ZHUH�FOHDUO\�DSSDUHQW�

(1) Highly saccharolytic species: e.g. Bacteroides fragilis and closely related taxa metabolize a range of sugars, have a functional glycolytic pathway and possess enzymes of the KH[RVH� PRQRSKRVSKDWH� SDWKZD\� VXFK� DV� JOXFRVH���SKRV-SKDWH� GHK\GURJHQDVH� DQG� ��SKRVKRJOXFRQDWH� GHK\GURJH-QDVH��0DODWH�GHK\GURJHQDVH�DQG�JOXWDPDWH�GHK\GURJHQDVH�are present in all species of the “Bacteroides fragilis group”. $OO�JURZ�LQ�WKH�SUHVHQFH�RI�ELOH��7KH\�ZHUH�UHFODVVL¿HG�DV�the genus Bacteroides sensu stricto �6KDK�DQG�&ROOLQV��������

(2) Moderately saccharolytic species: Bacteroides mela-ninogenicus, Bacteroides intermedius, Bacteroides oralis, Bacteroides buccalis, and Bacteroides denticola, etc. These

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A century of systematics of the genus Bacteroides: from a single genus up to the 1980s to an explosion of assemblages and the dawn of MALDI-TOF-Mass Spectrometry

The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

metabolize a limited range of carbohydrates that includes PXFLQV�� ,QWHUHVWLQJO\�� WKH\� ODFN�JOXFRVH���SKRVSKDWH�GHK\-GURJHQDVH� DQG� ��SKRVKRJOXFRQDWH� GHK\GURJHQDVH� EXW� SRV-sess both malate dehydrogenase and glutamate dehydroge-QDVH��*URZWK�LV�LQKLELWHG�E\�ELOH��7KH\�ZHUH�SODFHG�LQ�WKH�genus Prevotella��6KDK�DQG�&ROOLQV��������

(3) Asaccharolytic species: Bacteroides asaccharolyticus and Bacteroides gingivalis, etc. Radiolabeling studies with ��C-glucose revealed that although glucose was taken up, it remained in cell wall polymers and not present in their PHWDEROLF�HQG�SURGXFWV��6KDK�DQG�:LOOLDPV������E���6RPH�species metabolize a limited range of carbohydrates that LQFOXGHV�PXFLQV�� 7KH\� ODFN� JOXFRVH���SKRVSKDWH� GHK\GUR-JHQDVH�DQG���SKRVKRJOXFRQDWH�GHK\GURJHQDVH�EXW�SRVVHVV�both malate dehydrogenase and glutamate dehydrogenase.

7KHVH� ZHUH� UHFODVVL¿HG� LQ� D� QHZ� JHQXV�� Porphyromonas �6KDK�DQG�&ROOLQV��������

These proposals left the following species incertae sedis��Bacteroides amylophilus, Bacteroides capillosus, Bacteroi-des coagulans, Bacteroides furcosus, Bacteroides hyperme-gas, Bacteroides microfusus, Bacteroides multiacidus, Bac-teroides nodosus, Bacteroides pneumosintes, Bacteroides praeacutus, Bacteroides putredinis, Bacteroides succino-genes, Bacteroides termitidis, and Bacteroides ureolyticus. These species were so incompatible with other members that subsequent work over the following two decades failed WR�UHWDLQ�D�VLQJOH�VSHFLHV�ZLWKLQ�WKH�WKUHH�QHZ�JHQHUD��0DQ\�were displaced into very distant lineages in one of the most radical taxonomic changes witnessed within a genus that hitherto comprised an established group that dates back to

Table 2.�5HGHÀQLWLRQ�RI�WKH�JHQXV�Bacteroides (Shah and Collins, 1983) excluded a vast number of species that remain incertae sedis even up to the current edition of Bergey’s Manual (2011) – furthermore, many of these taxa ZHUH�IRXQG�WR�EH�VR�XQLTXH�WKDW�VHYHUDO�KDYH�UHWDLQHG�WKHLU�VWDWXV�DV�PRQRVSHFLÀF�JHQHUD

“Bacteroides species” Taxonomic designation following UHGHÀQLWLRQ

Current status (phylum/family/genus)

Bacteroides amylophilus Ruminobacter amylophilus Gammaproteobacteria/Succinivibronaceae/Rumi-nobacter

Bacteroides capillosus Bacteroides capillosus (3VHXGRÁDYRQLIUDFWRU�capillosus); closest relatives: Clostridium orbiscindens and Eubacterium plautii

Firmicutes/Clostridiaceae/3VHXGRÁDYRQLIUDFWRU

Bacteroides coagulans Bacteroides coagulans �PLVFODVVLÀHG� Bacteroidetes/Bacteroidaceae/Bacteroides

Bacteroides furcosus Anaerorhabdus furcosa Bacteroidetes/Bacteroidaceae/Anaerorhabdus

Bacteroides hypermegas Megamonas hypermegas �QRW�RIÀFLOOD\�DV-signed a family)

Firmicutes/Veillonellaceae/Megamonas

Bacteroides microfusus Rikenella microfusus Bacteroidetes/Rikenellaceae/Rikenella

Bacteroides multiacidus Mitsuokella multiacida Firmicutes/Veillonellaceae/Mitsuokella

Bacteroides nodosus Dichelobacter nodosus Gammaproteobacteria/Cardiobacteriaceae/Dich-elobacter

Bacteroides pneumosintes Dialister pneumosintes Firmicutes/Veillonellaceae/Dialister

Bacteroides praeacutus Tissierella praeacuta Firmicutes/Family XI incertae sedis/Tissierella

Bacteroides putredinis Alistipes putredinis Bacteroidetes/Rikenellaceae/Alistipes

Bacteroides ruminicola Prevotella ruminicola Firmicutes/Prevotellaceae/Prevotella

Bacteroides succinogenes Fibrobacter succinogenes Fibrobacteres/Fibrobacteraceae/Fibrobacter

Bacteroides termitidis Sebaldella termitidis Fusobacteria/Leptotrichiaceae/Sebaldella

Bacteroides ureolyticus Bacteroides ureolyticus �PLVFODVVLÀHG� Proteobacteria (delta/epsilon)/Campylobactera-ceae/Campylobacter

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� Asaccharolytic� Visible porphyrins on blood agar� Major menaquinone: MK-9� LCFA: major: C15:0 iso

� DeH2: MDH, GDH

� Highly saccharolytic� No visible porphyrins on blood agar� Major menaquinones: MK-11, -10� LCFA: major: C15:0 anteiso

� DeH2: MDH, GDH, G6PDH, 6PGDH

� Moderately saccharolytic� Visible porphyrins on blood agar in most

species� Major menaquinones: MK-11, -13� LCFA: major: C15:0 anteiso

� DeH2: MDH, GDH

Figure 4. Early 16S rRNA tree and its correlation with key biochemical and chemotaxonomic data. The three clusters, Bacteroides sensu stricto, Prevotella and Porphyromonas (Shah and Collins, 1988, 1989 and 1990) were proposed ahead of 16S rRNA gene sequence analysis (adapted from Shah et al., 1998). Abbreviations: LCFA; long-chained fatty acid; DeH2: dehydrogenase; MDH, malate dehydrogenase; GDH, glutamate dehydrogenase; G6PDH, glucose-6-phosphate dehydrogenase; 6PGDH, 6-phoshogluconate dehydrogenase.

WKH� �VW� HGLWLRQ� RI�Bergey’s Manual� �%HUJH\� HW� DO��� �������6RPH� VSHFLHV�ZHUH� HYHQ� UHFRYHUHG� DPRQJ�*UDP�SRVLWLYH�WD[D��H�J��Clostridiaceae), various lineages within the Pro-teobacteria and Firmicutes, while new orders and families were created to accommodate some such as Bacteroides succinogenes �Fibrobacteres���VHH�VXPPDU\�LQ�7DEOH���

The impact of molecular systematics on restructuring of Bacteroides and related taxa

&RPSDUDWLYH�'1$�VHTXHQFLQJ�DQDO\VLV�RI�WKH�VPDOO�VXEXQLW�U51$� ���6� U51$�� EHFDPH� WKH� GULYLQJ� IRUFH� RI� EDFWHULDO�V\VWHPDWLFV� LQ� WKH� HDUO\� ����V� DQG� QHDUO\� DOO� WD[RQRPLF�FKDQJHV� QHFHVVLWDWHG� LWV� DSSOLFDWLRQ�� 3URSRVDOV� WR� UHVWUXF-

ture the “Bacteroides” ZDV�GRQH�SULRU� WR�FRPSDUDWLYH���6�U51$� JHQH� VHTXHQFH� DQDO\VLV�� FRQVHTXHQWO\� WKH� VWUHQJWK�of the proposed changes would be scrupulously challenged LQ�WKH�HQVXLQJ�\HDUV��)LJXUH���VKRZV�JRRG�FRQFRUGDQFH�EH-tween the key biochemical/chemical features used to cir-cumscribe the three groups of “Bacteroides” into the new JHQHUD�DQG�WKH�LQLWLDO�GDWD�REWDLQHG�E\���6�U51$��6KDK�HW�DO����������+RZHYHU��WKLV�ZDV�MXVW�WKH�LQLWLDO�SKDVH�RI�DQ�H[-WHQVLYH�OLWHUDWXUH�WKDW�IROORZHG��VHH�H�J��3DVWHU�HW�DO���������6DNDPRWR�DQG�2KNXPD��������������6DNDPRWR�HW�DO���������*XSWD�� ������*XSWD� DQG�/RUHQ]LQL�� ������� FXOPLQDWLQJ� LQ�their acceptance in Bergey’s Manual of Systematic Bacte-riology� ������� DQG�ZLWQHVVHG� WKH� UHPDUNDEOH� HOHYDWLRQ� RI�some of these taxa from species/subspecies to family level. 0RVW�VWULNLQJ�ZDV�WKH�GLVSODFHPHQW�RI�PDQ\�WD[D�WKDW�ZHUH�

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A century of systematics of the genus Bacteroides

KLWKHUWR�H[FOXGHG�IURP�WKH�UHGH¿QHG�JHQXV��6KDK�DQG�&RO-OLQV��������WR�YHU\�GLVWDQW�OLQHDJHV��VHH�7DEOH�����7KH�DUULYDO�RI�3&5�DQG�WKH�HDVH�DQG�VLPSOLFLW\�ZLWK�ZKLFK�FRPSDUDWLYH���6�U51$�VHTXHQFLQJ�FRXOG�EH�DFKLHYHG�OHG�WR�ODUJH�QXP-bers of species periodically being added to each of the newly SURSRVHG�JHQHUD��7KXV��ZKHUHDV�WKH��VW�HGLWLRQ�RI�Bergey’s Manual of Systematic Bacteriology��������OLVWHG����VSHFLHV��WKH�FXUUHQW�HGLWLRQ��������OLVWV����VSHFLHV�LQ�WKUHH�JHQHUD�DV�IROORZV�� ��� VSHFLHV� DV�Bacteroides� �SOXV� HLJKW� ODEHOHG� in-certae sedis��� ��� DV�Prevotella� VSHFLHV�� DQG���� DV�Porphy-romas species. The remainder are dispersed into immensely GLYHUVH�OLQHDJHV�DQG�DUH�VXPPDUL]HG�LQ�7DEOH���

The topology of the phylogenetic tree using compara-tive sequencing alignment of several gene targets such as hsp60��6DNDPRWR�DQG�2KNXPD���������gyrB �/HH�DQG�/HH��������� rpoB �.R� HW� DO��� ������� HWF���PLUURUV� WKRVH� GHULYHG�E\���6�U51$��0RUH�UHFHQWO\�PXOWLORFXV�VHTXHQFH�DQDO\VLV�of internal fragments of the gene targets dnaJ, gyrB, hsp60, recA, rpoB��DQG���6�U51$�ZHUH�FRQFDWHQDWHG�DQG�YDULRXV�algorithms used to test the robustness of the phylogenetic relationships among Bacteroides VSHFLHV� �6DNDPRWR� DQG�2KNXPD�� �������7KH� OHYHO� RI� GLVFULPLQDWLRQ� EHWZHHQ� VSH-cies was greater compared with single-gene trees and a level RI�������JHQH�VHTXHQFH�VLPLODULW\��EDVHG�RQ�WKH�IUDJPHQWV�of these six genes, was used to demarcate members of the genus Bacteroides sensu stricto. In future, such work may EH�VLPSOL¿HG�VLQFH�FRQFDWHQDWLRQ�RI�WKUHH�JHQH�WDUJHWV�DORQH��dnaJ, gyrB, and hsp60��SDUDOOHOHG� WKH�DERYH� UHVXOWV� �6DND-PRWR�DQG�2KNXPD���������,QWHUHVWLQJO\��WKH�gyrB gene was IRXQG�WR�EH�WD[RQRPLFDOO\�WKH�PRVW�LQIRUPDWLYH��$W�KLJKHU�taxonomic rank, the branching of these lineages were sub-VWDQWLDWHG�XVLQJ�LQGHOV�WKDW�FRUUHODWH�ZLWK�WKH�'1$�*\UDVH�%�SURWHLQ��$���DPLQR�DFLG� LQVHUW� LQ�*\U%�DQG�D����DPLQR��DFLG�LQVHUW�LQ�WKH�6HF$�SURWHLQV�ZHUH�XQLTXHO\�VKDUHG�E\�WKLV�group of species and clearly differentiated them from other SK\OD��*XSWD�HW�DO���������������

The wealth of molecular systematic data over the last decade KDV�HVWDEOLVK�EH\RQG�GRXEW�KLJK�FRQ¿GHQFH�LQ�WKH�WD[RQRP-LF�VWUXFWXUH�RI�WKLV�JURXS��+RZHYHU��PRVW�RI�WKH�ELRFKHPLFDO�FKHPLFDO�DQG��PROHFXODU�WHFKQLTXHV�VXFK�DV�'1$±'1$�UH-association that initially revealed the immense heterogeneity of this group are now outside the realms of most laboratories. 3KHQRW\SLF�WHVWV�UHYHDO�H[SUHVVLRQ�DQG�DV�VXFK�DUH�VWLOO�SUDJ-PDWLF� FKDUDFWHUV� IRU� WKH� LGHQWL¿FDWLRQ�RI�ZLOG�W\SH� VWUDLQV�and variants and help elucidate the inherent diversity of a taxon. This is exacerbated where taxa are non-fermentative since traditional biochemical tests, based on carbohydrate IHUPHQWDWLRQ�UHDFWLRQV�DUH�IXWLOH��1HZ�DSSURDFKHV�EDVHG�RQ�the proteome represent a cornucopia of biomolecules that KDYH� QRW� EHHQ� V\VWHPDWLFDOO\� H[SORUHG�� 0HWKRGV� VXFK� DV�

PXOWLORFXV� HQ]\PH� HOHFWURSKRUHVLV�� 6'6�3$*(� DQG� ÀDW�EHG�,()��VHH��H�J��)LJXUH����)LJXUH���DQG�6ZLQGOHKXUVW�HW�DO����������KDYH�SURYLGHG�FRPSHOOLQJ�SURRI�RI�FRQFHSW�RI�WKHLU�value for microbial systematics but the technology for high-WKURXJKSXW�LGHQWL¿FDWLRQ�RI�GLVFULPLQDWRU\�PDUNHU�SURWHLQV�had to await the arrival of new forms of mass spectrometry �06�� VXFK� DV� PDWUL[�DVVLVWHG� ODVHU� GHVRUSWLRQ�LRQL]DWLRQ�WLPH�RI�ÀLJKW� PDVV� VSHFWURPHWU\� �0$/',�72)�06�� DQG�liquid chromatography-mass spectrometry/mass spectrom-HWU\��/&�06�06���0$/',�72)�06�LV� WRGD\�EHLQJ�HVWDE-lished as a reliable adjunct to molecular-based methods and some of its pioneering developments were entrenched in ap-plications to seek new characters for the delineation of non-IHUPHQWDWLYH�SRRUO\� GH¿QHG� WD[D� VXFK� DV� Porphyromonas, Prevotella, and Bacteroides.

Mass spectral analysis of “Bacteroides” and the dawn of MALDI-TOF-MS

'XULQJ�WKH�ÀRXULVKLQJ�HUD�RI�FKHPRWD[RQRP\�DURXQG�WKH�����V��06�DQDO\VLV�RI�FHOOXODU�FRPSRQHQWV�VXFK�DV�porphyrins, respiratory quinones, long-chain cellular fatty DFLGV��JDV�FKURPDWRJUDSK\�06��06��H�J��6KDK�DQG�&RO-OLQV���������SRODU�OLSLGV��)DVW�$WRPLF�%RPEDUGPHQW�06��H�J��'UXNHU�HW�DO���������RU�ZKROH�FHOO�SUR¿OHV�E\�3\URO\VLV�PDVV�VSHFWURPHWU\��H�J��*XWWHULGJH�HW�DO���������ZHUH�H[-tensively reported for “Bacteroides´��+RZHYHU��D�OLPLWD-tion of these methods was their inability to analyze large biomolecules such as proteins.

7KXV��ZKHUHDV�HDUOLHU�06�PHWKRGV�ZHUH� OLPLWHG� WR� LRQL]D-WLRQ�RI�VPDOO�PROHFXOHV��������'D��VXFK�DV�PHQDTXLQRQHV��QHZ�06�PHWKRGV� VXFK� DV�0$/',�72)�06� DQG� /&�06�06�theoretically had no upper limit.

,Q�WKH�HDUO\�DSSOLFDWLRQV�RI�0$/',�72)�06��QXPHURXV�SD-rameters needed optimization to obtain reproducible spec-WUDO�SUR¿OHV��7KXV��VDPSOH�SUHSDUDWLRQ��WKH�GHVLJQ�RI�WKH�06�target plate for spotting the analyte, the type, concentration and method of application of the matrix solution used for ionization, cultural conditions such as the medium composi-WLRQ��WHPSHUDWXUH��S+��DJH�RI�WKH�FXOWXUH��VWUDLQ�YDULDWLRQ�HWF�WRJHWKHU�ZLWK�06�SDUDPHWHUV�VXFK�DV�ODVHU�HQHUJ\��UHSURGXF-ibility between instruments and the application of various algorithms for data analysis all required considerable re-search to eventually establish a standardized protocol. In our SUHDPEOH�WR�DVVHPEOH�D�PLFURELDO�GDWDEDVH�RI�06�SUR¿OHV��we hypothesized that since many virulence determinants of pathogenic microbes are surface-associated, a database RI�06�SUR¿OHV�EDVHG�RQ� WKHVH�PROHFXOHV�ZRXOG� VHUYH� WKH�GXDO� SXUSRVH� RI� SURYLGLQJ� XQLTXH� VSHFLHV�VSHFL¿F� VLJQD-WXUHV�ZKLOH�DOVR�KLJKOLJKWLQJ�SDWKRJHQLF�YDULDQWV��3URRI�RI�

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principle was established by being able to delineate smooth �YLUXOHQW��DQG�URXJK��EHJXLQH��YDULDQWV�RI�Peptostreptococ-cus micros �5DMHQGUDP��������

+RZHYHU�� FXOWXUH� FRQGLWLRQV�PDUNHGO\� DIIHFWV� WKH� VXUIDFH�composition of cells and, for the same strain different spec-WUDO�SUR¿OHV�ZHUH�REWDLQHG� �VHH�� H�J��)LJXUH����6KDK�HW� DO����������,Q�RUGHU�WR�GHYHORS�D�VWDQGDUG�SURWRFRO�WKDW�FRXOG�EH�used for all bacteria, considerable in-depth analysis was un-dertaken using a broad range of bacterial species to establish D�GDWDEDVH�RI�PDLQO\�W\SH�DQG�UHIHUHQFH�VWUDLQV�RI�VRPH�����VSHFLHV�IURP�WKH�1DWLRQDO�&ROOHFWLRQ�RI�7\SH�&XOWXUHV��VHH��H�J��.H\V�HW�DO���������

$�ZDWHUVKHG� LQ� WKH� GHYHORSPHQW� RI� WKLV�ZRUN�ZDV� WKH� GH-lineation of species of the genus Porphyromonas which provided unequivocal support for pursuing this approach �6KDK� HW� DO��� ������� 6LQFH�PHPEHUV� RI� WKLV� JHQXV� DUH� YLU-WXDOO\� LQGLVWLQJXLVKDEOH� H[FHSW� E\� '1$±'1$� UHDVVRFLD-WLRQ�� WKHLU� XQDPELJXRXV� VHSDUDWLRQ� E\� 0$/',�72)�06�heralded a new simple approach to study the systematics of VXFK�SRRUO\�FKDUDFWHUL]HG�WD[D��VHH��H�J��)LJXUH����6KDK�HW�DO����������7KLV�ZRUN�ZDV�H[WHQGHG�WR�LQFOXGH�VHYHUDO�RWKHU�genera where they was a paucity of reliable characters for GHOLQHDWLQJ�VSHFLHV��.H\V�HW�DO���������

7KH�PHWKRG�ZDV�WULDOOHG�LQ�D�FOLQLFDO�ODERUDWRU\�LQ�����±�����DQG�ZKLOH� LW�ZDV�VXFFHVVIXO� IRU�Staphylococcus au-reus� �5DMDNXUDQD� HW� DO�� ������� &ORVWULGLXP� GLI¿FLOH iso-lates were poorly differentiated. The latter was resolved by changing the matrix solution from ��FKORUR���PHU-FDSWREHQ]RWKLD]ROH� �&0%7�� to ����GLK\GUR[\� EHQ]RLF�DFLG� LQ� DFHWRQLWULOH�HWKDQRO�ZDWHU� �������� ZLWK� ������7)$ ZKLFK�KDG�WKH�EHQH¿FLDO�HIIHFW�RI�VKLIWLQJ�WKH�PDVV�VSHF-WUDO� SUR¿OH� DZD\� IURP�VXUIDFH�DVVRFLDWHG� WR� LQWUDFHOOXODU�PROHFXOHV� �PDLQO\� ULERVRPDO�SURWHLQV��DQG� UHVXOWHG� LQ�D�dramatic improvement in the stability of the spectral ions. Thus, whereas before it was necessary to culture cells on a single medium under standardized conditions to obtain D� UHSURGXFLEOH�PDVV� VSHFWUDO�SUR¿OH�� FHOOV�FRXOG�QRZ�EH�cultured on any medium and the stability of the ribosomal SURWHLQV�SHUPLWWHG�WKHLU�LGHQWL¿FDWLRQ�WR�WKH�VSHFLHV�OHYHO��VHH� UHYLHZ� .DOORZ� HW� DO��� ������� 6LJQL¿FDQW� GHYHORS-ments in the hardware and software by mass companies KDV�SURSHOOHG�0$/',�72)�06�WR�WKH�IRUHIURQW�RI�FOLQLFDO�ODERUDWRULHV� LQ�(XURSH�DQG�QRZ�UHSODFLQJ�WUDGLWLRQDO�ELR-FKHPLFDO�WHVWV�WKDW�KDYH�EHHQ�XVHG�IRU�GHFDGHV��$PRQJ�WKH�Bacteroides and related taxa, not only are species being resolved but the potential to identify antibiotic-resistant VWUDLQV�LV�HYLGHQW��1DJ\�HW�DO���������

P. catoniae - grown on FAA

P. catoniae - grown on CBA

Figure 5.�&KDQJHV�LQ�WKH�0$/',�72)�06�SURÀOH�RI�WKH�VDPH�VWUDLQ�RI Porphyromoas catoniae (NCTC 12856) grown RI�)DVWLGLRXV�$QDHURELF�$JDU��)$$��DQG�&ROXPELD�%ORRG�$JDU��&%$���0DQ\�RI�WKH�VLJQLÀFDQW�PDVV�LRQV��H�J���������������������������DQG�����'D��DUH�UHWDLQHG��+RZHYHU��VLJQLÀFDQW�PDVV�LRQV�VXFK�DV�����'D�DUH�SUHVHQW�RQO\�LQ�FHOOV�grown on CBA.

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100 The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

,Q�������WKH�¿UVW�FRQIHUHQFH�WR�H[SORUH�WKH�SRWHQWLDO�FOLQL-cal application for micro-organisms took place at the +HDOWK�3URWHFWLRQ�$JHQF\��IRUPHUO\�3XEOLF�+HDOWK�/DER-UDWRU\�6HUYLFH��/RQGRQ��VHH�)LJXUH����DQG�XVLQJ�D�VLPSOH�EDVLF�EHQFK�WRS�0$/',�72)�PDVV�VSHFWURPHWHU��WKH�VHS-aration of Porphyromonas species was demonstrated live WR�D�VFLHQWL¿F�DXGLHQFH��7KH�SRWHQWLDO�RI�WKH�WHFKQLTXH�ZDV�evident, however, it took a decade of continuous develop-ment to propel this technology to the forefront of micro-bial diagnostics. In the future, this approach is likely to be VXSHUVHGHG�E\�/&�06�06� WHFKQLTXHV� DV� WKLV�ZLOO�PDUN-HGO\�H[WHQG�LWV�DSSOLFDWLRQV�E\�SHUPLWWLQJ�LGHQWL¿FDWLRQ�RI�the protein/peptide biomarkers, pathogenic determinants, DQWLELRWLF� UHVLVWDQFH�� HWF��� LQ� D� VLQJOH� VWHS� �$O�6KDKLE� HW�DO��� ������� +RZHYHU�� OLNH�0$/',�72)�06�� WKH� IRUPHU�will require development of both hardware and software to make it more amenable for the clinical laboratory.

Coda

)URP������ZKHQ�9HLOORQ�DQG�=XEHU�¿UVW�GHVFULEHG�WKH�W\SH�species of Bacteroides, Bacteroides fragilis and paved the

way for over a century of work on these micro-organisms, their taxonomic structure today is considered robust and able to provide a sound phylogenetic framework from which to elucidate functional aspects of these species in their natural habiat. Their dominance in the intestinal track is so pronounced that several such as Bacteroides fragilis, Bacteroides thetaiotaomicron, Bacteroides vulgatus, Bacte-roides uniformis, Bacteroides distasonis, Bacteroides uni-formis��HWF���ZHUH�UHSRUWHG�EHIRUH�WKH�����V��Bergey’s Manu-als�±�%HUJH\�HW�DO���������������EHIRUH�DQDHURELF�WHFKQLTXHV�were well established. In one of the most extensive studies RI�WKH�JXW�PLFURELRPH�WRGDWH��4LQ�HW�DO���������UHSRUWHG����RI� WKH�PRVW� IUHTXHQW�PLFURELDO� JHQRPHV� DPRQJ� ���� LQGL-YLGXDOV� DQG� OLVWHG� ��� ³Bacteroides” species of which the most frequent was Bacteroides uniformis. It’s recent taxo-nomic structure further enabled new species such as Bac-teroides xylanisolvens, %DFWHURLGHV� ¿QHJROGLL, Bacteroides pectinophilus, Bacteroides intestinalis, Parabacteroides johnsonni, and Bacteroides dorei to be discerned while six groups were described only as “Bacteroides sp.”, indicat-LQJ�IXUWKHU�GLYHUVLW\�ZLWKLQ�WKLV�WD[RQ��6LPLODUO\��LQ�WKH�RUDO�cavity, several of the former “Bacteroides´��QRZ�Prevotella

P. cansulci

P. cangingivalis

P. macacae

Figure 6.�([DPSOHV�RI�WKH�GLVWLQFWLYH�0$/',�72)�06�SURÀOHV�RI�LQWDFW�FHOOV�RI�Porphyromoas sp. containing both JHQXV�VSHFLÀF��H�J������DQG�����'D�PDVV�LRQV��EXW�DOVR�D�VLJQLÀFDQW�QXPEHU�RI�VSHFLHV�VSHFLÀF�PDVV�LRQV��H[DPSOHV�indicated by arrows). Members of the genus Porphyromoas now comprise 16 species, in addition to several others whose names have not yet been validly published (Bergey’s Manual, 2011). However, with the exception of DNA–DNA reassociation, they cannot be reliably delineated. The MALDI-TOF-MS spectra shown above and those reported ear-lier (Shah et al., 2002) shows that each species can be unambiguously distinguished. It was this poorly characterized JURXS�WKDW�EHFDPH�RQH�RI�WKH�FRPSHOOLQJ�IRUFHV�IRU�WKH�GHYHORSPHQW�RI�WKLV�WHFKQLTXH�IRU�PLFURELDO�LGHQWLÀFDWLRQ�

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and Porphyromonas) that were previously reported to be VSHFL¿F� WR� WKLV�VLWH�KDYH�EHHQ�FRQ¿UPHG�E\�VWXGLHV�RI� WKH�RUDO�PLFURELRPH�XVLQJ���6� U51$� �'HZKLUVW� HW� DO��� �������ZKLOH�SURWHRPH�DQDO\VLV�UHYHDOHG�WKH�VLWH�VSHFL¿FLW\�RI�WKH�oral species, Porphyromonas gingivalis��1DQGDNXPDU�HW�DO����������7KH�ODWWHU�HPDQDWHG�IURP�RQH�RI�WKH�0/((�JURXSV�of the Bacteroides melaninogenicus complex reported some ���\HDUV�DJR��)LJXUH����6KDK�HW�DO����������UHLQIRUFLQJ�WKH�interrelationship between in-depth taxonomic studies and microbial ecology.

The biochemical properties of many species provides clues to their potential function in vivo and emphasizes the need to retain phenotypic tests as part of the description of a spe-cies. The division of the “Bacteroides” into saccharolytic, moderately saccharolytic and non-fermentative appears to be directly related to their functions in vivo. Degradation of polysaccharies is a key functional role of saccharolytic

“Bacteroides” and genome analysis of species such as Bacte-roides thetaiotaomicron������0E���Bacteroides vulgatus������0E���Bacteroides fragilis������0E��DQG�Bacteroides distaso-nis������0E��KDYH�EHHQ�H[WHQVLYHO\�VWXGLHG�DJDLQVW�D�EDFN-JURXQG� RI� WKHVH� SURSHUWLHV� �VHH�� H�J��0DJQXV� HW� DO��� ������.DUOVVRQ�HW�DO����������$OO�VSHFLHV�SRVVHVV�YHU\�KLJK�OHYHOV�of glycosidases and transglycosidases but Bacteroides the-

taiotaomicron has the most extensive array of carbohydrate HQ]\PHV��H�J��HQ]\PHV�LQYROYHG�LQ�JO\FDQ�ELRV\QWKHVLV�DQG�metabolism, N-glycan and glycosaminoglycan degradation and metabolism of galactose, glycerolipid, glycosphingolip-id, starch, pentose and glucuronate interconversions) includ-ing eight loci that are involved in capsular polysaccharide synthesis. “Bacteroides distasonis” can degrade polysac-charides but the species has the lowest capacity to do so and phylogenetically branches off the main cluster of species with lower sequence similarity and was eventually assigned to a closely related branch as Parabacteroides distasonis �6DNDPRWR� DQG�%HQQR�� ������� ,Q� WKH� JXW�� DERXW� RQH�WKLUG�RI� GLHWDU\� ¿EHU� DUH� SUHVHQW� DV� SODQW� FHOO�ZDOO� SRO\VDFFKD-rides of which xylan and arabioxylan are among the most DEXQGDQW�� 6SHFLHV� VXFK� DV�Bacteroides xylanisolvens was GLVFRYHUHG�E\�HQULFKPHQW��&KDVVDUG�HW�DO���������DQG�VKRZV�WKH�KLJKHVW�'1$�VHTXHQFH�VLPLODULW\�WR�Bacteroides ovatus, LUUHVSHFWLYH�RI�WKH�JHQH�WDUJHWV�XVHG��XQSXEOLVKHG���,QWHUHVW-ingly they both have the highest capacities to degrade xylan.

By contrast Porphyromonas� �IRUPHUO\� SDUW� RI� WKH� ³Bacte-roides”) lacks the capacity to degrade carbohydrates and in the case of Porphyromonas gingivalis, the most intensively VWXGLHG�VSHFLHV��LWV�JHQRPH�������0E��LV�RQO\�KDOI�WKH�VL]H�of that of the Bacteroides. It was shown previously that this

Figure 7.�&RQIHUHQFH�Á\HU�RI�WKH�ÀUVW�FRQIHUHQFH��������KHOG�WR�H[SORUH�WKH�SRWHQWLDO�DSSOLFDWLRQ�RI�0$/',�72)�PDVV�VSHFWURPHWU\�IRU�PLFURELDO�LGHQWLÀFDWLRQ��,W�WRRN�D�GHFDGH�RI�UHVHDUFK�DQG�GHYHORSPHQW�IRU�WKLV�WHFKQRORJ\�WR�gain widespread acceptance in the clinical microbiology laboratory.

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102 The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

species utilizes nitrogenous substrates such as peptides and amino acids as sources of energy in accordance with the eco-ORJLFDO�VLWH�LQ�ZKLFK�LW�WKULYHV��6KDK�DQG�:LOOLDPV������E��*KDUELD� HW� DO��� �������$QDO\VLV� RI� LWV� JHQRPH� IXQFWLRQ� UH-vealed that this species is rich in pyruvate/oxoglutarate oxi-GRUHGXFWDVHV��ȕ�DODQLQH��JO\FLQH�� VHULQH�DQG� WKUHRQLQH�DQG�WU\SWRSKDQ�PHWDEROLVP��$V�VWXGLHV�RQ�WKH�KXPDQ�DQG�DQLPDO�microbiome continues, relating such functions to precisely GH¿QHG�VSHFLHV�LV�QRZ�WKH�IRFXV�RI�FRQVLGHUDEOH�DWWHQWLRQ�

Today there is general consensus among microbiologists that there is a constant and representative core of genes that GH¿QHV�D�VSHFLHV��%HORZ�WKLV�OHYHO�RI�GLVFULPLQDWLRQ��IXQF-tional properties vary somewhat among strains suggesting WKDW�GLVWLQFW�QLFKHV�DUH�RFFXSLHG��2QH�RI�WKH�FKDOOHQJHV�RI�V\VWHPDWLFV�WRGD\��LQ�WKH�DEVHQFH�RI�'1$±'1$�UHDVVRFLD-WLRQ��LV�WR�¿QG�ZD\V�WR�TXDQWDWLYHO\�GHVFULEH�WKH�OLPLWV�RI�D�species and relate this to their ecological role. The control circuits within an organism are dynamic hence a cell cannot be considered as a simple projection of its genome. Cellular activity is discharged through a myriad of transport, signal-ing, regulatory and metabolic pathways each embodied in WKH�IXQFWLRQDO�DQG�VWUXFWXUDO�UHODWLRQVKLSV�RI�PDQ\�VSHFL¿F�molecules that provide a holistic function for the survival of the cell. It’s likely that physiological function and analy-sis of their proteome and transcriptome will feature more SURPLQHQWO\�LQ�WKH�IXWXUH�WR�KHOS�GHULYH�D�GH¿QLWLRQ�DQG��LQ�WKH�FDVH�RI�WKH�KXPDQ�PLFURÀRUD��SURYLGH�LQVLJKW�LQWR�WKHLU�IXQFWLRQ� LQ� WKH�PLFURELRPH��2QH� UHDVRQ�ZK\�'1$±'1$�reassociation was so successful was that it provided clear demarcation of a species based on the whole genome, its GUDZEDFN�ZDV� WKDW� LW� ZDV� OLPLWHG� WR� D� GH¿QHG� VHW� RI� WHVW�strains and gave no clues about the function of the species. )XWXUH�WD[RQRPLVWV�VKRXOG�SUR¿OH�WKH�JOREDO�H[SUHVVLRQ�RI�FHOOV�WR�VHDUFK�IRU�QHZ�SDUDPHWHUV�WR�TXDQWLWDWLYHO\�GH¿QH�D�XQL¿HG�VHW�RI�IXQFWLRQV�IRU�D�JLYHQ�VSHFLHV�

References

$O�-DOLOL�� 7�$�5�� DQG� +�1�� 6KDK�� ������ 3URWRKHPH�� D� GLV-pensable growth factor for Bacteroides fragilis grown by batch and continuous culture in a basal medium. Curr. 0LFURELRO� 16: ��±���

$O�6KDKLE��$���5��0LVUD��1��$KPRG��0��)DQJ��+��1��6KDK�DQG�6��(��*KDUELD��������&RKHUHQW�SLSHOLQH�IRU�ELRPDUNHU�discovery using mass spectrometry and bioinformatics. %0&�%LRLQIRUPDWLFV�11: ���

$UXPXJDP��0���-��5DHV, (��3HOOHWLHU��'��/H�3DVOLHU��7��<D-PDGD��'�5��0HQGH��*�5��)HUQDQGHV�� -��7DS��7��%UXOV��-��0��%DWWR��0��%HUWDODQ��1��%RUUXHO��)��&DVHOODV��/��)HU-QDQGH]��/��*DXWLHU��7��+DQVHQ��0��+DWWRUL��7��+D\DVKL��0��.OHHUHEH]HP��.��.XURNDZD��0��/HFOHUF��)��/HYHQH]��&��

0DQLFKDQK�� +�%�� 1LHOVHQ�� 7�� 1LHOVHQ�� 1�� 3RQV�� -�� 3RX-ODLQ��-��4LQ��7��6LFKHULW]�3RQWHQ��6��7LPV��'��7RUUHQWV��(��8JDUWH��(�*��=RHWHQGDO��-��:DQJ��)��*XDUQHU��2��3HGHUVHQ��:�0��GH�9RV��6��%UXQDN��-��'RUp��0HWD+,7�&RQVRUWLXP��0��$QWROtQ��)��$UWLJXHQDYH��+�0��%ORWWLHUH��0��$OPHLGD��&��%UHFKRW��&��&DUD��&��&KHUYDX[��$��&XOWURQH��&��'H-ORUPH��*��'HQDULD]��5��'HUY\Q��.�8��)RHUVWQHU��&��)ULVV��0��YDQ�GH�*XFKWH��(��*XHGRQ��)��+DLPHW��:��+XEHU�� -��YDQ�+\OFNDPD�9OLHJ��$��-DPHW��&��-XVWH��*��.DFL��-��.QRO��2��/DNKGDUL��6��/D\HF��.��/H�5RX[��(��0DJXLQ��$��0pUL-HX[��5��0HOR�0LQDUGL��&��0¶ULQL��-��0XOOHU��5��2R]HHU��-��3DUNKLOO��3��5HQDXOW��0��5HVFLJQR��1��6DQFKH]��6��6XQD-JDZD��$��7RUUHMRQ��.��7XUQHU��*��9DQGHPHXOHEURXFN��(��9DUHOD��<��:LQRJUDGVN\��*��=HOOHU�� -��:HLVVHQEDFK��6�'��(KUOLFK�DQG�3��%RUN��������(QWHURW\SHV�RI�WKH�KXPDQ�JXW�microbiome. 1DWXUH�473�����±�����HUUDWXP��474������

%HUJH\��'�+���)�&��+DUULVRQ��5�6��%UHHG��%�:��+DPPHU�DQG�)�0��+XQWRRQ��������*HQXV�Bacteroides Castellani and &KDOPHUV� ������ In %HUJH\¶V� 0DQXDO� RI� 'HWHUPLQDWLYH�%DFWHULRORJ\���VW�HGQ��:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

%HUJH\��'�+���)�&��+DUULVRQ��5�6��%UHHG��%�:��+DPPHU�DQG�)�0��+XQWRRQ��������*HQXV�;;, Bacteroides Castellani DQG�&KDOPHUV� ������ In %HUJH\¶V�0DQXDO� RI�'HWHUPLQD-WLYH� %DFWHULRORJ\�� �QG� HGQ��:LOOLDPV� �:LONLQV�� %DOWL-PRUH��SS�����±����

%HUJH\��'�+���)�&��+DUULVRQ��5�6��%UHHG��%�:��+DPPHU�DQG�)�0��+XQWRRQ�� ������ *HQXV�;;,9��Bacteroides Castel-ODQL�DQG�&KDOPHUV�������In %HUJH\¶V�0DQXDO�RI�'HWHUPL-QDWLYH�%DFWHULRORJ\���UG�HGQ��:LOOLDPV��:LONLQV��%DOWL-PRUH��SS�����±����

%HUJH\�� '�+��� 5�6�� %UHHG�� %�:�� +DPPHU�� )�0�� +XQWRRQ��(�*�'��0XUUD\� DQG� )�&��+DUULVRQ�� ������*HQXV�;;9,��Bacteroides &DVWHOODQL� DQG�&KDOPHUV������� In Bergey’s 0DQXDO�RI�'HWHUPLQDWLYH�%DFWHULRORJ\���WK�HGQ��:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

%HUJH\��'�+���5�6��%UHHG��(�*�'��0XUUD\�DQG�$�3��+LWFKHQV��������*HQXV�9,,,��Bacteroides Castellani and Chalmers ������In�%HUJH\¶V�0DQXDO�RI�'HWHUPLQDWLYH�%DFWHULRORJ\���WK�HGQ��:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

%UHHG��5�6���(�*�'��0XUUD\�DQG�1�5��6PLWK��������*HQXV�I. Bacteroides &DVWHOODQL�DQG�&KDOPHUV�������In Bergey’s 0DQXDO�RI�'HWHUPLQDWLYH�%DFWHULRORJ\���WK�HGQ��:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

%UHHG��5�6��� (�*�'��0XUUD\� DQG�$�3��+LWFKHQV�� ������*H-QXV�;;,��Bacteroides &DVWHOODQL�DQG�&KDOPHUV�������In %HUJH\¶V�0DQXDO�RI�'HWHUPLQDWLYH�%DFWHULRORJ\���WK�HGQ��:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

%U\DQW�� 0�3��� 1�� 6PDOO�� &�� %RXPDQ� DQG� +�� &KX�� ������Bacteroides ruminicola, n. sp., and Succinimonas amy-lolytica WKH�QHZ�JHQXV�DQG�VSHFLHV��6SHFLHV�RI�VXFFLQLF�DFLG�SURGXFLQJ�DQDHURELF�EDWHULD�RI�WKH�ERYLQH�UXPHQ��-��

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103

Haroun N. Shah and Saheer E. Gharbia

The Bulletin of BISMiS

Bacteriol. 76:���±���%MXUVHOO��0�.���(�&��0DUWHQV�DQG�-�,��*RUGRQ��������)XQF-

tional genomic and metabolic studies of the adaptations of a prominent adult human gut symbiont, Bacteroides thetaiotaomicron�� WR� WKH�VXFNOLQJ�SHULRG��-��%LRO��&KHP��281:������±������

&DUOLHU��-��3���0��%HGRUD�)DXUH��*��.¶RXDV��&��$ODX]HW�DQG�)��0RU\��������3URSRVDO�WR�XQLI\�Clostridium orbiscindens Winter et al.������DQG�Eubacterium plautii��6pJXLQ�������+RIVWDG� DQG�$DVMRUG�������ZLWK�GHVFULSWLRQ�RI�Flavoni-fractor plautii gen. nov., comb. nov., and reassignment of Bacteroides capillosus to 3VHXGRÀDYRQLIUDFWRU� FDSLO-losus�JHQ��QRY���FRPE��QRY��,QW��-��6\VW��(YRO��0LFURELRO��60:����±����

&DWR��(�3��DQG�(�0��%DUQHV��������'HVLJQDWLRQ�RI�WKH�QHR-type strain of Bacteroides hypermegas +DUULVRQ�DQG�+DQ-VHQ��,QW��-��6\VW��%DFWHULRO��26:����±����

&KDVVDUG�� &��� (�� 'HOPDV�� 3�$�� /DZVRQ� DQG�$�� %HUQDOLHU�'RQDGLOOH�� ������ Bacteroides xylanisolvens sp. nov., a xylan-degrading bacterium isolated from human faeces. ,QW��-��6\VW��(YRO��0LFURELRO� 58:�����±�����

&ROOLQV�0�'���+�1��6KDK��$�6��0F.HH�DQG�5�0��.URSSHQ-VWHGW��������&KHPRWD[RQRP\�RI�WKH�JHQXV�Capnocytoph-aga��/HDGEHWWHU��+ROW�DQG�6RFUDQVN\���-��$SSO��%DFWHULRO��52:����±����

'HZKLUVW��)�(���7��&KHQ��-��,]DUG��%�-��3DVWHU��$�&�5��7DQQHU��)�(��:HQ�+DQ��$�/DNVKPDQDQ�DQG�:�*��:DGH��������7KH�KXPDQ�RUDO�PLFURELRPH��-��%DFWHULRO��192:�����±�����

'RZHOO��9�5��DQG�7�0��+DZNLQV��������/DERUDWRU\�PHWKRGV�LQ� DQDHURELF� EDFWHULRORJ\��1DWLRQDO�&RPPXQLFDEOH�'LV-HDVH�&HQWHU��8�6����8QLWHG�6WDWHV�3XEOLF�+HDOWK�6HUYLFH��3XEOLF�+HDOWK�6HUYLFH�SXEOLFDWLRQ��QR�������

'UXFNHU��'�%��������8VH�RI�)DVW�$WRP�%RPEDUGPHQW�0DVV�6SHFWURPHWU\�IRU�DQDO\VLV�RI�SRODU�OLSLGV�RI�DQDHUREHV��,Q�Anaerobic Pathogens �HGLWHG�E\�(OH\�DQG�%HQQHWW���6KHI-¿HOG�$FDGHPLF�3UHVV��6KHI¿HOG��SS�����±����

'XHUGHQ�� %�,�� ������ 3LJPHQW� SURGXFWLRQ� E\� Bacteroides VSHFLHV�ZLWK� UHIHUHQFH� WR� VXEFODVVL¿FDWLRQ�� -��0HG��0L-crobiol. 8:����±����

(JJHUWK��$�+��DQG�%�+��*DJQRQ��������7KH�Bacteroides of KXPDQ�IHFHV��-��%DFWHULRO��25:����±����

)LQHJROG��6�0��DQG�(�0��%DUQHV��������5HSRUW�RI�WKH�,QWHU-QDWLRQDO�&RPPLWWHH�RQ�6\VWHPDWLF�%DFWHULRORJ\�6XEFRP-PLWWHH� RQ� WKH� 7D[RQRP\� RI� *UDP�1HJDWLYH�$QDHURELF�5RGV��,QW��-��6\VW��%DFWHULRO��27: ���±����

*KDUELD��6�(���+�1��6KDK�DQG�6�*��:HOVK��������,QÀXHQFH�of peptides on the uptake of amino acids in Fusobacteri-um��SUHGLFWHG�LQWHUDFWLRQ�ZLWK�Porphyromonas gingivalis. &XUU��0LFURELRO��19:����±����

*XSWD��5�6��������7KH�SK\ORJHQ\�DQG�VLJQDWXUH�VHTXHQFHV�characteristics of Fibrobacteres, Chlorobi, and Bacte-roidetes. &ULW��5HY��0LFURELRO� 30: ���±����

*XSWD��5�6��DQG�(��/RUHQ]LQL��������3K\ORJHQ\�DQG�PROHF-XODU� VLJQDWXUHV� �FRQVHUYHG�SURWHLQV� DQG� LQGHOV�� WKDW� DUH�VSHFL¿F�IRU�WKH�Bacteroidetes and Chlorobi�VSHFLHV��%0&�(YRO��%LRO�������>GRL�������������������������@�

*XWWHULGJH�� &�6��� /��9DOOLV� DQG� +�-�+��0DF)LH�� ������ 1X-PHULFDO�PHWKRGV�LQ�WKH�FODVVL¿FDWLRQ�RI�PLFURRUJDQLVPV�by pyrolysis mass spectrometry. In Computer-assisted %DFWHULDO�6\VWHPDWLFV �HGLWHG�E\�*RRGIHOORZ��-RQHV�DQG�3ULHVW���$FDGHPLF�3UHVV��/RQGRQ��SS�����±����

+DUULVRQ��$�3��� -U� DQG� 3�$��+DQVHQ�� ����� Bacteroides hy-permegas�QRY��VSHF��$QWRQLH�YDQ�/HHXZHQKRHN�-��0LFUR-ELRO��6HURO��29: ��±���

+ROGHPDQ��/�9��DQG�:�(�&��0RRUH��������$QDHUREH�/DER-UDWRU\�0DQXDO��$QDHUREH�/DERUDWRU\��9LUJLQLD�3RO\WHFK-QLF�,QVWLWXWH�DQG�6WDWH�8QLYHUVLW\��%ODFNVEXUJ��9$�

+ROGHPDQ��/�9�� DQG�:�(�&��0RRUH�� ������*UDP�QHJDWLYH�DQDHURELF� URGV�� Bacteroidaceae� 3ULEUDP� ������ ���� In %HUJH\¶V�0DQXDO�RI�'HWHUPLQDWLYH�%DFWHULRORJ\���WK�HGQ��HGLWHG�E\�%XFKDQDQ�DQG�*LEERQV���:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

+ROGHPDQ�� /�9�� DQG� -�/�� -RKQVRQ�� ������ 'HVFULSWLRQ� RI�Bacteroides loescheii VS�� QRY�� DQG� (PHQGDWLRQ� RI� WKH�Descriptions of Bacteroides melaninogenicus �2OLYHU�DQG�:KHUU\��5R\�DQG�.HOO\������DQG�Bacteroides den-ticola 6KDK�DQG�&ROOLQV�������,QW��-��6\VW��%DFWHULRO��32: ���±����

+ROGHPDQ�� /�9��� 5�:�� .HOOH\� DQG� :�(�&�� 0RRUH�� ������Family I. Bacteroidaceae. In %HUJH\¶V� 0DQXDO� RI� 6\V-WHPDWLF�%DFWHULRORJ\��YRO�����HGLWHG�E\�.ULHJ�DQG�+ROW���:LOOLDPV��:LONLQV��%DOWLPRUH��SS�����±����

+XQJDWH��5�(��������7KH�5XPHQ�DQG�LWV�0LFUREHV��$FDGHP-LF�3UHVV��1HZ�<RUN��SS����±����

,QWHUQDWLRQDO�&RPPLWWHH�RQ�6\VWHPDWLF�%DFWHULRORJ\��������0LQXWHV�RI�WKH�6XEFRPPLWWHH�RQ�WKH�7D[RQRP\�RI�*UDP�QHJDWLYH�$QDHURELF�5RGV�� ��� DQG���� -XO\�������%XFKD-UHVW��5RPDQLD��,QW��-��6\VW��%DFWHULRO��26:����±����

.DOORZ�� .��� 0�� (UKDUG�� +�1�� 6KDK�� (�� 5DSWDNLV� DQG� 0��:HONHU�� ������ 0$/',�72)�06� IRU� PLFURELDO� LGHQWL¿-FDWLRQ�� \HDUV� RI� H[SHULPHQWDO� GHYHORSPHQW� WR� DQ� HVWDE-lished protocol. In�0DVV�6SHFWURPHWU\�IRU�0LFURELDO�3UR-WHRPLFV��HGLWHG�E\�6KDK�DQG�*KDUELD���:LOH\��&KLFKHVWHU��SS�����±����

.DUOVVRQ�� )�+��� '�:�� 8VVHU\�� -�� 1LHOVHQ� DQG� ,�� 1RRNDHZ��������$�FORVHU�ORRN�DW�Bacteroides: phylogenetic relation-ship and genomic implications of a life in the human gut. 0LFURE��(FRO��61:����±����

.H\V��&�-���'�-��'DUH��+��6XWWRQ��*��:HOOV��0��/XQW��7��0F.-HQQD��0��0F'RZDOO�DQG�+�1��6KDK��������&RPSLODWLRQ�RI� D�0$/',�72)�PDVV� VSHFWUDO� GDWDEDVH� IRU� WKH� UDSLG�screening and characterisation of bacteria implicated LQ� KXPDQ� LQIHFWLRXV� GLVHDVHV�� ,QIHFW�� *HQHW�� (YRO�� 4: ���±����

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104 The Bulletin of BISMiS

A century of systematics of the genus Bacteroides

.R��.�6���7��.XZDKDUD��/��+DHKZD��<��-��<RRQ��%��-��.LP��.��+��/HH��<��2KQLVKL�DQG�<��+��.RRN��������51$�SRO\-PHUDVH�ȕ�VXEXQLW�JHQH��rpoB) sequence analysis for the LGHQWL¿FDWLRQ�RI�Bacteroides VSS��&OLQ��0LFURELRO��,QIHFW� 13:���±���

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is 60: ���±����3UpYRW��$�5���$��7XUSLQ�DQG�3��.DLVHU��������/HV�%DFWpULHV�$QDHURELHV��'XQRG��3DULV�

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5DMHQGUDP��'��������'LVVHFWLQJ�WKH�GLYHUVLW\�RI�WKH�JHQXV�Peptostreptococcus using genomics and proteomic analy-VHV��3K'�WKHVLV��8QLYHUVLW\�RI�(DVW�/RQGRQ�

6DNDPRWR��0��DQG�<��%HQQR��������5HFODVVL¿FDWLRQ�RI�Bac-teroides distasonis, Bacteroides goldsteinii and Bacte-roides merdae as Parabacteroides distasonis gen. nov., comb. nov., Parabacteroides goldsteinii comb. nov. and Parabacteroides merdae FRPE�� QRY�� ,QW�� -�� 6\VW�� (YRO��0LFURELRO��56:�����±�����

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6DNDPRWR��0���0��.LWDKDUD�DQG�<��%HQQR��������Parabacte-roides johnsonii sp. nov., isolated from human faeces. Int. -��6\VW��(YRO��0LFURELRO� 57:����±����

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105

Haroun N. Shah and Saheer E. Gharbia

The Bulletin of BISMiS

terium melaninogenicum ±� D�PLVQRPHU�� -�� *HQ��0LFUR-biol. 1:����±����

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6KDK�� +�1�� 7KH� JHQXV� Porphyromonas and related taxa. ����E�� In 7KH� 3URNDU\RWHV�� D� +DQGERRN� RQ� WKH� %LRO-RJ\� RI� %DFWHULD�� (FRSK\VLRORJ\�� ,VRODWLRQ�� ,GHQWL¿FD-WLRQ��$SSOLFDWLRQV�� �QG� HGQ� �HGLWHG� E\� %DORZV�� 7U�SHU��'ZRUNLQ��+DUGHU�DQG�6FKOHLIHU���6SULQJHU��1HZ�<RUN��SS������±�����

6KDK��+�1��������%LRFKHPLFDO�DQG�FKHPLFDO�SURSHUWLHV��In %LRORJ\�RI�WKH�6SHFLHV�Porphyromonas gingivalis��HGLWHG�E\�6KDK��0D\UDQG�DQG�*HQFR���&5&�3UHVV��%RFD�5DWRQ��SS����±���

6KDK�� +�1��� 5�� %RQQHW�� %�� 0DWHHQ� DQG� 5�$�'��:LOOLDPV��������7KH�SRUSK\ULQ�SLJPHQWDWLRQ�RI�VXEVSHFLHV�RI�Bac-teroides melaninogenicus��%LRFKHP��-� 180:���±���

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6KDK��+�1��DQG�0��&ROOLQV��������Bacteroides buccalis, sp. nov., Bacteroides denticola, sp. nov., and Bacteroides pentosaceus, sp. nov., new species of the genus Bacteroi-des�IURP�WKH�RUDO�FDYLW\��=HQWUDOEO��%DNWHULRO��3DUDVLWHQNG��,QIHNWLRQVNU��+\J��$EW����2ULJ��&��2:����±����

6KDK��+�1��DQG�0�'��&ROOLQV��������*HQXV�Bacteroides, a FKHPRWD[RQRPLFDO� SHUVSHFWLYH�� -�� $SSO�� %DFWHULRO� 55: ���±����

6KDK�� +�1�� DQG� 0�'�� &ROOLQV�� ������ 3URSRVDO� IRU� UHFODV-VL¿FDWLRQ� RI� Bacteroides asaccharolyticus, Bacteroides gingivalis and Bacteroides endodontalis in a new genus, Porphyromonas��,QW��-��6\VW��%DFWHULRO��38:����±����

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6KDK��+�1���0�'��&ROOLQV��-��:DWDEH�DQG�7��0LWVXRND������� Bacteroides oulorum sp. nov. a nonpigmented saccharo-O\WLF�VSHFLHV�IURP�WKH�RUDO�FDYLW\��,QW��-��6\VW��%DFWHULRO��35:����±����

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lation and characterization of gingivain. In Biology of WKH� 6SHFLHV�Porphyromonas gingivalis� �HGLWHG� E\�6KDK��0D\UDQG� DQG� *HQFR��� &5&� 3UHVV�� %RFD� 5DWRQ�� SS�����±����

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6KDK��+�1��DQG�5�$�'��:LOOLDPV��������'HK\GURJHQDVH�SDW-terns in the taxonomy of Bacteroides��-��*HQ��0LFURELRO��128:�����±�����

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6KDK��+�1���5�$�'��:LOOLDPV��*�+��%RZGHQ�DQG�-�0��+DU-GLH��������&RPSDULVRQ�RI� WKH�ELRFKHPLFDO�SURSHUWLHV�RI�Bacteroides melaninogenicus from human dental plaque DQG�RWKHU�VLWHV��-��$SSO��%DFWHULRO� 41:����±����

6KDK��+�1���7�-�0��YDQ�6WHHQEHUJHQ��-�0��+DUGLH�DQG�-��GH�*UDDII�-��������'1$�EDVH�FRPSRVLWLRQ��'1$±'1$�UHDV-sociation and isoelectric focusing of proteins of strains designated Bacteroides oralis. )(06�0LFURELRO��/HWW��13: ���±����

6RFUDQVN\��6�6�� DQG�5�-��*LEERQV�� ������5HTXLUHG� UROH�RI�Bacteroides melaninogenicus in mixed anaerobic infec-WLRQV��-��,QIHFW��'LV��115:����±����

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106 The Bulletin of BISMiS

7XQQLFOLII��5��������7KH�PLFURVFRSLF�DSSHDUDQFHV� LQ�XOFHU�PHPEUDQRXV�WRQVLOOLWLV��9LQFHQW¶V�$QJLQD���-��,QIHFW��'LV��25:����±����

9HLOORQ��0�+��DQG�+��=XEHU��������5HFKHUFKHV�VXU�TXHOTXHV�microbes strictement anaerobies et leur role en patholo-JLH��$UFKLYHV�GH�0HGLFLQH�([SHULPHQWDOH�HW�G¶$QDWRPLH�3DWKRORJLTXH��10:����±����

:DWDEH�� -���<�� %HQQR� DQG� 7��0LWVXRND�� ������ 7D[RQRPLF�study of Bacteroides oralis and related organisms and proposal of Bacteroides veroralis� VS�� QRY�� ,QW�� -�� 6\VW��Bacteriol. 33:���±���

A century of systematics of the genus Bacteroides

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The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 107-115

© BISMiS 2011 107

Introduction

Because only a small fraction of environmental bacteria is brought into pure culture and grown on culture media in the ODE��FXOWXUH�EDVHG�DSSURDFKHV�KDYH�VLJQL¿FDQW�GLVDGYDQWDJ-HV�IRU�DQDO\VHV�RI�HQYLURQPHQWDO�FRPPXQLWLHV��$OWHUQDWLYHO\��molecular genetic approaches have been developed with a ODUJH�GDWDEDVH�RI���6�U51$�JHQH�VHTXHQFHV�DV�D�UHIHUHQFH��These approaches have the advantage of covering a much larger fraction of the natural communities, but they often cannot be well correlated with pure culture approaches, in particular, because both approaches address different frac-WLRQV�RI�D�EDFWHULDO�FRPPXQLW\��0ROHFXODU�WRROV�VXFK�DV���6�U51$� JHQH� VHTXHQFHV�� ZKLFK� FRYHU� D� ZLGH� SK\ORJHQHWLF�range of bacteria, fail in many cases to depict the diversity RI� VSHFL¿F� IXQFWLRQDO� JURXSV�RI� EDFWHULD� LQ� HQYLURQPHQWDO�communities. The most important reason is the fact that they DUH�VSHFL¿F�WR�SK\VLRORJLFDO�JURXSV�RI�HFRORJLFDO�UHOHYDQFH�WR�D�OLPLWHG�H[WHQW��+HUH��PRUH�VSHFL¿F�DSSURDFKHV�KDYH�WR�EH�DSSOLHG��6XFK� WRROV�KDYH�EHHQ�HODERUDWHG� IRU� WKH�JUHHQ�VXOIXU�EDFWHULD��Chlorobi) on the basis of the fmoA JHQH��$O-H[DQGHU�HW�DO���������DQG�IRU�WKH�SKRWRWURSKLF�SXUSOH�EDFWH-ria on the basis of the pufLM JHQHV��7DQN�HW�DO���������DQG�were applied to selected habitats.

From classical taxonomy to molecular systematics

Treatment of phototrophic green and purple sulfur bacte-ULD�DGYDQFHG�VLJQL¿FDQWO\�ZKHQ�1RUEHUW�3IHQQLJ� �3IHQQLJ�������� HVWDEOLVKHG�SURSHU�PHGLD� DQG�FXOWLYDWLRQ� FRQGLWLRQV�for these bacteria and isolated a large number of strains from aquatic, mainly freshwater habitats. Together with +DQV�*HRUJ�7U�SHU�WKH�FODVVLFDO�WD[RQRP\�RI�WKHVH�EDFWHULD�has been established, and a large number of species were SURSHUO\�GHVFULEHG�DQG�WKH�KLJKHU�WD[D�ZHUH�GH¿QHG��3IHQ-QLJ�DQG�7U�SHU������D������E���������3ULPDULO\�SKHQRW\SLF�SURSHUWLHV�ZHUH�XVHG�WR�GH¿QH�DQG�FKDUDFWHUL]H�WKH�VSHFLHV��EHFDXVH�PROHFXODU� JHQHWLF� GDWD� DQG� '1$� VHTXHQFH� LQIRU-PDWLRQ�ZHUH�QRW�DYDLODEOH�DW�WKDW�WLPH��3URSHUWLHV�XVHG�IRU�LGHQWL¿FDWLRQ� LQFOXGHG� FHOO� VKDSH� DQG� VL]H�� RWKHU� PRUSKR-logical criteria, the presence of gas vesicles, internal mem-EUDQH�VWUXFWXUHV��FKORURVRPHV��ÀDJHOODWLRQ��FDURWHQRLG�DQG�photosynthetic pigment composition, absorption spectra, YLWDPLQ�UHTXLUHPHQW��*�&�FRQWHQW�RI�WKH�'1$��DV�ZHOO�DV�physiological properties including substrate utilization and the deposition of elemental sulfur, a storage product and LQWHUPHGLDWH�GXULQJ�VXO¿GH�R[LGDWLRQ��LQVLGH�RU�RXWVLGH�WKH�FHOOV��3IHQQLJ�DQG�7U�SHU��������������

Despite the fact that morphological properties through PLFURVFRSLF� REVHUYDWLRQV� DUH� DPRQJ� WKH� ¿UVW� LQIRUPDWLRQ�available for phototrophic bacteria in environmental sam-ples, they are of limited value for the recognition of species.

Functional gene sequence studies of pure cultures are the basis of systematic studies of environmental communities of photo-WURSKLF�EDFWHULD�DQG�WKHLU�VSHFLHV�VSHFLÀF�DQDO\VHVJohannes F. Imhoff

Contact detailsLeibniz-Institut für Meereswissenschaften, Düsternbrooker Weg 20, D-24105 Kiel, Germany

[email protected]

From the establishment of proper cultivation conditions of phototrophic sulfur bacteria 50 years DJR�XS�WR�WRGD\�VLJQLÀFDQW�LPSURYHPHQWV�KDYH�EHHQ�PDGH�WR�V\VWHPDWLFDOO\�WUHDW�WKH�SKRWRWURSKLF�green and purple sulfur bacteria and identify them in environmental communities. Important steps for WKHVH�LPSURYHPHQWV�ZHUH�ÀUVW�RI�DOO�WKH�GHVFULSWLRQ�RI�D�ODUJH�QXPEHU�RI�SXUH�FXOWXUHV�UHSUHVHQWLQJ�D�SURSHU�IUDFWLRQ�RI�HQYLURQPHQWDO�GLYHUVLW\��WKHLU�FRUUHFW�WD[RQRPLF�WUHDWPHQW�DQG�WKH�FOHDU�GHÀQL-tion of the taxa. Further important steps were the establishment of a phylogenetics-based taxonomy supported by 16S rRNA gene sequences and the demonstration of congruence between phylogenies based on 16S rRNA genes and functional genes. The formation of a large database of fmoA genes of green sulfur bacteria and of pufLM genes of purple sulfur bacteria and their obvious phylogenetic congruence with the 16S rRNA gene enabled detailed studies of environmental communities of these bacteria and the recognition of species and genera in natural habitats. The comprehensive studies of selected habitats yielded promising results and demonstrated the potential of this approach for the systematic characterization of environmental communities.

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108 The Bulletin of BISMiS

Functional genes in studies of phototrophic bacteria

Consequently, most of our knowledge on occurrence of pho-totrophic bacteria in nature is based on culture studies and LGHQWL¿FDWLRQ�RI�WKH�LVRODWHV��3IHQQLJ��������,PKRII������D���though in recent years an increasing number of investiga-tions use genetic approaches to characterize environmental communities, often in combination with the isolation and FXOWXUH�RI�WKHVH�EDFWHULD��H�J��0DUWtQH]�$ORQVR�HW�DO���������5DQFKRX�3H\UXVH�HW�DO����������$OWKRXJK�FXOWXUH�DSSURDFK-es yielded a rough idea on the bacteria present and eventu-ally even on their relative proportion, the question always remained whether cultivation conditions were appropriate to cover the bacteria of relevance in the analyzed sample even if variation of culture media was used to increase the number of bacteria cultured from a particular source. It is generally assumed that the selective properties of media and cultivation conditions give rise only to a limited portion of the phototrophic bacteria present in the sample.

A phylogenetic system for phototrophic sulfur bacteria

7KH�XVH�RI�VHTXHQFH�LQIRUPDWLRQ�RI�WKH���6�U51$�PROHFXOH�DQG�LWV�JHQH�LQWR�EDFWHULDO�SK\ORJHQ\�E\�:RHVH��������DQG�the application of this sequence information for systemat-ic considerations not only revealed the great phylogenetic diversity of the phototrophic bacteria but also promoted FKDQJHV�LQ�WKHLU�WD[RQRP\��7KH�¿UVW�WD[RQRPLF�FRQVHTXHQF-es from the recognition of the phylogenetic relationships among the phototrophic bacteria included the separation of the genus Ectothiorhodospira from the Chromatiaceae and its recognition as a distinct family, the Ectothiorhodospira-ceae with Ectothiorhodospira and the new genus Halorho-dospira� DV� JHQHUD� �,PKRII�� ������� ,Q� DGGLWLRQ�� WKH� SXUSOH�QRQVXOIXU� EDFWHULD� ZHUH� UHRUJDQL]HG�� 0RVW� VLJQL¿FDQWO\�members of Alpha- and Betaproteobacteria were separated. 6RPH�RI�WKHVH��LQ�WKH�FODVVLFDO�V\VWHP��KDG�EHHQ�FRPELQHG�as a single genus. For example, the former Rhodospiril-lum tenue and Rhodopseudomonas gelatinosus, previously thought to be close relatives to the alphaproteobacterial SXUSOH� QRQVXOIXU� EDFWHULD��ZHUH� UHFODVVL¿HG� DV�Betaproteo-bacteria and were transferred to the genus Rhodocyclus and renamed Rhodocyclus tenuis and Rhodocyclus gelatinosus �,PKRII�HW�DO��������� ODWHU�Rubrivivax gelatinosus Willems, *LOOLV�DQG�'H�/H\��������Rhodocyclus purpureus as the only and type species of this genus was recognized itself as a member of the Betaproteobacteria among the majority of the alpha-proteobacterial purple nonsulfur bacteria. With increasing precision and accuracy of the sequence data, fur-WKHU�UHDUUDQJHPHQWV�DPRQJ�WKH�SXUSOH�VXOIXU�EDFWHULD��*X\-RQHDXG�HW�DO���������,PKRII�HW�DO�������E��DQG�WKH�SXUSOH�QRQ-VXOIXU�EDFWHULD��,PKRII�HW�DO�������D��ZHUH�SURSRVHG��$OO�RI�these taxonomic changes carefully considered phenotypic

SURSHUWLHV�DV�ZHOO�DV�DYDLODEOH�PROHFXODU�GDWD��H�J��IDWW\�DF-LGV� DQG� TXLQRQH� FRPSRVLWLRQ�� /36� VWUXFWXUH�� F\WRFKURPH�c amino acid sequences) and genetic sequence data of the ��6�U51$�JHQH��$OWRJHWKHU�WKH�QHZ�PROHFXODU�WD[RQRP\�RI�SKRWRWURSKLF�EDFWHULD�E\�DQG�ODUJH�UHÀHFWHG�WKH�SK\ORJHQ\�RI�WKH���6�U51$�JHQH��,PKRII������E��

Phylogeny of functional genes of phototrophic sulfur bacteria

6HYHUDO� DVSHFWV� SURPRWHG� WKH� LQWURGXFWLRQ� RI� RWKHU� JHQHV�into systematic considerations and the phylogenetic com-SDULVRQ�RI�WKHVH�JHQHV�ZLWK�WKDW�RI�WKH���6�U51$�JHQH��)LUVW��WKH�SK\ORJHQ\�RI�WKH���6�U51$�JHQH��DOWKRXJK�D�ZHOO�FRQ-served and ideal molecule, does not necessarily exactly re-ÀHFW�WKH�SK\ORJHQ\�RI�WKH�EDFWHULD�DV�D�ZKROH��6HFRQG��WKH���6�U51$�JHQH�LV�QRW�VXLWDEOH�IRU�VWXGLHV�RQ�FRPPXQLWLHV�RI�SKRWRWURSKLF�EDFWHULD��LQ�SDUWLFXODU��SXUSOH�EDFWHULD�GR�QRW�form a coherent phylogenetic group and are closely related to non-phototrophic chemotrophic Alpha-, Beta- and Gam-maproteobacteria. Therefore, it was necessary to look for PRUH�VSHFL¿F�PROHFXOHV�DQG�JHQHV�FKDUDFWHULVWLF�IRU�WKHVH�bacteria. Third, the largest collection of pure cultures and type strains of phototrophic purple and green sulfur bacteria was available in our laboratory, including all strains initially LVRODWHG�DQG�PDLQWDLQHG�E\�1RUEHUW�3IHQQLJ�

Phylogeny of the fmoA gene in green sulfur bacteria

7KH�JUHHQ�VXOIXU�EDFWHULD�ZHUH�WKH�¿UVW�JURXS�WKDW�ZDV�FDUH-fully analyzed this way. The fmoA gene encoding a bacte-riochlorophyll-a protein appeared suitable to establish a SK\ORJHQ\�GLVWLQFW�IURP�WKH���6�U51$�JHQH�SK\ORJHQ\��7KH�)02�SURWHLQ�PHGLDWHV�HQHUJ\�WUDQVIHU�EHWZHHQ�WKH�FKORUR-somes and the reaction center in the cytoplasmic membrane RI�JUHHQ�VXOIXU�EDFWHULD��)HQQD�HW�DO����������7KH�fmoA gene is present in green sulfur bacteria and the recently described

“Candidatus� &KORUDFLGREDFWHULXP� WKHUPRSKLOXP´� �%U\DQW�HW�DO����������,W�LV�DEVHQW�LQ�DQRWKHU�PDMRU�SK\ORJHQHWLF�OLQH�of phototrophic green bacteria containing chlorosomes, the &KORURÀH[L��%ODQNHQVKLS�HW�DO����������7KHUHIRUH�LW�LV�DQ�DS-SURSULDWH�WDUJHW�WR�VSHFL¿FDOO\�DQDO\]H�HQYLURQPHQWDO�FRP-PXQLWLHV�RI�WKH�JUHHQ�VXOIXU�EDFWHULD��$OH[DQGHU�DQG�,PKRII��������� %HFDXVH� D� FRPSUHKHQVLYH� SK\ORJHQ\� RI� WKH� JUHHQ�VXOIXU�EDFWHULD��EDVHG�RQ���6�U51$�JHQH�VHTXHQFHV��ZDV�QRW�DYDLODEOH��SK\ORJHQLHV�RI�ERWK���6�U51$�DQG� fmoA genes ZHUH�HVWDEOLVKHG�LQFOXGLQJ�DOO�DYDLODEOH�W\SHV��$OH[DQGHU�HW�DO����������7KH�UHVXOWV�ZHUH�TXLWH�UHPDUNDEOH�LQ�WKDW�WKH�SK\-logenies of the two independent genes were largely congru-HQW�DQG�VSHFLHV�DQG�VWUDLQV�FRXOG�EH�LGHQWL¿HG�E\�HLWKHU�RI�WKH�WZR�JHQHV��$�FRPSDUDWLYH�YLHZ�RI�WKH�SK\ORJHQHWLF�WUHHV�RI�JUHHQ�VXOIXU�EDFWHULD�DFFRUGLQJ�WR���6�U51$�DQG� fmoA JHQHV�LV�SUHVHQWHG�E\�,PKRII��������

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Johannes F. Imhoff

The Bulletin of BISMiS

First of all, the available information on sequences from both genes was used to rearrange the strains of green sulfur EDFWHULD� DPRQJ� WKH� VSHFLHV�� UHGH¿QH� WKH� VSHFLHV� DQG� LQ� D�IHZ� FDVHV� HVWDEOLVK� QHZ� VSHFLHV� DQG� RQH� QHZ� JHQXV� �,P-KRII���������0LVFODVVL¿FDWLRQ�RI�D� ODUJH�QXPEHU�RI�VWUDLQV�was recognized and considerable taxonomic changes were UHTXLUHG�� EHFDXVH� WKH� FODVVL¿FDWLRQ� E\�PRUSKRORJLFDO� DQG�VLPSOH� SK\VLRORJLFDO� SURSHUWLHV� �VXFK� DV� IRUPDWLRQ�RI� JDV�vesicles, thiosulfate utilization, carotenoid and bacterio-chlorophyll molecules present) in many instances was not in congruence with the genetic relatedness supported by WKHVH�WZR�LQGHSHQGHQW�JHQHV��$�FDUHIXO�FRPSDULVRQ�RI� WKH�properties of all available strains and of their phylogenetic relations according to both fmoA�DQG���6�U51$�JHQHV�ZDV�presented together with the proposed taxonomic changes �,PKRII�� ������� 7KH� FOHDU� FRUUHODWLRQ� RI� SK\ORJHQHWLF� UH-lations and taxonomy were preconditions for the possible recognition of species in natural samples by molecular ap-proaches based on genetic sequence information.

Phylogeny of the pufLM genes in purple sulfur bacteria

3KRWRWURSKLF� SXUSOH� EDFWHULD� DUH� GLVWULEXWHG� DPRQJ� WKH� DO-pha-, beta- and gamma-groups of the Proteobacteria and many are closely related to non-phototrophic chemotrophic EDFWHULD��$V� D� FRQVHTXHQFH�� KLJKHU� WD[D� RI� IDPLO\� DQG� RU-der rank contain phototrophic and non-phototrophic genera, WKRXJK�WKH�JHQXV�GH¿QLWLRQV�RI�WKH�SKRWRWURSKLF�SXUSOH�EDF-teria maintain the presence of a photosynthetic apparatus DQG�WKH�DELOLW\�WR�SHUIRUP�SKRWRV\QWKHVLV�DV�GH¿QLQJ�SURS-HUWLHV��,PKRII�DQG�&DXPHWWH���������>8QIRUWXQDWHO\��QXPHU-ous violations published to this recommendation and to the given genus descriptions, in particular among the aerobic phototrophic bacteria, have caused considerable confusion and made necessary the renaming of the bacteria of concern LQ�D�QXPEHU�RI�FDVHV�@

In order to selectively approach the phylogeny of the photo-trophic purple bacteria and to develop tools for the analysis of natural communities of these bacteria, the pufLM genes ZHUH�VHOHFWHG��ZKLFK�HQFRGH�WKH�OLJKW��/��DQG�PHGLXP��0��subunits of the photosynthetic reaction center type II struc-WXUDO�SURWHLQV�RI�DOO�SKRWRWURSKLF�SURWHREDFWHULD��SXUSOH�VXO-fur bacteria, purple nonsulfur bacteria as well as the aerobic phototrophic purple bacteria producing bacteriochlorophyll and forming a photosynthetic apparatus) and the photo-trophic members of &KORURÀH[L. The establishment of a comprehensive database of pufLM gene sequences of most of the recognized type strains of the purple sulfur bacteria and the determination of their phylogenetic relationships again was possible due to the large culture collection main-WDLQHG��$�JRRG�FRUUHODWLRQ�ZDV�IRXQG�EHWZHHQ�SK\ORJHQLHV�

RI���6�U51$�DQG�pufLM genes of the purple sulfur bacte-ria and is demonstrated by comparison of the phylogenetic WUHHV�RI�ERWK�JHQHV��7DQN�HW�DO����������7KLV�VXSSRUWHG�WKH���6�U51$�EDVHG�WD[RQRP\��,PKRII������E��*X\RQHDXG�HW�DO���������,PKRII������E��DQG�DW�WKH�VDPH�WLPH�TXDOL¿HG�WKH�pufLM genes as a valuable tool for studies of environmental FRPPXQLWLHV� RI� SKRWRWURSKLF� SXUSOH� EDFWHULD�� 6SHFLHV� UHF-ognition of these bacteria even in complex mixtures of envi-ronmental communities is now possible.

Molecular ecology and species recognition of phototrophic sulfur bacteria in the natural environment

$IWHU�WKH�LQWURGXFWLRQ�RI�3&5�LQ�WKH�����V�DQG�LQ�FRPELQD-WLRQ�ZLWK�FORQLQJ�WHFKQLTXHV��LW�EHFDPH�SRVVLEOH�WR�XVH�'1$�extracted from environmental samples to identify individual sequences in a habitat and to compare these with sequences known from characterized species. In principle, this opened up the possibility of analyzing the species composition of HQYLURQPHQWDO�FRPPXQLWLHV�� LI���6�U51$�JHQH�VHTXHQFHV�are accepted not only as a phylogenetic marker but also as a taxonomic characteristic. In fact, an extensive comparison RI�'1$±'1$�UHDVVRFLDWLRQ�GDWD�DQG���6�U51$�JHQH�VLPL-larities of pure cultures demonstrated that sequence similari-ties ��������QRW�WKH�SUHYLRXVO\�FRQVLGHUHG������FRXOG�EH�UHFRPPHQGHG�DV�D�SRLQW�DW�ZKLFK�'1$±'1$�K\EULGL]DWLRQ�VWXGLHV�ZRXOG�EH�H[SHFWHG�WR�H[FHHG�����DQG�WKXV�ZRXOG�EH� DQ� DFFHSWDEOH� ERUGHUOLQH� WR� UHFRJQL]H� VSHFLHV� �6WDFNH-EUDQGW�DQG�(EHUV���������7DNLQJ�WKHVH�QXPEHUV�DV�D�URXJK�rule of thumb, species could be recognized in environmental VDPSOHV�RQ�WKH�EDVLV�RI���6�U51$�JHQH�VHTXHQFH�VLPLODUL-WLHV��3LWIDOOV�RI�DSSO\LQJ���6�U51$�EDVHG�DSSURDFKHV�WR�WKH�analysis of communities of phototrophic bacteria, in par-ticular phototrophic purple bacteria, were due to the lack of VSHFL¿F�SULPHUV��UHVSHFWLYHO\�WKH�ODFN�RI�VSHFL¿F�VHTXHQFH�VWUHWFKHV�WKDW�ZRXOG�DOORZ�D�VSHFL¿F�DQDO\VLV�RI�WKLV�SK\OR-genetically diverse group of bacteria in complex mixtures and environmental samples. Their position in the Proteo-bacteria and in part close relationship to non-phototrophic bacteria made it impossible to identify phototrophic purple EDFWHULD�IURP���6�U51$�JHQH�VHTXHQFHV�REWDLQHG�IURP�WKH�environment. In consequence, this necessitated the use of functional genes, e.g. based on genes related to photosyn-thesis of these bacteria for such studies. In addition, due to the great phylogenetic distance between major groups of phototrophic prokaryotes it is likely that separate approach-HV��SULPHUV��WDUJHW�JHQHV��DUH�UHTXLUHG�WR�FRYHU�IRU�WKHVH�PD-jor groups.

6HTXHQFH� LQIRUPDWLRQ� LV�SUH�GHVWLQHG� WR� OLQN�EDFWHULDO� V\V-WHPDWLFV�DQG�HFRORJLFDO�VWXGLHV�EHFDXVH��L��VHTXHQFH�LQIRU-

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110 The Bulletin of BISMiS

Functional genes in studies of phototrophic bacteria

mation is now well established as a property in bacterial systematics and forms a backbone for bacterial phylogeny DQG� V\VWHPDWLF� WUHDWPHQW�� DQG� �LL�� VHTXHQFH� LQIRUPDWLRQ�becomes available from individual clones of environmen-tal communities. While bacterial systematics primarily is dealing with strains and cultures of bacteria, molecular ge-netic studies of natural communities are relying on sequence LQIRUPDWLRQ��(QYLURQPHQWDO� VHTXHQFHV� FDQ�EH� DUUDQJHG� LQ�SK\ORW\SHV��ZKLFK�XQLI\�VHTXHQFHV��UHVSHFWLYHO\�WKH�EDFWH-ULD�DVVRFLDWHG�ZLWK�WKH�VHTXHQFHV��DERYH�D�GH¿QHG�VLPLODULW\�and are used to measure the genetic diversity within envi-ronmental samples. If distinction of phylotypes is made at a sequence level that compares to the level of distinction between species with pure cultures, phylotypes can be used to describe the species diversity of environmental commu-QLWLHV��$Q\KRZ�� LI� HQYLURQPHQWDO� FORQH� VHTXHQFHV� DUH� VXI-¿FLHQWO\�VLPLODU�WR�NQRZQ�VSHFLHV��UHSUHVHQWHG�E\�WKHLU�W\SH�strains, it is quite likely that they are representatives of this species or close relatives thereof. If considerations concern-ing sequence similarities as a rough guide for species differ-entiation of pure cultures are transferred to sequences from the environment, they could help to obtain a rough estimate of the species diversity in environmental samples and help in species recognition. Based on the accepted rules estab-OLVKHG� IRU� WKH� ��6� U51$�JHQH�� VLPLODU� FRQVLGHUDWLRQV� FDQ�be made for functional genes, if their evolutionary rate in FRPSDULVRQ�WR�WKH���6�U51$�JHQH�LV�NQRZQ�RU�FDQ�EH�GHOLQ-HDWHG�IURP�D�GDWDEDVH�RI�VHTXHQFHV��$FFRUGLQJO\�WKUHVKROGV�RI� ����DQG�����VHTXHQFH� VLPLODULW\� RI� WKH�pufLM genes have been proposed for the distinction of genera and species RI�SXUSOH�VXOIXU�EDFWHULD��7DQN�HW�DO���������������=HQJ�HW�DO���������

Environmental communities of green sulfur bacteria

With the comprehensive study of fmoA�DQG���6�U51$�JHQH�phylogenies of pure cultures of green sulfur bacteria as a VROLG�EDVLV��D�¿UVW�GHWDLOHG�PROHFXODU�JHQHWLF�VWXG\�RQ� WKH�species composition of green sulfur bacteria communities was made with samples from saline habitats of different JHRJUDSKLFDO�ORFDWLRQ�XVLQJ�WKH�HVWDEOLVKHG�SULPHUV��7DEOH����$OH[DQGHU�DQG�,PKRII���������4XLWH� LQWHUHVWLQJO\��DOO�RI�WKH�FORQH�VHTXHQFHV��PRUH�WKDQ�������6�U'1$�VHTXHQFHV�DQG�PRUH�WKDQ�����fmoA sequences) from marine and saline KDELWDWV�DOO�RYHU� WKH�ZRUOG��RI� WKH�%DOWLF�6HD�� WKH�0HGLWHU-UDQHDQ�6HD��6LSSHZLVVHWW�VDOW�PDUVK��0DVVDFKXVHWWV��86$��DQG� %DG� :DWHU� �'HDWK� 9DOOH\�� &DOLIRUQLD�� ZHUH� DVVRFL-ated with salt-dependent phylogenetic lines of green sulfur bacteria which had been previously established with pure FXOWXUHV� �$OH[DQGHU� HW� DO��� �������7KH� FOHDU�GRPLQDQFH�RI�representatives of the true marine green sulfur bacteria, in particular of the genus Prosthecochloris �$OH[DQGHU�HW� DO���

������ ,PKRII��������ZDV� LQ� OLQH�ZLWK� WKH�H[SHULHQFH�IURP�culture approaches, which regularly yielded Prosthecochlo-ris aestuarii in enrichments and as isolated cultures from PDQ\� PDULQH� KDELWDWV� �VHH� ,PKRII�� ����D��� 7KRXJK� WKH�FXOWXUH� VWXGLHV� DOZD\V�KDG� OHIW� GRXEW�ZKHWKHU� WKH� VSHFL¿F�cultivation approaches had selected just strains of Prosthe-cochloris, the genetic analyses supported these results, con-clusively demonstrating that members of Prosthecochloris are the dominant green sulfur bacteria in many marine and saline habitats.

+RZHYHU�� WKH� SK\ORJHQHWLF� GLYHUVLW\� RI� PDULQH� JUHHQ� VXO-fur bacteria belonging to Prosthecochloris apparently is VLJQL¿FDQWO\�KLJKHU� WKDQ�NQRZQ� IURP�SXUH� FXOWXUHV� VR� IDU��$YDLODEOH�VHTXHQFH�LQIRUPDWLRQ�DOORZHG�WKH�UHFRJQLWLRQ�RI�at least four different groups within this genus, probably UHSUHVHQWLQJ�GLIIHUHQW�VSHFLHV��$OH[DQGHU�DQG�,PKRII���������$PRQJ� WKHVH� ZHUH� WKH� HVWDEOLVKHG� VSHFLHV�Prosthecochlo-ris aestuarii and Prosthecochloris vibrioforme. In addition, Prosthecochloris indica was described later with new iso-ODWHV�IURP�,QGLD��.XPDU�HW�DO���������

Environmental communities of phototrophic purple sulfur bacteria

Though the pufM gene has been recognized as a potential tool to study anoxygenic phototrophic bacteria in natural environments, environmental studies attempting species recognition were hampered by the lack of a comprehensive database of pufM JHQH�VHTXHQFHV��$FKHQEDFK�HW�DO���������.DUU�HW�DO���������2]�HW�DO���������+X�HW�DO���������$VDR�HW�DO����������7KRXJK�WKHVH�VWXGLHV�UHYHDOHG�LPSRUWDQW�LQIRUPDWLRQ�on the diversity of phototrophic bacteria in the investigated KDELWDWV�� V\VWHPDWLF� VWXGLHV� DQG� WKH� VSHFLHV�VSHFL¿F� DQDO\-sis of complex environmental communities of phototroph-ic purple bacteria were enabled only by the establishment of a comprehensive database using the almost complete sequences of the combined pufL and pufM genes of most SXUSOH�VXOIXU�EDFWHULD�DQG�WKH�YHUL¿FDWLRQ�RI�WKHLU�SK\ORJH-QHWLF�UHODWLRQVKLS��7DQN�HW�DO���������

Salt lakes of the Salar de Atacama

7KH� ¿UVW� GHWDLOHG� VWXG\� RI� HQYLURQPHQWDO� FRPPXQLWLHV� RI�these bacteria which referred to this large pufLM database DQG�XVHG�WKH�HVWDEOLVKHG�SULPHUV��7DEOH����ZDV�WKH�DQDO\VLV�RI� VDOW� ODNHV�RI� WKH�&KLOHDQ�KLJKODQGV� �7KLHO� HW� DO��� �������/LNH�RWKHU�K\SHUVDOLQH�HQYLURQPHQWV��ODNHV�RI�WKH�6DODU�GH�$WDFDPD� �/DJXQD�&KD[D� DQG�/DJXQD�7HEHQTXLFKH�� H[KLE-ited the presence of extended purple-red colored microbial mats in and on the surface of the lake sediments. The com-position of the clone libraries demonstrated a highly di-verse and variable community of anoxygenic phototrophic bacteria.

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Johannes F. Imhoff

The Bulletin of BISMiS

The communities of phototrophic bacteria from both lakes were characterized by the presence of representatives re-lated to the type strains of the moderately and extremely halophilic Chromatiaceae Halochromatium salexigens, Halochromatium glycolicum, Thiohalocapsa halophila, Ec-tothiorhodospira mobilis, Ectothiorhodospira variabilis and Halorhodospira halophila DV�³FORVHVW�UHODWLYHV´��&DXPHWWH�HW�DO���������������������*RUOHQNR�HW�DO����������(YLGHQFH�was also obtained for the presence of several phylotypes of BChl b-containing anoxygenic phototrophic bacteria GLVWDQW� WR� ������ VHTXHQFH� VLPLODULW\�� WKH� JHQHUD�Thiococ-cus, 7KLRÀDYLFRFFXV, and Thioalkalicoccus, which form a distinct phylogenetic branch among the purple sulfur bac-WHULD� �,PKRII� HW� DO��� ����E�� %U\DQWVHYD� HW� DO��� ������7DQN�HW� DO��� ������� 7KHVH� EDFWHULD� DUH� NQRZQ� DV� LQKDELWDQWV� RI�PDULQH�VHGLPHQWV��,PKRII�DQG�3IHQQLJ��������1LFKROVRQ�HW�DO���������3IHQQLJ�HW�DO���������DQG�WKHUHIRUH�WKHLU�SUHVHQFH�in these lake sediments is not surprising, though they have been rarely isolated from coastal marine sediments and soda ODNHV��%U\DQWVHYD�HW�DO���������

The analysis of purple bacteria communities from Chilean VDOW� ODNHV� RI� WKH� 6DODU� GH�$WDFDPD� PRVW� VLJQL¿FDQWO\� UH-YHDOHG�WKDW�DOO�EXW�RQH��D�EHWDSURWHREDFWHULXP�YHU\�GLVWDQWO\�to Rubrivivax��RXW�RI����SK\ORW\SHV�LGHQWL¿HG�ZHUH�DI¿OLDW-ed with the Gammaproteobacteria��7KLHO�HW�DO����������2QO\�WZR�RI�WKHVH�SK\ORW\SHV�TXDOL¿HG�DFFRUGLQJ�WR�WKH�VHTXHQFH�VLPLODULW\�WR�EH�LGHQWL¿HG�DV�RQH�RI�WKH�UHFRJQL]HG�VSHFLHV��Ectothiorhodospira mobilis and Thiohalocapsa halophila), ZKLOH� WKH�PDMRULW\� RI� WKH� SK\ORW\SHV� �����ZHUH� DW� VXFK� D�ORZ�VLPLODULW\��������WR�NQRZQ�SXUSOH�VXOIXU�EDFWHULD�WKDW�TXLWH�OLNHO\�WKH\�PLJKW�UHSUHVHQW�QHZ�JHQHUD��0RVW�UHPDUN-DEOH�ZDV�WKH�GRPLQDQFH�DQG�GLYHUVLW\�����SK\ORW\SHV��RI�D�novel, so far unknown lineage of pufLM containing Gam-maproteobacteria, which was highly diverse and prevalent LQ�GLIIHUHQW�ODNHV�RI�WKH�6DODU�GH�$WDFDPD��7KLHO�HW�DO����������In conclusion, most of the bacteria recognized by pufLM se-quences in the two salt lakes represent new bacteria, more

than two-thirds even at the genus level or higher taxonomic rank. This depicts the extraordinary situation of the habitats in the Chilean highlands with extreme climatic and environ-mental conditions and great geographic distance to all so-far investigated habitats of phototrophic bacteria as well as the uniqueness of their bacterial communities.

Baltic Sea coastal lagoon

In another study based on the pufLM gene approach, the phototrophic bacterial community of a brackish water Baltic 6HD�FRDVWDO�ODJRRQ�ZDV�FKDUDFWHUL]HG��7DQN�HW�DO����������,Q-terestingly, major components of the purple sulfur bacterial FRPPXQLW\�RI� WKLV�EUDFNLVK�ZDWHU� ODJRRQ�DI¿OLDWHG� WR�JHQ-era and species of phototrophic purple sulfur bacteria typi-cally isolated from such habitats including Marichromatium, Thiocystis, Thiorhodococcus, Allochromatium, Thiocapsa, and Thiorhodovibrio��VRPH�VHTXHQFHV�ZHUH�UHODWHG�WR�PRG-erately halophilic Halochromatium and Thiohalocapsa spe-cies, which were not commonly seen thus far in brackish ZDWHUV��&DXPHWWH�HW�DO���������������������,PKRII������D���The overall diversity in the lagoon was comparable to that found in other studies on communities of anoxygenic pho-WRWURSKLF�SXUSOH�EDFWHULD�XVLQJ�PROHFXODU�WHFKQLTXHV��0DU-WtQH]�$ORQVR�HW�DO���������5DQFKRX�3H\UXVH�HW�DO����������$O-WRJHWKHU����pufLM�SK\ORW\SHV�ZHUH�LGHQWL¿HG�LQ�WKH�KDELWDW�VDPSOH��RI�ZKLFK����ZHUH�SXUSOH�VXOIXU�EDFWHULD�

Quite importantly, most of the phylotypes in this study could EH�FOHDUO\�DVVLJQHG�WR�NQRZQ�JHQHUD�DQG�RQO\���RXW�RI����phylotypes of purple sulfur bacteria had sequence similari-WLHV�VOLJKWO\�EHORZ�WKH�SURSRVHG�OLPLW�RI����������±�������pufLM sequence similarity to the closest known type strain and therefore might represent novel genera. In conclusion, the purple sulfur bacteria in the lagoon more or less are known at the genus level but novelty of these bacteria is KLJK�DW� WKH�VSHFLHV�OHYHO�ZLWK�RQO\���RXW�RI����SK\ORW\SHV�clearly assigned to known species.

Table 1. Primer systems recommended for the analysis of environmental communities of phototrophic bacteria

Gene Primer sequence Primer name Reference

Green sulfur bacteria

fmoA ATGGTCCTTTTYGG F-start-fmo Alexander et al. (2002)

CCGACCATNCCGTGRTG R-889-fmo

Purple bacteria

pufLM TTCGACTTYTGGRTNGGNCC pufL67F Tank et al. (2009)

CCAKSGTCCAGCGCCAGAANA pufM781R

Anoxygenic phototrophic bacteria

bchY CCNCARACNATGTGYCCNGCNTTYGG bchY_fwd Yutin et al. (2009)

GGRTCNRCNGGRAANATYTCNCC bchY_rev

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112 The Bulletin of BISMiS

Functional genes in studies of phototrophic bacteria

Interesting results were obtained by performance of enrich-PHQW�H[SHULPHQWV�DORQJ�JUDGLHQWV�RI�WHPSHUDWXUH����±���&��DQG�VDOLQLW\���±�����1D&O��ZLWK�VDPSOHV�IURP�WKLV�KDELWDW�and the molecular analysis of changes within the communi-ty. These experiments demonstrated that the media and cul-ture conditions were quite appropriate for almost all purple sulfur bacteria recognized by the genetic approach. With the exception of three phylotypes found as single clones in the environmental sample, all were retrieved at least from one of the enrichments. In addition, six phylotypes of purple sulfur bacteria were retrieved only after various enrich-PHQWV��$PRQJ�WKHVH�ZHUH�WKUHH�SK\ORW\SHV�PRVW�VLPLODU�WR�the known type strains of Thiorhodococcus mannitolipha-gus ���������Thiorhodococcus kakinadensis ��������� DQG�Marichromatium gracile ��������$Q� LQWHUHVWLQJ� SURSHUW\�of Marichromatium gracile was demonstrated by these experiments. This bacterium became most prominent in HQULFKPHQWV�DW�HOHYDWHG� WHPSHUDWXUHV�DERYH����&�EXW�ZDV�not detected at lower temperatures. The clear preference of Marichromatium gracile� IRU�HOHYDWHG� WHPSHUDWXUHV��VHH�DOVR�6HUUDQR�HW�DO���������SRLQWV�WR�LWV�REYLRXV�FRPSHWLWLYH�advantage in habitats heated during the daytime by the sun.

Conclusions

$�VROLG�WD[RQRPLF�V\VWHP�EDVHG�RQ�ZHOO�FKDUDFWHUL]HG�SXUH�cultures is of inestimable value to attempt species recogni-tion in the environment. Taxonomy of anoxygenic photo-trophic bacteria has over many decades established a well organized and clearly structured system of the bacteria depending on pure cultures. In recent years phylogenetic aspects were systematically included into the taxonomy of these bacteria and this work with pure cultures forms the basis for studies of environmental communities. Their con-sequent application to the characterization of natural bacte-rial communities certainly will promote our knowledge on species distribution of these bacteria and their environmen-tal importance.

The genetic approaches using fmoA and pufLM gene se-quences and in particular a database of these genes from WD[RQRPLFDOO\�FKDUDFWHUL]HG�DQG�ZHOO�GH¿QHG�VSHFLHV��PRVW�LPSRUWDQW�IURP�WKH�W\SH�VWUDLQV��PDGH�SRVVLEOH�WKH�VSHFL¿F�analysis of environmental communities of green and purple sulfur bacteria. With the background of sequences from most of the type strains of known species, it is possible to recognize these species in the natural communities and to relate other sequences to these known types. Thereby the novelty of the clone sequences as well as the diversity of the communities can be estimated. First comprehensive investi-gations, as outlined above, have demonstrated the power of these methods.

Both novelty and diversity were different in the two groups of phototrophic bacteria and in the different habitats studied. The sequences of green sulfur bacteria from different habi-WDWV�ZHUH�UHVWULFWHG�WR�NQRZQ�JHQHUD�DQG�¿WWHG�QLFHO\�LQWR�WKH�established marine and saltwater lineages of the green sulfur bacteria. In addition, the diversity of these bacteria was rath-er low with only a few phylotypes present in a single habitat. The purple sulfur bacterial communities were more diverse LQ� ERWK�KDELWDWV��7KH�%DOWLF�6HD� FRDVWDO� ODJRRQ� UHSUHVHQWV�a repeatedly investigated type of habitat from which quite a number of phototrophic bacteria have been isolated and FKDUDFWHUL]HG��$V�IDU�DV�FDQ�EH�FRQFOXGHG�IURP�WKH�JHQHWLF�sequence analyses, the majority of the components of this community was new at the species level but known at the genus level. The Chilean salares represent an extraordinary and extreme habitat with special conditions regarding salt concentration and composition, irradiation and drastic di-urnal changes. The great majority of purple sulfur bacterial phylotypes of this habitat was new at the genus level or even at higher taxonomic ranks.

Though we are far from being able to systematically de-scribe natural communities even of the well-characterized anoxygenic phototrophic bacteria, results of the work dis-cussed here are promising and demonstrate that this might EH� D� IHDVLEOH� JRDO� IRU� WKH� IXWXUH�� $Q� LPSRUWDQW� SRLQW� RI�support for this optimistic view is the fact that coordina-tion of cultivation-independent and cultivation-dependent approaches demonstrated that most of the phylotypes seen in situ also were found after enrichment with culture con-GLWLRQV�DQG�PHGLD�HVWDEOLVKHG�E\�1RUEHUW�3IHQQLJ��3IHQQLJ�DQG�7U�SHU��������7DQN�HW� DO��� ������� ,Q�DGGLWLRQ��PRVW�RI�the phylotypes present in the different habitats studied rep-resent close relatives to bacteria in culture with a clear taxo-QRPLF�LGHQWLW\��([WHQGHG�FXOWLYDWLRQ�VWXGLHV�PD\�JLYH�ULVH�to cultures representing novel phototrophic bacterial species detected with molecular ecology approaches in the natural environment. From such extreme habitats as the salt lakes RI�WKH�&KLOHDQ�$OWLSODQR��HYHQ�UHSUHVHQWDWLYHV�RI�QHZ�SK\OR-genetic lineages, once genetically detected in environmental samples, may be grown in culture by applying just slight PRGL¿FDWLRQV�RI�PHGLD�DQG�FRQGLWLRQV�FXUUHQWO\�XVHG�

$QRWKHU�SURPLVLQJ�DSSURDFK�XVHG�WKH�VHTXHQFH�RI�WKH�bchY gene, which is more widely distributed in phototrophic EDFWHULD�FRQWDLQLQJ�HLWKHU�D�W\SH���RU�D�W\SH���SKRWRV\VWHP�DQG� ZDV� GHPRQVWUDWHG� WR� SURYLGH� DPSOL¿FDWLRQ� SURGXFWV�from various purple bacteria, green sulfur bacteria and also JUHHQ�QRQVXOIXU�EDFWHULD��<XWLQ�HW�DO����������WKRXJK�WKH�WR-WDO� OHQJWK�RI� WKH�DPSOL¿FDWLRQ�SURGXFWV�ZDV�RQO\����±����QXFOHRWLGHV��7KHVH�SULPHUV��7DEOH����ZHUH�DOVR�VXFFHVVIXOO\�DSSOLHG�WR�HQYLURQPHQWDO�VDPSOHV��<XWLQ�HW�DO����������EXW�D�

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113

Johannes F. Imhoff

The Bulletin of BISMiS

comprehensive database of sequences from pure cultures is still lacking. When the phylogeny of this gene is established with the available type strains of phototrophic bacteria, the bchY gene may prove to be an additional valuable tool to systematically analyze natural communities of phototrophic bacteria.

References

$FKHQEDFK��/�$��� -��&DUH\��DQG�0�7��0DGLJDQ��������3KR-tosynthetic and phylogenetic primers for detection of DQR[\JHQLF� SKRWRWURSKV� LQ� QDWXUDO� HQYLURQPHQWV��$SSO��(QYLURQ��0LFURELRO��67:�����±�����

$OH[DQGHU�� %��� -�+�� $QGHUVHQ�� 5�3�� &R[� DQG� -�)�� ,PKRII�������� 3K\ORJHQ\� RI� JUHHQ� VXOIXU� EDFWHULD� RQ� WKH� EDVLV�RI�JHQH�VHTXHQFHV�RI���6�U51$�DQG�RI� WKH�)HQQD±0DW-WKHZV±2OVRQ�SURWHLQ��$UFK��0LFURELRO��178:����±����

$OH[DQGHU��%��DQG�-�)��,PKRII��������&RPPXQLWLHV�RI�JUHHQ�sulfur bacteria in marine and saline habitats analyzed by JHQH�VHTXHQFHV�RI���6� U51$�DQG�)HQQD±0DWWKHZV±2O-VRQ�SURWHLQ��,QW��0LFURELRO��9:����±����

$QLO� .XPDU�� 3��� 7�1�5�� 6ULQLYDV�� &K�� 6DVLNDOD�� &K�9�� 5D-PDQD��-��6�OLQJ�DQG�-�)��,PKRII��������Prosthecochloris indica sp. nov., a novel green sulfur bacterium from a ma-ULQH�DTXDFXOWXUH�SRQG�RI�.DNLQDGD��,QGLD��-��*HQ��$SSO��0LFURELRO��55:����±����

$VDR��0���+�&��3LQNDUW�DQG�0�7��0DGLJDQ��������'LYHUVLW\�RI� H[WUHPRSKLOLF� SXUSOH� SKRWRWURSKLF� EDFWHULD� LQ� 6RDS�/DNH�� D� FHQWUDO�:DVKLQJWRQ� �86$�� VRGD� ODNH�� (QYLURQ��0LFURELRO��13:�����±�����

%ODQNHQVKLS� 5�(��� -�0�� 2OVRQ��0��0LOOHU�� ������$QWHQQD�FRPSOH[HV� IURP� JUHHQ� SKRWRV\QWKHWLF� EDFWHULD�� �HGLWHG�E\�%ODQNHQVKLS��0DGLJDQ�DQG�%DXHU���.OXZHU�$FDGHPLF�3XEOLVKHUV��'RUGUHFKW��7KH�1HWKHUODQGV��SS�����±����

%U\DQW��'��$���$�0�*��&RVWDV��-�$��0DUHVFD��$�*�0��&KHZ��&�*��.ODWW��0�0��%DWHVRQ��/�-��7DOORQ��-��+RVWHWOHU��:�&��1HOVRQ��-�)��+HLGHOEHUJ�DQG�'��0��:DUG��������Candida-tus &KORUDFLGREDFWHULXP�WKHUPRSKLOXP��DQ�DHURELF�SKR-WRWURSKLF�DFLGREDFWHULXP��6FLHQFH�317:����±����

%U\DQWVHYD�� ,�$��� 9�0�� *RUOHQNR�� (�,�� .RPSDQWVHYD�� DQG�-�)�� ,PKRII�� ������Thioalkalicoccus limnaeus gen. nov., sp. nov., a new alkaliphilic purple sulfur bacterium with bacteriochlorophyll b�� ,QW�� -��6\VW��(YRO��0LFURELRO��50: ����±�����

&DXPHWWH��3���5��%DXODLJXH�DQG�5��0DWKHURQ��������&KDUDF-terization of Chromatium salexigens sp. nov., a halophilic Chromatiaceae�LVRODWHG�IURP�0HGLWHUUDQHDQ�VDOLQDV��6\VW��$SSO��0LFURELRO��10:����±����

&DXPHWWH�� 3��� 5�� %DXODLJXH� DQG�5��0DWKHURQ�� ������Thio-capsa halophila sp. nov, a new halophilic phototrophic SXUSOH�VXOIXU�EDFWHULXP��$UFK��0LFURELRO��155:����±����

&DXPHWWH��3���-�)��,PKRII��-��6�OLQJ�DQG�5��0DWKHURQ�������

Chromatium glycolicum sp. nov., a moderately halophilic purple sulfur bacterium that uses glycolate as substrate. $UFK��0LFURELRO��167:���±���

)HQQD�� 5�(��� %�:��0DWWKHZV�� -�0��2OVRQ� DQG� (�.�� 6KDZ�������� 6WUXFWXUH� RI� D� EDFWHULRFKORURSK\OO� SURWHLQ� IURP�green photosynthetic bacterium Chlorobium limicola ±�FU\VWDOORJUDSKLF�HYLGHQFH�IRU�D� WULPHU��-��0RO��%LRO��84: ���±����

*RUOHQNR��9�0��� ,�$��%U\DQWVHYD��6��5DEROG��7�3��7RXURYD��'��5XEWVRYD��(��6PLUQRYD��9��7KLHO�DQG�-�)��,PKRII��������$� QRYHO� DONDOLSKLOLF� DQG� KDORSKLOLF� SXUSOH� VXOIXU� EDFWH-rium Ectothiorhodospira variabilis from soda lakes. Int. -��6\VW��(YRO��0LFURELRO��59:����±����

*X\RQHDXG�� 5��� -�� 6�OLQJ�� 5�� 3HWUL�� 5��0DWKHURQ�� 3�� &DX-PHWWH��1��3IHQQLJ�DQG�-�)��,PKRII��������7D[RQRPLF�UHDU-rangements of the genera Thiocapsa and Amoebobacter RQ�WKH�EDVLV�RI���6�U'1$�VHTXHQFH�DQDO\VHV�DQG�GHVFULS-tion of Thiolamprovum� JHQ��QRY�� ,QW�� -��6\VW��%DFWHULRO��48:����±����

+X��<�+���+�/��'X��1�=�-LDR�DQG�<�+��=HQJ��������$EXQGDQW�presence of the gamma-like proteobacterial pufM gene in R[LF�VHDZDWHU��)(06�0LFURELRO��/HWW��263:����±����

,PKRII��-�)��������5HDVVLJQPHQW�RI� WKH�JHQXV�Ectothiorho-dospira� 3HOVK� ����� WR� D� QHZ� IDPLO\��Ectothiorhodospi-raceae fam. nov., and emended description of the Chro-matiaceae�%DYHQGDPP�������,QW��-��6\VW��%DFWHULRO��34: ���±����

,PKRII��-�)��������+DORSKLOLF�SKRWRWURSKLF�EDFWHULD��In�+DOR-SKLOLF�%DFWHULD��9RO��,��HGLWHG�E\�5RGULJXH]�9DOHUD���&5&�3UHVV��%RFD�5DWRQ��)/��SS����±����

,PKRII��-�)������D��7UXH�PDULQH�DQG�KDORSKLOLF�DQR[\JHQLF�SKRWRWURSKLF�EDFWHULD��$UFK��0LFURELRO��176:����±����

,PKRII�� -�)�� ����E�� 7KH� DQR[\JHQLF� SKRWRWURSKLF� SXUSOH�bacteria. In�%HUJH\¶V�0DQXDO�RI�6\VWHPDWLF�%DFWHULRORJ\���QG�HGQ��YRO�����7KH�Archaea and the Deeply Branching DQG�3KRWRWURSKLF�Bacteria �HGLWHG�E\�%RRQH�DQG�&DVWHQ-KRO]������±����

,PKRII�� -�)�� ������ 3K\ORJHQHWLF� WD[RQRP\� RI� WKH� IDPLO\�Chlorobiaceae RQ�WKH�EDVLV�RI���6�U51$�DQG� fmo� �)HQ-QD±0DWWKHZV±2OVRQ�SURWHLQ��JHQH�VHTXHQFHV��,QW��-��6\VW��(YRO��0LFURELRO��53:����±����

,PKRII�� -�)�� DQG� 3�� &DXPHWWH�� ������ 5HFRPPHQGHG� VWDQ-dards for the description of new species of anoxygenic SKRWRWURSKLF� EDFWHULD�� ,QW�� -�� 6\VW��(YRO��0LFURELRO��54: ����±�����

,PKRII�-�)��DQG�1��3IHQQLJ��������7KLRÀDYLFRFFXV�PRELOLV gen. nov., sp. nov., a novel purple sulfur bacterium with bacteriochlorophyll b�� ,QW�� -��6\VW��(YRO��0LFURELRO��51: ���±����

,PKRII��-�)���5��3HWUL�DQG�-��6�OLQJ������D��5HFODVVL¿FDWLRQ�of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the _-Proteobacteria��GHVFULSWLRQ�RI�WKH�

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114 The Bulletin of BISMiS

Functional genes in studies of phototrophic bacteria

new genera Phaeospirillum gen. nov., Rhodovibrio gen. nov., Rhodothalassium gen. nov. and Roseospira gen. nov. as well as transfer of Rhodospirillum fulvum to Pha-eospirillum fulvum comb. nov., of Rhodospirillum molis-chianum to Phaeospirillum molischianum comb. nov., of Rhodospirillum salinarum to Rhodovibrio salinarum comb. nov., of Rhodospirillum sodomense to Rhodovi-brio sodomensis comb. nov., of Rhodospirillum salexi-gens to Rhodothalassium salexigens comb. nov., and of Rhodospirillum mediosalinum to Roseospira mediosalina FRPE��QRY��,QW��-��6\VW��%DFWHULRO��48:����±����

,PKRII��-�)���-��6�OLQJ�DQG�5��3HWUL������E��3K\ORJHQHWLF�UH-lationships among the Chromatiaceae, their taxonomic UHFODVVL¿FDWLRQ� DQG� GHVFULSWLRQ� RI� WKH� QHZ� JHQHUD� Al-lochromatium, Halochromatium, Isochromatium, Mari-chromatium, Thiococcus, Thiohalocapsa, and Thermo-chromatium.�,QW��-��6\VW��%DFWHULRO��48:�����±�����

,PKRII��-�)���+�*��7U�SHU�DQG�1��3IHQQLJ��������5HDUUDQJH-PHQW�RI�WKH�VSHFLHV�DQG�JHQHUD�RI�WKH�SKRWRWURSKLF�³3XUSOH�1RQVXOIXU�%DFWHULD´��,QW��-��6\VW��%DFWHULRO��34:����±����

.DUU��(�$���:�0��6DWWOH\��'�2��-XQJ��0�7��0DGLJDQ�DQG�/�$��$FKHQEDFK��������5HPDUNDEOH�GLYHUVLW\�RI�SKRWRWURSKLF�SXUSOH� EDFWHULD� LQ� D� SHUPDQHQWO\� IUR]HQ�$QWDUFWLF� ODNH��$SSO��(QYLURQ��0LFURELRO��69:�����±�����

.XPDU��$�3���7�1�5��6ULQLYDV��&K��6DVLNDOD��9��5DPDQD�� -��6�OLQJ�DQG�-�)��,PKRII��������Prosthecochloris indica sp. nov., a novel green sulfur bacterium from a marine aqua-FXOWXUH�SRQG�RI�.DNLQDGD��,QGLD��-��*HQ��$SSO��0LFURELRO��55:����±����

0DUWtQH]�$ORQVR��0���-��%OHLMVZLMN��1��*DMX��DQG�*��0X\]HU��������'LYHUVLW\�RI�DQR[\JHQLF�SKRWRWURSKLF�VXOIXU�EDFWH-ULD�LQ�WKH�PLFURELDO�PDWV�RI�WKH�(EUR�'HOWD��D�FRPELQHG�PRUSKRORJLFDO� DQG� PROHFXODU� DSSURDFK�� )(06� 0LFUR-ELRO��(FRO��52:����±����

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2]��$���*��6DEHKL��0��.REOL]HN��5��0DVVDQD�DQG�2��%HMD�������� Roseobacter�OLNH� EDFWHULD� LQ� 5HG� DQG� 0HGLWHUUD-QHDQ�6HD�DHURELF�DQR[\JHQLF�SKRWRV\QWKHWLF�SRSXODWLRQV��$SSO��(QYLURQ��0LFURELRO��71:����±����

3IHQQLJ�� 1�� ������ (LQH� YROOV\QWKHWLVFKH� 1lKUO|VXQJ� ]XU�VHOHNWLYHQ� $QUHLFKHUXQJ� HLQLJHU� 6FKZHIHOSXUSXUEDN-WHULHQ��1DWXUZLVVHQVFKDIWHQ�48:�����

3IHQQLJ��1��������3KRWRWURSKLF�JUHHQ�DQG�SXUSOH�EDFWHULD��D�FRPSDUDWLYH�V\VWHPDWLF�VXUYH\��$QQX��5HY��0LFURELRO��31:����±����

3IHQQLJ��1���+��/�QVGRUI��-��6�OLQJ��DQG�-�)��,PKRII��������Rhodospira trueperi, gen. nov. and spec. nov., a new pho-WRWURSKLF�SURWHREDFWHULXP�RI�WKH�DOSKD�JURXS��$UFK��0L-crobiol. 168:���±���

3IHQQLJ��1��DQG�+�*��7U�SHU������D��+LJKHU�WD[D�RI�WKH�SKR-WRWURSKLF�EDFWHULD��,QW��-��6\VW��%DFWHULRO��21:���±���

3IHQQLJ�� 1�� DQG� +�*�� 7U�SHU�� ����E�� 7\SH� DQG� QHRW\SH�strains of the species of phototrophic bacteria maintained LQ�SXUH�FXOWXUH��,QW��-��6\VW��%DFWHULRO��21:���±���

3IHQQLJ��1�� DQG�+�*��7U�SHU��������7KH�SKRWRWURSKLF�EDF-teria. In�%HUJH\¶V�0DQXDO�RI�'HWHUPLQDWLYH�%DFWHULRORJ\���WK�HGQ��HGLWHG�E\�%XFKDQDQ�DQG�*LEERQV���:LOOLDPV��:LONLQV��%DOWLPRUH��SS����±���

3IHQQLJ��1�� DQG�+�*��7U�SHU�� ������ ,VRODWLRQ�RI�PHPEHUV�of the families Chromatiaceae and Chlorobiaceae. In 7KH�3URNDU\RWHV��D�+DQGERRN�RQ�+DELWDWV��,VRODWLRQ��DQG�,GHQWL¿FDWLRQ�RI�%DFWHULD��YRO���� �HGLWHG�E\�6WDUU��6WROS��7U�SHU��%DORZV� DQG�6FKOHJHO��� 6SULQJHU��1HZ�<RUN�� SS�����±����

3IHQQLJ�� 1�� DQG�+�*��7U�SHU�� ������ )DPLO\� ,��Chromatia-ceae. In %HUJH\¶V�0DQXDO�RI�6\VWHPDWLF�%DFWHULRORJ\���WK�HGQ��YRO�����HGLWHG�E\�6WDOH\��%U\DQW��3IHQQLJ�DQG�+ROW���:LOOLDPV��:LONLQV��%DOWLPRUH�SS������±�����

5DQFKRX�3H\UXVH��$���5��+HUEHUW��3��&DXPHWWH�DQG�5��*X\R-QHDXG�� ������&RPSDULVRQ� RI� FXOWLYDWLRQ�GHSHQGHQW� DQG�molecular methods for studying the diversity of anoxy-genic purple phototrophs in sediments of an eutrophic EUDFNLVK�ODJRRQ��(QYLURQ��0LFURELRO��8:�����±�����

6HUUDQR��:���5��$PDQQ�DQG�8��)LVFKHU��������$�QHZ�PRG-HUDWHO\�WKHUPRSKLOLF�DQG�KLJK�VXO¿GH�WROHUDQW�ELRW\SH�RI�Marichromatium gracile, isolated from tidal sediments of WKH�*HUPDQ�:DGGHQ� 6HD��Marichromatium gracile bio-W\SH�WKHUPRVXO¿GLSKLOXP��6\VW��$SSO��0LFURELRO��32:��±�

6WDFNHEUDQGW��(��DQG�-��(EHUV��������7D[RQRPLF�SDUDPHWHUV�UHYLVLWHG�� WDUQLVKHG� JROG� VWDQGDUGV�� 0LFURELRO�� 7RGD\�8:�±��

7DQN��0���0��%O�PHO�DQG�-�)��,PKRII��������&RPPXQLWLHV�RI�SXUSOH�VXOIXU�EDFWHULD�LQ�D�%DOWLF�6HD�FRDVWDO�ODJRRQ�DQD-lyzed by pufLM gene libraries and the impact of tempera-WXUH�DQG�1D&O�FRQFHQWUDWLRQ�LQ�H[SHULPHQWDO�HQULFKPHQW�FXOWXUHV��)(06�0LFURELRO��(FRO��78�����±����

7DQN��0���9��7KLHO�DQG�-�)��,PKRII��������3K\ORJHQHWLF�UHOD-tionship of phototrophic purple sulfur bacteria according to pufL and pufM JHQHV��,QW��0LFURELRO��12:����±����

7KLHO��9���0��7DQN�� 6�&��1HXOLQJHU�� /��*HKUPDQQ�� &��'R-UDGRU�DQG�-�)��,PKRII��������8QLTXH�FRPPXQLWLHV�RI�DQ-R[\JHQLF�SKRWRWURSKLF�EDFWHULD�LQ�VDOLQH�ODNHV�RI�6DODU�GH�$WDFDPD� �&KLOH��� (YLGHQFH� IRU� D� QHZ� SK\ORJHQHWLF� OLQ-eage of phototrophic Gammaproteobacteria from pufLM JHQH�DQDO\VHV��)(06�0LFURELRO��(FRO��74:����±����

:LOOHPV��$���0��*LOOLV�DQG�-��'H�/H\��������7UDQVIHU�RI�Rho-docyclus gelatinosus to Rubrivivax gelatinosus gen. nov., comb. nov., and phylogenetic relationships with Lepto-thrix, Sphaerotilus natans, Pseudomonas saccharophila, and Alcaligenes latus��,QW��-��6\VW��%DFWHULRO��41:���±���

:RHVH��&�5��������%DFWHULDO�HYROXWLRQ��0LFURELRO��5HY��51: ���±����

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115

Johannes F. Imhoff

The Bulletin of BISMiS

<XWLQ��1���0�7��6X]XNL��0��5RVHQEHUJ��'��5RWHP��0�7��0D-GLJDQ�� -�� 6�OLQJ�� -�)�� ,PKRII� DQG� 2�� %HMD�� ������BchY-based degenerate primers target all types of anoxygenic SKRWRV\QWKHWLF�EDFWHULD� LQ�D�VLQJOH�3&5��$SSO��(QYLURQ��0LFURELRO��75:�����±�����

=HQJ�<�+���;�+��&KHQ�DQG�1�=��-LDR��������*HQHWLF�GLYHU-sity assessment of anoxygenic photosynthetic bacteria by distance-based grouping analysis of pufM sequences. /HWW��$SSO��0LFURELRO��45:����±����

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117© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 117–123

Introduction

The developments over recent years in rapid, culture-inde-pendent molecular methods for describing microbial com-munities have been truly remarkable. Initial progress relied ODUJHO\�RQ�WKH�DQDO\VLV�RI���6�U51$�JHQH�VHTXHQFHV��=RH-WHQGDO� HW� DO��� ������GLUHFWO\� DPSOL¿HG� IURP�HQYLURQPHQWDO�VDPSOHV�E\�3&5��0RUH�UHFHQWO\�WKH�XVH�RI�EDUFRGHG�SULP-ers in conjunction with pyrosequencing represents a further technical advance that circumvents the need for cloning. 0RUH� WDUJHWHG� DSSURDFKHV� LQFOXGH� T3&5�� ÀXRUHVFHQFH� in situ� K\EULGL]DWLRQ� �),6+��� DQG� WKH� GHYHORSPHQW� RI� PLFUR-arrays which may use many thousands of oligonucleotide probes to target different taxonomic tiers. Rapid progress is now being made with non-targeted metagenomic sequenc-LQJ�RI�'1$�UHFRYHUHG�IURP�HQYLURQPHQWDO�VDPSOHV��DJDLQ�driven by remarkable developments in sequencing technol-ogy and bioinformatic analysis.

In contrast, few research laboratories now engage in isolat-ing and culturing bacteria, and this area of endeavour has largely fallen out of fashion. Indeed there is even a strand of opinion that cultural microbiology should be regarded

DV�GHIXQFW� �5LW]�� �������:H�EHOLHYH�KRZHYHU� WKDW� LW� LV� LP-portant to critically examine the assumptions on which this YLHZ�LV�EDVHG�SDUWLFXODUO\�LQ�UHODWLRQ�WR�JXW�FRPPXQLWLHV��$W�the start of this revolution in molecular ecology it was fre-TXHQWO\�VWDWHG�WKDW�OHVV�WKDQ����RI�PLFUR�RUJDQLVPV�SUHVHQW�in most environmental samples could be cultivated in the ODERUDWRU\��(LOHUV�HW�DO����������7KLV�PD\�LQGHHG�EH�WUXH�IRU�ecosystems such as oceans and soils that have low nutrient availability and often very low growth rates. In these cases metagenomics may represent the only approach available to FKDUDFWHUL]H�WKHVH�FRPPXQLWLHV��2XU�SXUSRVH�KHUH��KRZHYHU��is to consider the contribution of cultural approaches, allied to molecular methodologies, to studying the microbial com-munities of the human intestine.

The human colon contains a high microbial cell density of DURXQG����� cells per ml of contents and in adults the colon FDUULHV�DURXQG�����PO�RI�FRQWHQWV��7KH�V\VWHP�LV�LQ�D�VWDWH�of constant turnover, requiring resident organisms to have a certain minimum growth rate to avoid being washed out. In contrast to many other ecosystems, the colon is nutrition-ally rich, and develops a highly anoxic environment with DQ�R[LGDWLRQ�UHGXFWLRQ�SRWHQWLDO� RI� DURXQG�í����P9��7KH�S+�DORQJ� WKH� FRORQ�ZLOO� DOVR�ÀXFWXDWH� IURP�PLOGO\� DFLGLF�to neutral values. It is possible that many colonic bacterial VSHFLHV�KDYH� UDWKHU�H[DFWLQJ�QXWULWLRQDO� UHTXLUHPHQWV��QHY-ertheless, culturing these metabolically diverse anaerobes, if

Contact detailsMicrobiology Group, Rowett Institute of Nutrition and Health, Greenburn Road, Bucksburn, Aberdeen AB21 9SB, UK.

&RUUHVSRQGLQJ�DXWKRU��+DUU\�-��)OLQW��³�K�ÁLQW#URZHWW�DF�XN

Harry J. Flint and Sylvia H. Duncan

The importance of cultured representatives of the human intestinal microbiota in the metagenomic era

There has been remarkable progress in the application of molecular approaches, mainly based on analysis of the 16S rRNA gene, to characterize complex microbial ecosystems including that of the hu-man colon. This has been augmented recently by high throughput metagenomic approaches. Although there is an obvious need to link sequence information to functionality, much less emphasis has been given to the isolation and culturing of the gut anaerobes from the colon. Lack of research effort in this area may be due to the fact that the majority of these bacteria are anaerobes that have rather exacting growth requirements. Nevertheless, it is becoming evident that the most dominant bacterial VSHFLHV�WKDW�DUH�OLNHO\�WR�SOD\�D�VLJQLÀFDQW�UROH�LQ�WKH�IRUPDWLRQ�RI�VKRUW�FKDLQ�IDWW\�DFLGV��LQFOXGLQJ�butyrate and propionate, and in the degradation of recalcitrant substrates such a resistant starch and GLHWDU\�ÀEHU�FDQ�EH�LVRODWHG�DQG�FXOWXUHG��0DQ\�RI�WKH�EDFWHULDO�VWUDLQV�UHSUHVHQWLQJ�WKH�GRPLQDQW�species have also recently been genome-sequenced. Moreover, these genome sequences are publicly available and mining this information will provide researchers with the most tremendous insight into the genetic make-up of the inhabitants of our gut. It is important however to continue to culture an-aerobic micro-organisms as well as applying molecular methods, as it is only then that we can truly assess the role of these fascinating micro-organisms in the colon. Some novel bacterial isolates may prove to have potential for biotechnological applications or as probiotics.

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118 The Bulletin of BISMiS

Importance of cultured representatives in the metagenomic era

feasible, must have a major role to play in understanding WKHLU�UROH�LQ�KXPDQ�KHDOWK��$�UHSUHVHQWDWLYH�FXOWXUHG�LVRODWH�enables study of pathogenicity potential, substrate prefer-ences, growth requirements, fermentation pathways, inter-actions with the immune system, environmental tolerance, resistance traits and a host of other characteristics. The ge-nome can also be sequenced rapidly and inexpensively, thus contributing to interpretation of physiological as well as metagenomic data.

What is the culturability of bacteria that inhabit the human intestine?

$QDO\VLV� RI� ��6� U51$� JHQH� VHTXHQFHV� KDV� LQGLFDWHG� WKDW�DURXQG�����RU� OHVV� RI� SK\ORW\SHV� UHFRYHUHG� IURP�KXPDQ�IHFDO� VDPSOHV� FRUUHVSRQG� WR� FXOWXUHG� VSHFLHV� �6XDX� HW� DO���������+D\DVKL�HW�DO���������(FNEXUJ�HW�DO���������7DS�HW�DO���������:DONHU�HW�DO����������6XFK�HVWLPDWHV�KDYH�EHHQ�EDVHG�RQ�³ROG�IDVKLRQHG´�6DQJHU�VHTXHQFLQJ�RI�DW�OHDVW�����EDVHV�XS�WR�IXOO�OHQJWK�VHTXHQFHV��XVLQJ���±����LGHQWLW\�FXW�RIIV��GHSHQGLQJ�RQ�WKH�SUHFLVH�UHJLRQ�VHTXHQFHG��WKDW�GLVWLQJXLVK�NQRZQ�VSHFLHV��3\URVHTXHQFLQJ�GDWD�IURP�PRUH�UHFHQW�VXU-veys generally comprise shorter reliable read lengths that do not allow phylotype discrimination at this level.

)UHTXHQF\�GLVWULEXWLRQV�IURP�VXFK�DQDO\VHV�KDYH�LGHQWL¿HG�a group of phylotypes that are typically more abundant than others in fecal samples from adult humans. These phylo-W\SHV�DUH�QRW�IRXQG�WR�EH�GRPLQDQW�LQ������RI�LQGLYLGXDOV��DQG�VR�FDQQRW�EH�VDLG�WR�FRQVWLWXWH�D�VWULFW�³FRUH´��1HYHUWKH-less they have now been reported in multiple studies and can reasonably be described as “dominant” phylotypes within WKH� KXPDQ� FRORQLF�PLFURELRWD��7DS� HW� DO�� ������� UHSRUWHG�PRUH�WKDQ����SK\ORW\SHV�WKDW�RFFXUUHG�DPRQJ�WKH�GRPLQDQW�IHFDO�PLFURELRWD�LQ�QLQH�RU�PRUH�RI�WKHLU�JURXS�RI����KHDOWK\�DGXOWV��:DONHU� HW� DO�� ������� IRXQG� ��� SK\ORW\SHV� WKDW� DF-counted for ������RI�DPSOL¿HG���6�U51$�JHQH�VHTXHQFHV�IURP���RYHUZHLJKW�PDOHV��7ZR�WKLUGV�RI�WKHVH�FRUUHVSRQGHG�either to previously described species, or to cultured isolates that will form the basis for new species descriptions in the future. This analysis showed therefore that the low cultural coverage of the human intestinal microbiota applies mainly WR�WKH�OHVV�DEXQGDQW�SK\ORW\SHV��L�H��WKRVH�WKDW�LQGLYLGXDOO\�comprised ������RI�WRWDO�VHTXHQFHV���,PSRUWDQWO\��WKLV�VXJ-gests that low cultural representation may simply be the result of the small number of cultured isolates for which ��6�U51$�JHQH�VHTXHQFHV�DUH�DYDLODEOH��L�H��KXPDQ�JXW�EDF-teria should be considered as “undercultivated” rather than

“unculturable”.

$QRWKHU�YHU\�VWULNLQJ�REVHUYDWLRQ�LV�WKDW�IRXU�RI�WKH�WRS�¿YH�PRVW� DEXQGDQW� IHFDO� EDFWHULDO� VSHFLHV� UHSRUWHG� E\�0RRUH�

DQG�0RRUH� ������� DQG� E\�:DONHU� HW� DO�� ������� LQ� &DXFD-VLDQ�SRSXODWLRQV�ZHUH�WKH�VDPH��7DEOH�����:KDW�PDNHV�WKLV�remarkable, apart from the fact that the populations were from different continents and involved different recruitment FULWHULD��LV�WKDW�WKH�0RRUH�DQG�0RRUH��������VWXG\�ZDV�HQ-WLUHO\�FXOWXUH�GHSHQGHQW��ZKHUHDV�:DONHU�HW�DO���������ZHUH�UHSRUWLQJ�DQDO\VLV�RI�DPSOL¿HG���6�U51$�JHQH�VHTXHQFHV��While much has been made of the problem of cultural bias, it appears that this has not been such a major factor with regard to the recovery of the dominant species of human fecal bacteria, provided that strict anaerobic culture tech-niques are used. The very large culture collections obtained LQ�HDUOLHU�VWXGLHV�WKDW�SUH�GDWHG�URXWLQH���6�U51$�VHTXHQF-ing may therefore have contained a much wider range of cultured variation than is currently available.

Geographic variation

$�UHFHQW���6�U51$�EDVHG�VWXG\�E\�GH�)LOOLSR�HW�DO���������demonstrated major differences in fecal microbiota compo-VLWLRQ�EHWZHHQ�JURXSV�RI�$IULFDQ�DQG�,WDOLDQ�FKLOGUHQ��:KLOH�many species were common to both groups, the ratio of Bac-teroidetes to Firmicutes�ZDV�KLJKHU�LQ�WKH�$IULFDQ�FKLOGUHQ��Furthermore the dominant Bacteroidetes were Prevotella VSS��LQ�WKH�$IULFDQ�FKLOGUHQ�DQG�Bacteroides spp. in the Ital-LDQ�FKLOGUHQ��6LQFH�OLWWOH�LQWHQVLYH�FXOWLYDWLRQ�ZRUN�KDV�EHHQ�GRQH�UHFHQWO\�ZLWK�VXEMHFWV�RXWVLGH�1RUWK�$PHULFD��(XURSH�DQG�-DSDQ��WKLV�VXJJHVWV�WKDW�WKHUH�PD\�EH�FRQVLGHUDEOH�XQ-described diversity that might be recovered readily by cul-tivation in other human populations. The authors proposed that differences in staple diet were the main factors underly-ing these differences, although the evidence for this was cir-FXPVWDQWLDO��7KH�HDUOLHU�FXOWXUH�EDVHG�VWXG\�RI�0RRUH�DQG�0RRUH� ������� H[DPLQHG� DGXOW� UXUDO� QDWLYH�$IULFDQV�� UXUDO�QDWLYH�-DSDQHVH�DQG�-DSDQHVH�+DZDLDQV�LQ�DGGLWLRQ�WR�1RUWK�$PHULFDQ�&DXFDVLDQV��7KHLU�GDWD�DOVR�VXJJHVWHG�VRPH�JHR-graphic or ethnic differences, e.g. the lack of Eubacterium rectale among the dominant bacteria detected in the rural -DSDQHVH�JURXS��DQG�D� ODFN�RI�Bacteroides vulgatus in the UXUDO�$IULFDQV�

Metagenomics

0HWDJHQRPLFV� LV� WKH� DQDO\VLV� RI� WKH� WRWDO� '1$� UHFRY-HUHG� IURP�HQYLURQPHQWDO� VDPSOHV� �)UDQN�DQG�3DFH���������0HWDJHQRPLF�OLEUDULHV�PD\�HLWKHU�EH�DQDO\]HG�E\�IXQFWLRQDO�screening with a view to novel gene discovery, or analyzed by random sequencing, with the latter approach proving IDU�PRUH�UDSLG�DQG�LQFUHDVLQJO\�SRSXODU��6HTXHQFHV�FDQ�EH�analyzed to determine the prevalence of different types of JHQH�SUHVHQW� �*LOO� HW� DO����������7D[RQRPLF�DVVLJQPHQW�RI�sequences to bacterial species is possible but this is depen-

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119

Harry J. Flint and Sylvia H. Duncan

The Bulletin of BISMiS

GHQW�HLWKHU�RQ�FRPSDULVRQ�RI�WKH���6�U51$�JHQH�VHTXHQFHV�present, or on the availability of reference genomes from FXOWXUHG� LVRODWHV� �4LQ� HW� DO��� ������� 6XFK� KLJK�WKURXJKSXW�sequencing allows large numbers of samples to be analyzed ZLWKRXW�WKH�SUREOHP�RI�3&5�ELDV��$UXPXJDP�HW�DO���������analyzed fecal samples of volunteers from four countries and found that the microbiota composition could be grouped LQWR� WKUHH� GLVWLQFW� FOXVWHUV� RU� HQWHURW\SHV��2QH� HQWHURW\SH�was enriched in Bacteroides spp., a second in Prevotella spp. whilst the third was enriched in Lachnospiraceae related to Ruminococcus obeum. It was suggested that factors such as ERG\�PDVV�LQGH[��DJH��RU�JHQGHU�KDG�OLWWOH�LPSDFW�LQ�GH¿QLQJ�these enterotypes.

Functional screening of metagenomic libraries is dependent on appropriate high-throughput screening assays, as have EHHQ�DSSOLHG� LQ� WKH�RWKHU�HFRV\VWHPV�VXFK�DV�VRLO� �5LHVHQ-IHOG� HW� DO��� �������$Q� DOWHUQDWLYH� W\SH� RI�PHWDJHQRPLF� DS-SURDFK� LV� WR� XVH� D� 3&5�EDVHG� DSSURDFK� WR� WDUJHW� VSHFL¿F�functional genes as this gives a phylogenetic perspective to VSHFL¿F�IXQFWLRQDO�JURXSV��7KLV�DSSURDFK�KDV�EHHQ�XVHG�WR�analyze hydrogen-metabolizing bacteria including sulfate-UHGXFLQJ�EDFWHULD�DQG�PHWKDQRJHQV� �'HQPDQ�HW� DO��� ������'HSODQFNH�HW�DO���������DQG�ZLOO� DOVR�EH�GLVFXVVHG� IXUWKHU�below in relation to butyrate-producing bacteria.

Composition of the human colonic micro-biota

7KH�PRVW�DEXQGDQW�*UDP�QHJDWLYH�SK\OXP�RI�EDFWHULD�LQ�WKH�human colon are the Bacteroidetes, represented mainly by four genera, Bacteroides, Parabacteroides, Prevotella, and Alistipes��7KHVH�JHQHUD� LQFOXGH�PRUH� WKDQ����FXOWXUHG�VSH-cies among which Bacteroides dorei, Bacteroides cellulo-lyticus, and Bacteroides faecis have been described in recent years. The genome size among the Bacteroidetes is compar-atively large and indicates activities against a wide range of plant- and host-derived polysaccharides. Proteobacteria are generally less numerous, but inhabitants of the large intes-tine include Enterobacteriaceae and sulfate-reducing bacte-ULD��65%��VXFK�DV�Desulfovibrio piger��7KH�*UDP�QHJDWLYH�phyla Verrucomicrobia and Lentisphaerae have two species so far described from the human gut, the mucin-degrader Akkermansia muciniphila��'HUULHQ�HW�DO���������DQG�Victival-lis vadensis� �=RHWHQGDO� HW� DO��� ������� UHVSHFWLYHO\��$PRQJ�WKH� KLJK� PRO�� *�&� FRQWHQW�� *UDP�VWDLQ�SRVLWLYH� Actino-mycetes are two abundant genera, Collinsella and� %L¿GR-bacterium,�ZKLFK�FDQ�UHSUHVHQW����RU�PRUH�RI�WKH�FRORQLF�PLFURELRWD��)OLQW�HW�DO����������7KH�JHQXV�%L¿GREDFWHULXP includes many cultured species of which %L¿GREDFWHULXP�adolescentis and %L¿GREDFWHULXP� ORQJXP� are generally abundant in the adult large intestine.

Table 1. Dominant bacterial phylotypes and species detected in human fecal samples HLWKHU�E\�VHTXHQFLQJ�RI�GLUHFWO\�DPSOLÀHG���6�U51$�RU�E\�DQDHURELF�FXOWXULQJ

16S rRNA data from Walker et al. (2011) are for six overweight males (Scottish, Caucasian) and cultural data from Moore and Moore (1996) are for 17 North American Caucasians. All species are listed that individually accounted for more than 2% of total bacteria in each study.

Species Total bacterial sequences (16S rRNA) (%)

Total bacterial isolates (cul-tured) (%)

Faecalibacterium prausnitzii 7.98* 3.0†Eubacterium rectale 4.43 5.9‡Clostridium clostridioforme 3.83Collinsella aerofaciens 3.67 10.0§Bacteroides vulgatus 3.21 8.2Anaerostipes sp. (SS2/1 related) 2.25Ruminococcus bromii 2.11 5.2Eubacterium hallii 2.0Eubacterium rectale 1 2.9||%LÀGREDFWHULXP�ORQJXP 2.6Peptostreptococcus DZ 2.2%LÀGREDFWHULXP�DGROHVFHQWLV 2.2

*Sum of three phylotypes corresponding to this species.†Described as Fusobacterium prausnitzii.‡“Eubacterium rectale��µ�WDNHQ�DV�FRUUHVSRQGLQJ�WR�WKH�FXUUHQW�GHÀQLWLRQ�RI�Eubacterium rectale.§Sum of “Eubacterium aerofaciens 1 and 2”.__7KRXJKW�OLNHO\�WR�FRUUHVSRQG�WR�RQH�RU�PRUH�RI�WKH�UHGHÀQHG�Roseburia spp.

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120 The Bulletin of BISMiS

Importance of cultured representatives in the metagenomic era

(FNEXUJ�HW�DO���������UHSRUWHG�¿QGLQJ�WKH�JUHDWHVW���6�U51$�JHQH�VHTXHQFH�GLYHUVLW\�ZLWKLQ�WKH�ORZ�PRO��*�&�FRQWHQW�Firmicutes�ZKLFK�DFFRXQWHG�IRU�����RI�����SK\ORW\SHV�GH-¿QHG�LQ� WKHLU�VWXG\�RI�FRORQ�DQG�IHFDO�VDPSOHV�IURP�WKUHH�LQGLYLGXDOV�� 7KH� FRUUHVSRQGLQJ� ¿JXUH� IURP�:DONHU� HW� DO���������IRU�VL[�LQGLYLGXDOV�ZDV�����RXW�RI�����SK\ORW\SHV��In such studies the largest number of Firmicutes phylotypes fall into two families, the Ruminococcaceae and Lachno-spiraceae. The Ruminococcaceae show a rather low repre-VHQWDWLRQ�RI�FXOWXUHG�VSHFLHV��/D\�HW�DO����������EXW�LQFOXGH�Faecalibacterium prausnitzii, a dominant colonic species WKDW�KDV�D�UHTXLUHPHQW�IRU�DFHWDWH�IRU�RSWLPDO�JURZWK��'XQ-FDQ�HW�DO��������� �7DEOH�����+XPDQ�FRORQLF�Ruminococcus species include Ruminococcus callidus and the starch-de-grading Ruminococcus bromii strains. Related ruminococci IURP� WKH� UXPHQ� �Ruminococcus albus and Ruminococcus ÀDYHIDFLHQV) however possess the ability to hydrolyze crys-talline celOXORVH��)OLQW�HW�DO����������,QWHUHVWLQJO\��&KDVVDUG�HW�DO���������UHFHQWO\�LVRODWHG�D�QHZ�FHOOXORO\WLF�UXPLQRFRF-cus species, Ruminococcus champanellensis, from a human IHFDO�VDPSOH��DQG�UXPLQRFRFFDO���6�U51$�JHQH�VHTXHQFHV�appear to be far more abundant on particulate material com-SDUHG�WR�WKH�OLTXLG�SKDVH�RI�KXPDQ�IHFDO�VDPSOHV��:DONHU�HW�DO���������

The Lachnospiraceae comprise a disparate collection of bacterial genera and species and has been estimated to also PDNH�XS�����RU�PRUH�RI�EDFWHULD�IRXQG�LQ�WKH�FRORQ��)OLQW�HW� DO��� �������$�QXPEHU�RI� GLIIHUHQW� JHQHUD�EHORQJ� WR� WKLV�cluster including Anaerostipes, Clostridium, Coprococcus, Eubacterium, Roseburia, Blautia, and Dorea. Roseburia spp. and Eubacterium rectale are a major component of this FOXVWHU� WKDW� SURGXFH�EXW\UDWH� DQG�PDNH�XS� DURXQG��±����RI� WKH� IHFDO�PLFURELRWD� �$PLQRY� HW� DO��� �������Blautia hy-drogenotrophica is of particular interest as it is an acetogen. Ruminococcus spp. belonging to the Lachnospiraceae��EXW�FOHDUO\� LQ� QHHG� RI� JHQHULF� UHFODVVL¿FDWLRQ�� LQFOXGH� Rumi-nococcus obeum, Ruminococcus torques, and Ruminococ-cus gnavus.�2WKHU�KXPDQ�JXW�Firmicutes fall into families that are generally less abundant. Veillonellaceae��FORVWULGLDO�FOXVWHU�,;��DUH�SRRUO\�FKDUDFWHUL]HG�IURP�WKH�KXPDQ�FRORQ�but based on other ecosystems such as the rumen that har-bors Selenomonas, Veillonella, and Megasphaera species, it would be expected that this group might make an important FRQWULEXWLRQ�WR�SURSLRQDWH�IRUPDWLRQ�LQ� WKH�FRORQ��6SHFLHV�WKDW� EHORQJ� WR� FORVWULGLDO� FOXVWHU� ;9� LQFOXGH Clostridium bartlettii��6RQJ�HW�DO���������DQG�Anaerofustis stercorihomi-nis��ZKLFK�LV�D�ELOH�WROHUDQW��EXW\UDWH�SURGXFHU��)LQHJROG�HW�DO����������2WKHU�Firmicutes� UHJXODUO\� LGHQWL¿HG� LQ�KXPDQ�stool include Eubacterium cylindroides belonging to clus-WHU�;9,�DQG�Clostridium ramosum belonging to clostridial FOXVWHU�;9,,,��:LOGHUERHU�9HORR�HW�DO���������+D\DVKL�HW�DO���������

The diversity of archaea in the human colon has so far re-ceived less intensive study. The dominant methanogen is reported to be Methanobrevibacter smithii with Methano-sphaera stadtmanae also detected. Methanobrevibacter smithii XVHV�+��DQG�&2� or formate to form methane.

Butyrate-producers from the human large intestine

0RVW�EDFWHULD�WKDW� LQKDELW� WKH�FRORQ�DUH�DQDHUREHV�WKDW�IHU-ment substrates to form mainly short-chain fatty acids and JDVHV��2QH�RI� WKHVH�6&)$�SURGXFWV��EXW\UDWH�� LV� WKH�PDMRU�energy source for colonocytes and has a role in regulat-LQJ�KRVW�JHQH�H[SUHVVLRQ�DQG�DSRSWRVLV��6FKHSSDFK��������+DPHU�HW�DO����������&RQVLGHUDEOH�HIIRUWV�KDYH�EHHQ�PDGH�to isolate butyrate producers from the human colon, all of which were found to be Firmicutes��%DUFHQLOOD�HW�DO���������3U\GH�HW�DO���������/RXLV�DQG�)OLQW���������7KLV�ZRUN�OHG�WR�WKH�LGHQWL¿FDWLRQ�RI�EXW\U\O�&R$�DFHWDWH�&R$�WUDQVIHUDVH�DV�WKH�¿QDO�VWHS� LQ�EXW\UDWH�V\QWKHVLV� LQ�PRVW�KXPDQ�FRORQLF�EXW\UDWH�SURGXFLQJ�EDFWHULD��/RXLV�HW�DO���������&KDUULHU�HW�DO����������5HFHQWO\��D�VHW�RI�GHJHQHUDWH�3&5�SULPHUV�ZDV�developed that could recognize this gene from phylogeneti-cally diverse Firmicutes� �/RXLV� HW� DO��� �������5HPDUNDEO\��WKH�PDMRULW\��������RI�WKH�EXW\U\O�&R$�DFHWDWH�&R$�WUDQV-IHUDVH� VHTXHQFHV� REWDLQHG� E\� 3&5� DPSOL¿FDWLRQ� IURP� IH-FDO� VDPSOHV� RI� ��� KHDOWK\� LQGLYLGXDOV� FRUUHVSRQGHG� WR� ���species that were already cultured, with the most abundant being Eubacterium rectale, Roseburia faecis, Eubacterium halli and a new species Anaerostipes to be proposed shortly �'XQFDQ�HW�DO���������$OOHQ�9HUFRH�HW�DO���LQ�SUHSDUDWLRQ��

In terms of function we can assign these butyrate-producers WR�WKUHH�EURDG�JURXSLQJV��7KH�ÀDJHOODWHG�Roseburia/Eubac-terium rectale�JURXS��$PLQRY�HW�DO���������EHORQJV� WR� WKH�Lachnospiraceae and their population has been shown to decrease in response to reductions in dietary starch intake LQ�KXPDQ�LQWHUYHQWLRQ�VWXGLHV��'XQFDQ�HW�DO����������$�VHF-ond group of Lachnospiraceae includes Eubacterium halli and two Anaerostipes species that appear to share the ability to utilize lactic acid together with acetate to form butyrate �'XQFDQ� HW� DO��� ������� 7KH� WKLUG� JURXS� DUH�Ruminococca-ceae related to Faecalibacterium prausnitzii. This is one of WKH�PRVW� DEXQGDQW� VSHFLHV� LQ� WKH� KHDOWK\� FRORQ� �7DEOH� ���DQG�LV�SURSRVHG�WR�KDYH�DQWL�LQÀDPPDWRU\�DFWLYLW\��6RNRO�HW�DO����������,WV�DEXQGDQFH�LV�GLPLQLVKHG�LQ�LQGLYLGXDOV�ZLWK�DFWLYH�,%'��6RNRO�HW�DO���������:LOOLQJ�HW�DO����������2WKHU�less dominant butyrate producers include those belonging to the genus Coprococcus. Unlike the species discussed above, Coprococcus eutactus forms butyrate using the butyrate ki-QDVH�HQ]\PH��/RXLV�HW�DO���������

Page 39: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

121

Harry J. Flint and Sylvia H. Duncan

The Bulletin of BISMiS

Conclusions

The availability of cultured isolates from the human colon has contributed enormously to our understanding of the taxonomy, physiology, metabolism, and ecology of the gut microbiota. Cultured isolates also facilitate the design of PROHFXODU�WRROV�VXFK�DV�),6+�SUREHV�DQG�SULPHUV�IRU�T57�3&5�WKDW�FDQ�EH�XVHG�WR�WDUJHW�IXQFWLRQDO�JURXSV��&XOWXUHG�LVRODWHV�PD\�DOVR�EH�XVHG�WR�GH¿QH�LQWHUDFWLRQV�EHWZHHQ�EDF-terial species and between bacteria and host cells that are GLI¿FXOW�RU� LPSRVVLEOH�WR�SUHGLFW�XQOHVV�WHVWHG�ELRORJLFDOO\��%HOHQJXHU�HW�DO���������)DORQ\�HW�DO���������0XQR]�7DPD\R�HW� DO��� ������� /DUJH� JHQRPH� SURJUDPV� LQFOXGLQJ� WKH�1,+�IXQGHG� +XPDQ� 0LFURELRPH� 3URMHFW� �KWWSV���FRPPRQIXQG�QLK�JRY�+PS���DQG�WKH�(8�IXQGHG�0HWD+,7�SURMHFW��KWWS���www.metahit.eu/) are collectively sequencing several hun-dred human intestinal isolates. These genome sequences are SXEOLFO\�DYDLODEOH� IURP�*HQ%DQN�DQG�DUH�JHQHUDWLQJ�YDOX-able information that reveals that these cultured intestinal species are in possession of genes encoding a wide array of glycosyl hydrolases with predicted activities against a broad range of polysaccharides, and also with pathways for vita-min and cofactor synthesis.

Whilst bacterial species from the large intestine and other ecosystems remain uncultured there will always be a need to strive to culture these elusive cells. Understanding of the microbial ecosystem of the human colon will continue to EHQH¿W�IURP�D�UDQJH�RI�PROHFXODU�DQG�FXOWLYDWLRQ�DSSURDFK-HV�ZKLFK�VKRXOG�EH�GHYHORSHG�LQ�SDUDOOHO��*RRGPDQ�HW�DO����������,Q�WKH�IXWXUH�FHUWDLQ�JXW�EDFWHULDO�LVRODWHV�DUH�KLJKO\�likely to be exploited for biotechnological applications or perhaps as new probiotics.

Acknowledgements

The Rowett Research Institute receives support from the 6FRWWLVK�*RYHUQPHQW�5XUDO�DQG�(QYLURQPHQWDO�6FLHQFH�DQG�$QDO\VLV�6HUYLFH�

References

$PLQRY��5�,���$�:��:DONHU��6�+��'XQFDQ��+�-�0��+DUPVHQ��*�:��:HOOLQJ�DQG�+��-�)OLQW��������0ROHFXODU�GLYHUVLW\��FXOWLYDWLRQ��DQG�LPSURYHG�GHWHFWLRQ�E\�ÀXRUHVFHQW�LQ�VLWX�hybidization of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale��$SSO��(QYLURQ��0LFURELRO��72: ����±�����

$UXPXJDP��0��� -� 5DHV�� (�� 3HOOHWLHU��'�� /H� 3DVOLHU��7��<D-PDGD�� '�5��0HQGH��� *�5�� )HUQDQGHV�� -�� 7DS�� 7�� %UXOV��-��0��%DWWR��0��%HUWDODQ��1��%RUUXHO��)��&DVHOODV��/��)HU-QDQGH]��/��*DXWLHU��7��+DQVHQ��0��+DWWRUL��7��+D\DVKL��0��.OHHUHEH]HP��.��.XURNDZD��0��/HFOHUF��)��/HYHQH]��&��

0DQLFKDQK�� +�%�� 1LHOVHQ�� 7�� 1LHOVHQ�� 1�� 3RQV�� -�� 3RX-ODLQ��-��4LQ��7��6LFKHULW]�3RQWHQ��6��7LPV��'��7RUUHQWV��(��8JDUWH��(�*��=RHWHQGDO��-��:DQJ��)��*XDUQHU��2��3HGHUVHQ��:�0��GH�9RV��6��%UXQDN��-��'RUH��0HWD+,7�&RQVRUWLXP��-��:HLVVHQEDFK��6�'��(KUOLFK�DQG�3��%RUN�������(QWHURW\SHV�RI�WKH�KXPDQ�JXW�PLFURELRPH��1DWXUH�473: ���±����

%DUFHQLOOD��$���6�(��3U\GH�� -�&��0DUWLQ��6�+��'XQFDQ��&�6��6WHZDUW��&��+HQGHUVRQ�DQG�+�-��)OLQW��������3K\ORJHQHWLF�relationships of butyrate-producing bacteria from the hu-PDQ�JXW��$SSO��(QYLURQ��0LFURELRO��66: ����±�����

%HOHQJXHU��$��� 6�+�� 'XQFDQ��$�*�� &DOGHU�� *�� +ROWURS�� 3��/RXLV��*�(��/REOH\�DQG�+�-��)OLQW��������7ZR�URXWHV�RI�metabolic cross-feeding between %L¿GREDFWHULXP� DGR-lescentis and butyrate-producing anaerobes from the hu-PDQ�JXW��$SSO��(QYLURQ��0LFURELRO��72: ����±�����

&KDUULHU�� &���*�-��'XQFDQ��0�'��5HLG��*�-�� 5XFNOLGJH��'��+HQGHUVRQ��3��<RXQJ��9�-��5XVVHOO��5�,��$PLQRY��+�-��)OLQW�DQG�3��/RXLV��������$�QRYHO�FODVV�RI�&R$�WUDQVIHUDVH�LQ-volved in short-chain fatty acid metabolism in butyrate-SURGXFLQJ� KXPDQ� FRORQLF� EDFWHULD�� 0LFURELRORJ\� 152: ���±���

&KDVVDUG�� &��� (�� 'HOPDV�� &�� 5REHUW�� 3�$�� /DZVRQ� DQG�$��%HUQDOLHU�'RQDGLOOH�� ������ Ruminococcus champanel-lensis sp. nov., a cellulose-degrading bacterium from the KXPDQ�JXW�PLFURELRWD��,QW��-��6\VW��(YRO��0LFURELRO��62: ���±���

'H�)LOOLSSR��&���'��&DYDOLHUL��0��'L�3DROD��0��5DPD]]RWWL��-�%��3RXOOHW��6��0DVVDUW��6��&ROOLQL��*��3LHUDFFLQL�DQG�3��/LRQHWWL��������,PSDFW�RI�GLHW�LQ�VKDSLQJ�JXW�PLFURELRWD�UHYHDOHG� E\� D� FRPSDUDWLYH� VWXG\� LQ� FKLOGUHQ� IURP� (X-URSH�DQG�UXUDO�$IULFD��3URF��1DWO��$FDG��6FL��8�6�$��107: �����±������

'HQPDQ�� 6�(��� 1�� 7RPNLQV� DQG� &�6�� 0F6ZHHQH\�� ������Quantitation and diversity analysis of ruminal methano-genic populations in response to the antimethanogenic FRPSRXQG� EURPRFKORURPHWKDQH�� )(06� 0LFURE�� (FRO��62: ���±����

'HSODQFNH��%���.�5��+ULVWRYD��+�$��2DNOH\��9�-��0F&UDNHQ��5��$PLQRY��5�,��0DFNLH�DQG�+�5��*DVNLQV��������0ROHF-ular ecological analysis of the succession and diversity RI�VXO¿WH�UHGXFLQJ�EDFWHULD�LQ�WKH�PRXVH�JDVWURLQWHVWLQDO�WUDFW��$SSO��(QYLURQ��0LFURELRO��66: ����±�����

'HUULHQ��0���(�(��9DXJKDQ��&�0��3OXJJH�DQG�:�0��GH�9RV��������Akkermansia muciniphila gen. nov., sp. nov., a hu-PDQ� LQWHVWLQDO� PXFLQ�GHJUDGLQJ� EDFWHULXP�� ,QW�� -�� 6\VW��(YRO��0LFURELRO��54: ����±�����

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122 The Bulletin of BISMiS

Importance of cultured representatives in the metagenomic era

bacteria, isolated from human feces, that produce butyr-DWH�DV�D�PDMRU�IHUPHQWDWLRQ�SURGXFW��$SSO��(QYLURQ��0L-crobiol. 70: ����±�����

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123

Harry J. Flint and Sylvia H. Duncan

The Bulletin of BISMiS

many novel molecular species within the human gut. $SSO��(QYLURQ��0LFURELRO��65: ����±����

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=RHWHQGDO��(�*�&�0��3OXJJH��$�'�/��$NNHUPDQV�DQG�:�0��GH�9RV��������Victivallis vadensis gen. nov., sp. nov., a VXJDU�IHUPHQWLQJ� DQDHUREH� IURP� KXPDQ� IDHFHV�� ,QW�� -��6\VW��(YRO��0LFURELRO��53: ���±����

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Page 43: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

125© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 125–134

Contact details1Key Laboratory of Microbial Diversity in Southwest China, Ministry of Education and the Laboratory for Conservation and Utilization of Bio-resources, Yunnan Institute of Microbiology, Yunnan University, Kunming 650091, China.2Key Laboratory of Synthetic Biology, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.3State Key Laboratory of Genetic Engineering, Department of Microbiology, School of Life Sciences and Institute of Biomedical Sci-ences, Fudan University, Shanghai 200433, China.4China HYK Gene Technology Company Ltd, Shenzhen, Guangdong 518057, China.5Shanghai-MOST Key Laboratory of Disease and Health Genomics, Chinese National Human Genome Center at Shanghai, Shanghai 201203; China.6Department of Microbiology and Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong, Prince of Wales Hos-pital, Shatin, New Territories, Hong Kong SAR, China.

Xiao-Yang Zhi and Wei Zhao contribute equally to the paper.

Corresponding author: Guo-Ping Zhao — [email protected]

Xiao-Yang Zhi,1 Wei Zhao,2,3,4 Wen-Jun Li1 and Guo-Ping Zhao2,3,5,6

Working towards a Molecular Systematics Library for Prokary-RWHV��D�SHUVSHFWLYH

Introduction

The main task of microbial taxonomy is to establish a logi-cal and hierarchical framework to accommodate micro-organisms with huge diversity to facilitate their biological VWXG\��&RZDQ���������3UDFWLFDOO\��WD[RQRP\�UHIHUV�WR�WKUHH�DUHDV�RU�JRDOV��WKH�VRUWLQJ�RI�LQGLYLGXDOV�LQWR�OLNHV�DQG�XQ-OLNHV��FODVVL¿FDWLRQ��� WKH�ODEHOLQJ�RU�QDPLQJ�RI�WKH�JURXSV�VRUWHG��nomenclature���DQG�WKH�FRPSDULVRQ�RI�WKH�XQNQRZQ�with the known followed by their corresponding LGHQWL¿FD-tion� �&RZDQ���������7KH�QRPHQFODWXUH�RI�SURNDU\RWHV�KDV�had a solid foundation through the unremitting efforts of VHYHUDO�JHQHUDWLRQV�RI�GHGLFDWHG�PLFURELRORJLVWV��H�J��(X]p-E\��������7LQGDOO�HW�DO����������$QG�QRZ��WKH�DFKLHYHPHQW�RI�naming micro-organisms has provided a platform for scien-WL¿F�FRPPXQLFDWLRQ��LQVRIDU�DV�WKH�FRUUHFW�XVH�RI�DQ\�QDPH�may open access to a catalog of information about that or-

JDQLVP��0HDQZKLOH�� WKH�FRQWLQXRXV�GHYHORSPHQW�RI�QRYHO�technologies used in taxonomy, including the investigation of prokaryotic communities by using improved culture-de-pendent approaches for extended environment conditions, KDV�VLJQL¿FDQWO\�DIIHFWHG� WKH�IRXQGDWLRQ�RI� WD[RQRP\��)RU�LQVWDQFH�� WKH�FODVVL¿FDWLRQ�DQG� LGHQWL¿FDWLRQ�RI�Actinobac-teria has been continuously updated to accommodate the dramatic increase of novel isolates during the past several GHFDGHV��6WDFNHEUDQGW�HW�DO���������=KL�HW�DO���������

The development of taxonomic research is closely linked to the advancement of new techniques, and the methods used WR�VWXG\�PLFUR�RUJDQLVPV�WD[RQRPLFDOO\�KDYH�UHÀHFWHG�FXU-UHQW�GHYHORSPHQWV�LQ�PLFURELRORJ\��,Q�WKH�ODWH���WK�FHQWXU\��initial emphasis was placed on morphology both micro-mor-phology, relying heavily upon microscopic observation such DV�FHOO�VKDSHV�DQG�WKH�VWUXFWXUHV�RI�FHOOXODU�FRPSRQHQWV��H�J��

With the breakthrough of high-throughput DNA sequencing technologies and development of bioinfor-matics tools, the dramatically increasing availability of genomic data has provided an opportunity and FKDOOHQJH�IRU�V\VWHPDWLVWV�WR�UHQRYDWH�WKH�WD[RQRPLF�V\VWHP�RI�SURNDU\RWHV�HVSHFLDOO\�IRU�WKH�FODVVLÀ-cation of species and their related genera and subspecies. With a better understanding of the genetic and ecological diversity of prokaryotes based on meta- and pan-genomic analyses, comprehensive insights into prokaryotic speciation will revitalize the taxonomic system for prokaryotes in the near future. By integrating more comprehensive genotypic information with corresponding phenotypes of the subject taxa at the genomics level, and relying on related physiological and ecological knowl-edge, we may upgrade our classical taxonomic treatment in encyclopedia-style books to a “Molecular Systematics Library for Prokaryotes” indexed by phylogenomic information and integrated with ever increasing knowledge of biological diversity, which may eventually lead us to a comprehensive under-standing of prokaryotic speciation.

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126 The Bulletin of BISMiS

Working towards a Molecular Systematics Library for Prokaryotes

ÀDJHOOD�RU�SLOL���DQG�FXOWXUDO�FKDUDFWHULVWLFV��UHO\LQJ�XSRQ�WKH�LQWURGXFWLRQ�RI�VROLG�PHGLD�IRU�FRORQ\�LVRODWLRQ��3KHQRW\SLF�studies developed later with the publication of new physi-ological and biochemical techniques, such as the growth properties and chemical composition of cell walls and mem-EUDQHV��HWF��$ORQJ�ZLWK�WKH�GHYHORSPHQW�RI�JHQHWLF�NQRZO-edge and sequencing techniques, it is well established that the phenotypes of prokaryotes are primarily determined by WKHLU�JHQRW\SHV��DQG�WR�D�FHUWDLQ�H[WHQW��WKH�HSLJHQHWLF�SURS-HUWLHV���*LYHQ�WKDW��PRUH�DQG�PRUH�DWWHQWLRQ�LV�EHLQJ�SDLG�WR�the genotypic characteristics and biomarkers for phylogeny by taxonomists. In that direction, with the aid of the strong correlation between sequence variations in the conserved ��6� U51$� JHQHV� DQG� WKH� SK\ORJHQHWLF�HYROXWLRQDU\� UHOD-tionships among the prokaryotes, there is a current trend to differentiate prokaryotic taxa more and more on the basis of the genotype, in particular, by sequence comparisons of the ��6�U51$�JHQHV��.lPSIHU���������2Q�WKH�RWKHU�KDQG��LW�LV�widely recognized that not all species can be differentiated PHUHO\�EDVHG�RQ�WKHLU���6�U51$�JHQH�VHTXHQFHV��DQG�WKXV�for the purpose of proposing a novel species, a phenotypic GHVFULSWLRQ�DQG�SRVVLEO\�'1$±'1$�K\EULGL]DWLRQ�UHPDLQ�essential. Recently, taking the advantage of the availability of large amount of genomic sequences from divergent spe-cies of prokaryotes, many researchers have extended their IRFXV� WR�RWKHU� KRXVHNHHSLQJ�JHQHV� �XVXDOO\�� VLQJOH� FRSLHG�among the taxa being studied) for addressing taxonomic and HYROXWLRQDU\�LVVXHV��1DVHU�HW�DO���������0DUWHQV�HW�DO���������5RQJ�DQG�+XDQJ��������/DEHGD���������)RU�WKH�VDNH�RI�GXUD-bility, many orthologous genes functioning in chromosomal UHSOLFDWLRQ��H�J��dnaK and gyrB), recombination and repair �H�J�� recA�� DQG� WUDQVFULSWLRQ� �H�J�� rpoB) are employed to SHUIRUP�PXOWLORFXV� VHTXHQFH� W\SLQJ� �0/67�� LQ� HSLGHPLR-ORJLFDO� LGHQWL¿FDWLRQ�RI� VWUDLQV�ZLWKLQ�GH¿QHG�SRSXODWLRQV��0DLGHQ�HW�DO����������:KHQ�WKH�QDWXUDO�DQG�HYROXWLRQDU\�UH-lationships among micro-organisms are not well resolved by WKH���6�U51$�JHQH�EDVHG�SK\ORJHQ\��DGGLWLRQDO�KRXVHNHHS-LQJ�JHQHV�KDYH�EHHQ�HPSOR\HG��)RVWHU�HW�DO���������$ODP�HW�DO���������=KDQJ�HW�DO���������

With respect to the integration of genomic information, there are at least two advantages obvious for prokaryotic taxon-RP\�� WKH� DEVROXWHO\� ODUJH� ERG\� RI� LQIRUPDWLRQ� IRU� SK\OR-genetic analysis, and genome-scale metabolic pathway and/or network as the backbone for answering questions about HYROXWLRQ� DQG� HFRORJLFDO� UHODWLRQVKLSV� �%DURQD�*yPH]� HW�DO��� �������%HFDXVH�PHWKRGV� RI� VWDWLVWLFV� FDQ�RQO\� OHDG� WR�improved precision but not necessarily improved accuracy, the use of appropriate statistical methods, including con-catenation, separate gene-by-gene analyses, and modelling, IRU�GDWD�DQDO\VLV��HVSHFLDOO\�IRU�ODUJH�GDWDVHWV��LV�LPSRUWDQW��5DQQDOD�DQG�<DQJ��������+RZHYHU��SK\ORJHQHWLF�WUHH�FRQ-

struction with analytical methods may not be consistent ZLWK�WKDW�EDVHG�RQ���6�U51$�JHQH�VHTXHQFHV��DQG�SHUKDSV�HYHQ�LQFRQJUXHQW�ZLWK�HDFK�RWKHU��5DQQDOD�DQG�<DQJ�������

$OWKRXJK� WKH� FXUUHQW� SRO\SKDVLF� WD[RQRP\� KDV� FRPELQHG�the biological characters of a taxon via multiple approaches ranging from phenotypic properties to genomic informa-WLRQ��LW�LV�VWLOO�JHQHUDOO\�GLI¿FXOW�WR�FRQVROLGDWH�WKH�JHQRW\SH�and phenotype into one uniform system. In other words, the taxonomic system is yet to be comprehensive, covering both the phylogeny backbone and the physiological and meta-EROLF�SURSHUWLHV�VWURQJO\�UHODWHG�WR�WKH�HFRORJLFDO�LQÀXHQFHV��*HQHUDOO\��WKHUH�DUH�WZR�NH\�LVVXHV�\HW�WR�EH�VROYHG���D��WKH�VSHFL¿F� FRUUHODWLRQ� RI� WD[RQRPLF� FKDUDFWHULVWLFV� �SKHQR-W\SHV��WR�WKH�JHQRPLF�VHTXHQFHV��JHQRW\SHV��EDVHG�RQ�DFFX-UDWH�DQQRWDWLRQV��DQG��E��WKH�SURSHU�VWUDWL¿FDWLRQ�RI�GLIIHUHQW�VHWV�RI�JHQRPLF�PDUNHUV��LQ�PDQ\�FDVHV��VLPSO\�JHQHV��IRU�prokaryotic phylogeny at different taxonomic levels. In ad-dition, the advent of genomics has revolutionized biological studies of micro-organisms and will also revitalize prokary-RWLF�WD[RQRP\�WR�WDFNOH�WKH�QHZ�VFLHQWL¿F�SUREOHPV�UDLVHG�E\�WKH�JHQRPLF�UHVHDUFK��7KH�JHQRPHV��RU�JHQRPLF�PDUN-ers) of isolates, including those yet to be cultured, not only provide comprehensive even complete and accurate genom-LF�LQIRUPDWLRQ�LQ�WKH�IRUP�RI�'1$�VHTXHQFHV�DQG�DQQRWDWHG�genes, but also an opportunity for investigating and under-standing the biological process encoded by the genome. 2QH� REYLRXV� H[DPSOH� LV� WKH� UHFRQVWUXFWLRQ� RI� PHWDEROLF�networks from genome sequences, which can provide novel in silico chemotaxa useful as potential evolutionary markers �%DURQD�*yPH]� HW� DO��� �������)XUWKHUPRUH�� DV� SKHQRW\SHV�represent the expression of genotypes under certain environ-mental conditions, phylogenomic studies based upon central and/or peripheral metabolism should be in agreement with the phenotypic characteristics of polyphasic taxonomy. Un-der these circumstances, the modern prokaryotic taxonomic V\VWHP�VKRXOG�QHLWKHU�EH�EDVHG�PHUHO\�RQ���6�U51$�RU�VH-lected housekeeping genes nor be portrayed as a phenotypic character-based traditional reference book. By introducing the theories and techniques of genomics to bridge the gap between genotypes and phenotypes, modern taxonomy will be enriched and vitalized in the true sense of biology, i.e. to UHÀHFW� WKH�HYROXWLRQDU\�KLVWRU\�DQG�QDWXUDO�HFRORJLFDO�UHOD-tionships among the taxa.

Understanding the genetic diversity of prokaryotes

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127The Bulletin of BISMiS

Xiao-Yang Zhi, Wei Zhao, Wen-Jun Li and Guo-Ping Zhao

housekeeping genes to the complete genomes encoding all the biological processes. It allows us to differentiate, at all levels of resolution, the genetic make-up between two VWUDLQV�DQG�WKXV�VXEVWDQWLDOO\�FRQWULEXWHV�WRZDUGV�WKH�GH¿QL-WLRQ�RI�D�PLFURELDO�VSHFLHV��.RQVWDQWLQLGLV�HW�DO���������

$� FRPSUHKHQVLYH� XQGHUVWDQGLQJ� RI� ELRGLYHUVLW\� EDVHG� RQ�our knowledge of genomics and the practice of taxonomy is the key for future development of taxonomy in the ge-nomics era. Genetic diversity, as the molecular foundation of ecological diversity, is a basic representation of biodiver-sity based on genetic variations of species interacting under variable environmental conditions.

(VWLPDWHV� RI� GLYHUVLW\� IRU� QDWXUDO� EDFWHULDO� FRPPXQLWLHV�KDYH�WUDGLWLRQDOO\�GHSHQGHG�RQ�FXOWLYDEOH�VSHFLHV��+RZHYHU��PROHFXODU�HFRORJLFDO� VWXGLHV�PDLQO\�SUREHG�E\���6� U51$�genes suggests that the culture-based estimation actually led to a longstanding underestimation of bacterial diversity �7RUVYLN�HW�DO����������7KHUHIRUH��WKH�JHQHWLF�GLYHUVLW\�RI�D�SRSXODWLRQ� �H�J�� DW� RU� EHORZ� WKH� VSHFLHV� OHYHO�� FDQ� EH� H[-plored thoroughly in the era of genomics. This is particular-ly true if the functional aspects of physiology, metabolism and growth in a complex environment are considered along with the genomic sequences for comprehending biologi-FDO�GLYHUVLW\��0RFDOL�DQG�%HQHGHWWL���������0HWD�JHQRPLF�analysis of a given community may offer an alternative ap-proach towards that direction by describing the genetic di-versity of a microbiota and characterizing some of the major contributing species without physical isolation of the strains �3HWURVLQR��������

:LWKLQ�D�EDFWHULDO�VSHFLHV��RU�HYHQ�JHQXV���WKH�core genome WKDW�LV�UHVSRQVLEOH�IRU�WKH�EDVLF�IXQFWLRQV��*LO�HW�DO���������may not change dramatically except for some obligate bac-WHULDO�V\PELRQWV��0RUDQ���������2Q�WKH�RWKHU�KDQG��WKH�JHQH�reservoir available for inclusion in its pan-genome� �7HWWH-OLQ�HW�DO���������LV�YDVW�DQG�GUDPDWLFDOO\�YDULDEOH��0RUH�DQG�more individual genome�VSHFL¿F� JHQHV�� LQFOXGLQJ� PRELOH�genetic elements, plasmids and bacteriophages, may con-WLQXH�WR�EH�LGHQWL¿HG�DIWHU�VHTXHQFLQJ�KXQGUHGV�RI�JHQRPHV��7HWWHOLQ�HW�DO����������+HQFH��WKH�peripheral genome is con-VLGHUHG�WR�SOD\�DQ�LPSRUWDQW�UROH��H�J��FRQIHUULQJ�DGDSWLRQ�to different niches) in the maintenance of genetic diversity. The genomic variability of Streptococcus pneumoniae has EHHQ�VWXGLHG�ZLWK�D�ODUJH�JURXS�RI�LVRODWHV��LWV�SDQ�JHQRPH�can greatly vary in size, and that guarantees the species a TXLFN� DQG� HI¿FLHQW� UHVSRQVH� WR� GLYHUVH� HQYLURQPHQWV� �'R-QDWL�HW�DO����������7KH�ORQJHU�DQ�LQGLYLGXDO�KDV�HYROYHG�LQGH-pendently, the more new genes it will potentially contribute to the species’ pan-genome. The size of the pan-genome, WKHUHIRUH��UHÀHFWV�WKH�GHJUHH�WR�ZKLFK�WKH�VHTXHQFHG�VWUDLQV�

are phylogenetically related, and it yields information on the HYROXWLRQ�RI�WKH�VSHFLHV��0X]]L�DQG�'RQDWL���������5HFHQWO\��/XR�HW�DO���������GHPRQVWUDWHG�WKDW�WKH�JHQRPHV�RI�WKH�LQWHV-tinal commensal Escherichia coli encode some functional JHQHV�EHQH¿WWLQJ�WKH�¿WQHVV�LQ�WKH�KXPDQ��DQG�DQLPDO��JXW��while their environmental counterparts possess another set RI�VSHFL¿F�JHQHV�WKDW�LV�LQVWUXPHQWDO�LQ�UHVRXUFH�DFTXLVLWLRQ�and survival in the environment. Thus, although all of these Escherichia coli isolates belong to the same species based on our current phylogenomic standards for species demar-FDWLRQ� �*RULV� HW� DO��� ������� LW� LV� FOHDU� WKDW� WKH�GLYHUVLW\� RI�their peripheral genomes may provide more insight into the biological diversity within a population, such as of a species, and may facilitate our understanding about the evolution-ary dynamics among individuals, either representing cryp-tic new species or a process of speciation under different environmental conditions. These two examples imply that it is essential to know the gene content of a bacterium in order to understand how it speciates. To the higher ranks in the taxonomic system, two taxa sharing closer evolutionary relationships should possess, in theory, more genes in com-mon. The core genome will likely be valuable in revealing the divergence amongst different taxa.

For the most clinically important species, some prevalent VHTXHQFH�EDVHG� DSSURDFKHV�� H�J��0/67�� KDYH� EHHQ� LQVWUX-mental in studying the population structure and evolution RI�SDWKRJHQV�DQG�HYHQ�XVHG�IRU� LGHQWL¿FDWLRQ��&KDQ�HW�DO����������+RZHYHU��WKH�JHQHWLF�YDULDWLRQV�W\SLFDOO\�XVHG�HQWDLO�small-sized samples and limited fractions of the genomes and cannot distinguish among closely related isolates. The use of next-generation sequencing technologies to gener-DWH�ZKROH�JHQRPH�'1$�VHTXHQFH�GDWD�IRU�ODUJH�SRSXODWLRQ�samples of bacteria has enabled subspecies typing reveal the global geographic structure and transmission process of SDWKRJHQLF�EDFWHULD��+DUULV�HW�DO���������

Understanding the ecological diversity of prokaryotes

The various environmental conditions in which microbes re-side are supposed to be one of the factors contributing to the ambiguity of genetic diversity of prokaryotes and to their PHFKDQLVPV� RI�PLFURELDO� VSHFLDWLRQ�� -DPHV�6WDOH\� �������recently pointed out that a comprehensive understanding of microbial diversity should be the fourth goal of microbial taxonomy. In our opinion, there are two levels of implica-tions, i.e. the discovery and description of the diversity, and the rationale for the formation of microbial diversity. There-fore, it is more important for a taxonomist to reveal the ge-netic and ecological relationships among the species, and based on these analyses, to explain why such diverse mi-

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128 The Bulletin of BISMiS

Working towards a Molecular Systematics Library for Prokaryotes

crobial species exist and how they have evolved. In recent decades, using pure cultures as well as culture-independent approaches, microbiologists and ecologists have begun to study the biogeography of microbial life on earth compre-KHQVLYHO\��0DUWLQ\�HW�DO���������2¶0DOOH\���������5HPDUN-ably, genome sequences are providing detailed information about the complete genetic composition of microbes in a GH¿QHG�HFRORJLFDO�QLFKH��DQG�RIIHULQJ�DQ�XQFRPPRQ�RSSRU-tunity to search for evolutionary traces left in the genome and to reveal what causes the ecological diversity of the microbiota.

$� QDWXUDO� FULWHULRQ� WR� LGHQWLI\� PLFURELRWD� ZLWK� HYROXWLRQ-DU\� VLJQL¿FDQFH� LV� WR� FKDUDFWHUL]H� HFRORJLFDO� IHDWXUHV� WKDW�PD\�GLVWLQJXLVK�WKHP�IURP�WKHLU�FORVH�UHODWLYHV��+LVWRULFDOO\��SDWKRJHQV�ZHUH�FODVVL¿HG�DV�GLIIHUHQW�VSHFLHV�EDVHG�RQ�WKHLU�DELOLW\�WR�FDXVH�D�GLVWLQFWLYH�GLVHDVH��)UDVHU�HW�DO���������DQG�WKHVH�DUH�QRZ�RIWHQ�UHOHJDWHG�WR�³SDWKRYDU´�VWDWXV��0DSSLQJ�of prokaryotic diversity onto environmental resources indi-cates that closely related groups of micro-organisms might EH�HFRORJLFDOO\�GLYHUJHQW��+XQW�HW�DO����������$OWKRXJK�WKH�WUDGLWLRQDO� DSSURDFKHV� FRQFHUQLQJ� WKH� GH¿QLWLRQ� RI� VSH-cies and molecular microbial ecology hints at the concept RI�HFRORJLFDO� VSHFLHV� �&RKDQ��������� WKH\�DUH� LQWULQVLFDOO\�poor in resolution and power for understanding the ecologi-cal diversity of microbes, and thus limited in their implica-WLRQ�WR�VSHFLDO�SXUSRVH�FODVVL¿FDWLRQV��LQ�WKLV�FDVH��HFRORJ\��1HYHUWKHOHVV��HQYLURQPHQWDO�IDFWRUV�DUH�LPSRUWDQW�QRW�RQO\�for shaping different species but also for their role in the HYROXWLRQ� RI� PLFUREHV�� 3DUWLFXODUO\�� ZKHQ� WKH� FU\SWLF� OLQ-eage of one species has formed and readies itself to adapt to different niches, periodic selective sweeps could, in theory lead to a new species boundary. Therefore, it is a reasonable hypothesis that the genetic diversity of prokaryotes corre-spond to some kinds of ecological diversity, which in turn, are likely the natural force to generate new genetic diversity.

Understanding microbial speciation

The genomes of micro-organisms have been continuously HYROYLQJ� HYHU� VLQFH� WKH�RULJLQDWLRQ�RI� OLIH��$V� WKH�NH\�G\-namic force of molecular evolution, most of the single nu-cleotide mutations were neutral when they occurred but then HLWKHU�ORVW�RU�¿[HG�LQ�D�SRSXODWLRQ�YLD�JHQHWLF�GULIW��.LPXUD��������5HHYHV��������DQG�RU�ZLSHG�RXW�E\�SHULRGLF�VHOHFWLRQ��&RKDQ� DQG� 3HUU\�� ������� 2YHU� ORQJHU� HYROXWLRQDU\� WLPH��those “neutral” variations could also have contributed to speciation, especially for accumulating the divergence of JHQRPHV��2Q�WKH�RWKHU�KDQG��DGDSWLQJ�WR�YDULRXV�DQG�FRP-plicated ecological niches, populations were under natural selection which eventually may favor genes encoding new functions that are seemingly unnecessary or even hazardous

RU�JHQHWLF�HOHPHQWV�EHLQJ�VLOHQFHG�RU�UHGXFHG��$UEHU��������&DSRUDOH���������$FWXDOO\�� WKH�KLVWRU\�RI�HYROXWLRQ�ZDV� UH-corded not only by mutations in genetic sequences known DV� VLQJOH� QXFOHRWLGH� YDULDWLRQV� �619V�� RU� SRO\PRUSKLVPV��613V��� EXW� DOVR� E\� YDULRXV� W\SHV� RI�PRUH� FRPSOH[�'1$�alterations, which sculpted prokaryotic chromosomes more VLJQL¿FDQWO\��'RROLWWOH�DQG�=KD[\ED\HYD���������%DVHG�RQ�the type of genetic material transferred, the genome could have evolved via vertical and/or lateral inheritances.

6SHFLDWLRQ� RI� SURNDU\RWHV� RFFXUV� LQ� WZR� IRUPV�� 9HUWLFDO�LQKHULWDQFH� RFFXUV� DFFRUGLQJ� WR� WKH�'DUZLQLDQ�0HQGHOLDQ�PRGHO�RI�SDUHQW�WR�RIIVSULQJ�JHQH�ÀRZ��L�H��DQ�RUJDQLVP�UH-ceives genetic material from its ancestor, the species from ZKLFK�LW�KDV�HYROYHG��+RZHYHU��WKLV�KDV�EHHQ�VHYHUHO\�FKDO-lenged by the quantitative and qualitative importance of ge-netic transfers between lineages, i.e. horizontal gene transfer �+*7�� �&KDUOHERLV� HW� DO��� �������+HQFH�� WKH� SDUDGLJPDWLF�shift from a monistic to a pluralistic understanding of the evolutionary processes is illustrated by a graph-theoretical VKLIW��IURP�WUHHV��L�H��FRQQHFWHG�DF\FOLF�JUDSKV��WR�QHWZRUNV��L�H�� FRQQHFWHG� JUDSKV� ZKLFK� PD\� FRQWDLQ� UHWLFXODWLRQV���%DSWHVWH�HW�DO����������+RZHYHU��WKLV�NLQG�RI�HYROXWLRQDU\�network seems to be complex particularly at lower levels, EHFDXVH�+*7�RFFXUV�IUHTXHQWO\�DPRQJ�FORVHO\�UHODWHG�LQGL-viduals and species, and more rarely between genealogical-O\�GLVWDQW�UHODWLYHV��$QGDP�DQG�*RJDUWHQ���������$FWXDOO\��+*7�FRXOG�EH�DQ�LPSRUWDQW�HOHPHQW�LQ�VKDSLQJ�WKH�SRSXOD-tion structure of bacterial species, and it indicates that bacte-rial speciation might present a reticulate evolutionary his-WRU\��&DUGD]]R�HW�DO����������,Q�DGGLWLRQ��WKH�VLPLODU�KDELWDW�and the close geographical distance between the donor and the recipient for their genetic material exchange seem to be DQRWKHU�UHTXLUHPHQW�IRU�WKH�RFFXUUHQFH�RI�+*7��3HDUVRQ�HW�DO���������/XR�HW�DO����������,Q�IDFW��HYHQ�ZKHQ�WKH�FRPSOLFD-tion brought by lateral inheritance was excluded, the phylo-genetic incongruence of orthologous genes implied that they SUREDEO\�KDYH�D�GLIIHUHQW�HYROXWLRQDU\�KLVWRU\��%DSWHVWH�HW�DO���������� ,QGHHG��HPSOR\LQJ�GLIIHUHQW� WUHH� UHFRQVWUXFWLRQ�methods may give rise to a non-negligible statistically sig-QL¿FDQW�LQFRQJUXHQFH��-HIIUR\�HW�DO���������

By using traditional chemotaxonomic approaches, which provided merely phenotypic evidence to distinguish the sub-MHFW�IURP�RWKHU�UHIHUHQFHV��LW�LV�GLI¿FXOW�WR�UHYHDO�DQG�XQGHU-stand the speciation of prokaryotes or to answer the question DERXW�ZKDW�FDXVHG�WKHVH�GLIIHUHQFHV��2Q�WKH�RWKHU�KDQG��WKH�molecular phylogeny of an organism is typically based on a VLQJOH�JHQH��XVXDOO\�WKH���6�U51$�JHQH��RU�UHFUXLWLQJ�RWKHU�housekeeping genes, while the effect of the environmen-WDO�SUHVVXUH� UHODWHG�+*7V�DUH�XVXDOO\� LJQRUHG��$OWKRXJK�D�statistically well-supported tree would be obtained, we still

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129The Bulletin of BISMiS

Xiao-Yang Zhi, Wei Zhao, Wen-Jun Li and Guo-Ping Zhao

need to better understand what happened to result in the two bifurcated branches.

Integrating the extensive biological knowledge of taxa

$QVZHUV� RI� ZKDW� H[DFWO\� KDSSHQV� ZKHQ� VSHFLHV� GLYHUJH�from their ancestor, and what the similarities or differences of the biological characteristics are among the diverse spe-cies are important for a complete taxonomic study. The ge-nomic diversity contained in pan-genome of a species may be substantial and these data must be summarized within a species description for the purpose of taxonomy. In practice, all genes belonging to the pan-genome can be divided into WZR�SDUWV��RQH�FRQWDLQV�RUWKRORJRXV�JHQHV��LQFOXGLQJ�SDUDO-RJRXV�JHQHV���DQRWKHU�FRQWDLQV�VSHFL¿F�JHQHV�RI�RQH�VWUDLQ�RU� D� JURXS� �QRW� DOO�� RI� VWUDLQV�� 7R� VXPPDUL]H� WKH� VKDUHG�genes within the description for a species, the orthologous DQG�SDUDORJRXV�JHQHV�VKRXOG�EH�LGHQWL¿HG�E\�ELRLQIRUPDWLF�WRROV�¿UVWO\��DQG�WKHQ�PDSSHG�LQ�GLIIHUHQW�SKHQRW\SLF��PH-tabolism and physiology, etc.) pathways and even networks �VHH� %DURQD�*yPH]� HW� DO��� ������� 7KHUHIRUH�� WKH� HYHU�LQ-creasing genomic information will be helpful not only for delineating a more accurate and precise phylogenetic rela-tionship of a species, but also for truly understanding the biology concealed in the prokaryotic systematics.

In the era of chemotaxonomy, chemical characteristics of metabolism, growth, differentiation and cellular compo-nents such as cell wall and membrane constituents were FRPPRQO\� XVHG� SKHQRW\SHV� IRU� EDFWHULDO� LGHQWL¿FDWLRQ��QRWDEO\� LQ� *UDP�VWDLQ�SRVLWLYH� DFWLQRP\FHWHV�� +RZHYHU��analysis and comparison of these chemical indices makes LW�DQ� LQHI¿FLHQW�DQG�RQHURXV� WDVN� LQ�PDQ\�FDVHV��:LWK� WKH�assistance of whole genome sequence information, it is be-coming realistic to gradually correlate the chemotaxonomic phenotypes with the molecular genotypes of the correspond-LQJ� WD[D�� SDUWLFXODUO\�� VSHFLHV� DQG� VXEVSHFLHV� �6XWFOLIIH��������=KDR� HW� DO��� �������2I� FRXUVH�� DW� WKLV�PRPHQW�� LW� LV�VWLOO�GLI¿FXOW�WR�DFKLHYH�WKLV�ZRUWK\�DLP�LQ�SUDFWLFH��EHFDXVH�WKH�JHQH�H[SUHVVLRQ�SUR¿OHV�IRU�VRPH��PD\EH�PRVW�RI��WKH�phenotypes heavily rely on the related signal transduction and regulatory systems both encoded by their corresponding genes and depends on their interactions with environmen-tal signals. For those phenotypes determined by multiple genes and their interactions under different environmental conditions, although comparative and functional genomic analyses and epigenetic studies are designed to elucidate the molecular mechanism in order to understand and fur-ther control the processes in a quantitative manner, it is not easy to develop a precise and stable correlation as a criterion IRU�WD[RQRP\�DW�WKLV�PRPHQW��+RZHYHU��RQ�RQH�KDQG��WKHVH�

relationships eventually will be established with increas-LQJ�DFFXUDF\�DQG�SUHFLVLRQ��2Q�WKH�RWKHU�KDQG��PRVW�RI�WKH�phenotypes included in polyphasic taxonomy are relatively stable and qualitative and therefore, their exact relation-ship with genotypes should be able to be established via ef-forts combining bioinformatic annotation and experimental proof. Finally, via integration of genomic analysis and ge-netic studies with the effort of reanalyzing the physiological characteristics critical for taxonomy, new criteria may arise and even to replace some of the old criteria. In that direction, taxonomy may function not only in describing the species as GH¿QHG�E\�LWV�RULJLQDO�VFRSH��EXW�DOVR�SURYLGHV�IXQGDPHQWDO�research schema to facilitate the study of physiology and ecology related to the subject taxa.

2QH�VXFFHVVIXO�H[DPSOH�LV�WKH�FRUUHODWLRQ�RI�EDFWHULDO�VHUR-types with their genetic make-ups. Classically, serology was XVHG�WR�QDPH�SDWKRJHQV��VXFK�DV�a�����³VSHFLHV´�RI�Salmo-nella in the early editions of Bergey’s Manual��$OWKRXJK�E\�������WKH�VSHFLHV�QXPEHU�KDG�EHHQ�UHGXFHG�WR�a���VHURW\SHV�still maintained as the criteria not only for Salmonella but DOVR�IRU�WKH�LGHQWL¿FDWLRQ�RI�Escherichia�FOLQLFDO�LVRODWHV��H�J��2����RU�2����RI�WKH�(QWHURKHPRUUKDJLF�Escherichia coli/(+(&��LQ�WKH�VWXG\�RI�HSLGHPLRORJ\�IRU�VXUYHLOODQFH��%HX-WLQ�HW�DO���������6ZLWW�HW�DO����������'XH� WR� LWV� WHGLRXV� WHVW-ing procedure and the numerous special reagents required, it is exciting progress in developing a simple and convenient method for rapid bacterial serotyping via genetic analysis based on genomic information, which correlates the gene FOXVWHUV��RU�JHQHV��WR�WKH�V\QWKHVLV�RI�FRUUHVSRQGLQJ�EDFWH-ULDO�VXUIDFH�DQWLJHQ��/LX�HW�DO����������5HFHQWO\��VHURW\SHV�RI�several bacteria like Vibrio parahemolyticus, Proteus and Cronobacter sakazakii ZHUH�VKRZQ�WR�EH�LGHQWL¿HG�E\�XVLQJ�WKLV�DSSURDFK�DV�ZHOO��2NXUD�HW�DO���������:DQJ�HW�DO���������6XQ�HW�DO���������

$V�ZH�KDYH�HPSKDVL]HG��SURNDU\RWLF�WD[RQRP\�LV�DQ�HVVHQ-WLDO�VXEGLVFLSOLQH�RI�PLFURELRORJ\��$OWKRXJK�LWV�WD[D�VKRXOG�be organized in a phylogenetic network, the biological characteristics encoded by the genome may not be revealed unless comparative and functional genomic analyses are executed that match with their phenotypes. This kind of bio-logical knowledge, integrated into the phylogenomic back-bone of taxonomy may further facilitate biology research in general, including those originally impossible cases of un-cultured bacteria with their genome sequence derived from metagenomic sequencing.

Approaching the ultimate aim of prokary-otic taxonomy

In summary, prokaryotic taxonomy is a subject fundamental

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130 The Bulletin of BISMiS

Working towards a Molecular Systematics Library for Prokaryotes

IRU�H[SORULQJ�PLFURELDO�ZRUOG�RQ�(DUWK��DQG�DQVZHULQJ�WKH�questions about what they are, how diverse they are, and what relationships exist among them. Taxonomy shares in-tricate relationships with other disciplines in microbiology DQG� HYHQ� RWKHU� ¿HOGV� RI� ELRORJ\��7KLV� HVVHQFH�PDNHV� WKH�boundaries between taxonomy and other disciplines am-biguous sometimes, which, in our opinion, is good for the development of taxonomy. For instance, although ecologi-cal investigations usually go beyond the scope of taxonomy, prokaryotic taxonomy is the inevitable basis for ecology ZLWK�UHJDUG�WR�GH¿QLQJ�WKH�PLFURELDO�GLYHUVLW\�LQ�RQH�NLQG�RI�unexploited environment via the description of taxonomic positions of prokaryotes detected by any method. While the population genetic study of one bacterial species, either a pathogen or a commensal relative to human beings, not only SUHVHQWV� D� SRWHQWLDO� URXWH� RI� PLFURHYROXWLRQ� �H�J�� 6WXNHQ-EURFN�HW�DO���������7DNXQR�HW�DO����������EXW�DOVR�SURYLGHV�YDOXDEOH�LQIRUPDWLRQ�IRU�WKH�XQGHUVWDQGLQJ�RI�VSHFLDWLRQ��H�J��/XR�HW�DO���������=KDQJ�HW�DO����������7KH�UHODWLRQVKLS�RI�WKLV�NLQG�RI�JHQHWLF�VWXG\�ZLWK�WD[RQRP\�PLJKW�EH�UHÀHFWHG�DW�the level of speciation, which was usually ignored by tradi-WLRQDO�WD[RQRP\��3KLORVRSKLFDOO\��WKHUH�DUH�WZR�HOHPHQWDU\�substances in the theoretic system that discriminates taxono-P\�IURP�RWKHU�VXEGLVFLSOLQHV�RI�PLFURELRORJ\��2QH�LV�WKH�HO-HPHQW��L�H��VSHFLHV�RU�SRSXODWLRQ��WKDW�PDNHV�XS�WKH�V\VWHP��while the other is the connection, referring in particular to the evolutionary relationships, among the elements. In fact, all taxonomic studies circumfuse this theoretic system, to ZKLFK�DOO�SUDFWLFDO�DUHDV��QRPHQFODWXUH��LGHQWL¿FDWLRQ��DQG�FODVVL¿FDWLRQ��RI�WD[RQRP\�RIIHU�WKHLU�VHUYLFHV�WR�VROYH�WKH�VFLHQWL¿F�TXHVWLRQV�DERXW�WKHVH�WZR�REMHFWV��7KHUHIRUH��WKH�ultimate aim of prokaryotic taxonomy is to establish a ratio-nal and hierarchical system to accommodate the micro-or-ganisms with huge biological diversity, which may facilitate research aiming at answering the above questions. In turn, the results of these studies will provide further information for understanding and improving the system, and prompting other subdisciplines in microbiology.

The present taxonomic system has been organized as a book, dictionary or encyclopedia, such as Bergey’s Manual of Sys-tematic Bacteriology�� �QG� HGLWLRQ� �%RRQH� DQG�&DVWHQKRO]��������%UHQQHU� HW� DO��� ������'H�9RV� HW� DO��� ������.ULHJ� HW�DO��� ������*RRGIHOORZ� HW� DO��� ������� ZKRVH� IUDPHZRUN� UH-OLHV�PDLQO\�RQ�WKH�SK\ORJHQ\�RI�WKH���6�U51$�JHQH��8S�WR�date, it has successfully managed to include all prokaryotic PLFUREHV�� +RZHYHU�� VHYHUDO� LVVXHV� KDYH� DULVHQ� WR� SHUWXUE�the current system. Firstly, the information included in the traditional taxonomic book is limited due to narrow range RI�JHQH�LQIRUPDWLRQ����6�51$�DQG�'1$±'1$�K\EULGL]D-tion) that was used to construct the phylogenetic framework. 6HFRQGO\��LQ�PDQ\�FDVHV��WKH�SKHQRW\SHV�XVHG�IRU�GHVFULELQJ�

different taxa are yet to be correlated with their encoding genotypes. Finally, the seeming segregation of phylogeny from their biological traits of taxa has made it more and more complex in description rather than rational in their natural history. Therefore, we believe it is important to em-phasize to understand the nature of species and why they exist, not only what the differences are among them. For UHFRJQL]LQJ�D�VLQJOH�PLFUR�RUJDQLVP��D�SRSXODWLRQ�DFWXDOO\���we should move our sight into the cell and observe what happens there and understand why, by using more and more genomic and epigenomic information associated with their DPELHQW�HQYLURQPHQWDO�FRQGLWLRQV��$ORQJ�ZLWK�RXU�LQFUHDV-ing knowledge learned from phylogenomic analysis of the species via large scale sequencing efforts, more important or FULWLFDO�ELRORJLFDO�WUDLWV��SKHQRW\SHV��UHYHDOHG�E\�JHQRPLF��functional genomic and/or proteomic analyses and related experimental studies should be involved in the criteria for taxonomy.

For approaching the ultimate goal of prokaryotic taxonomy and making it integrative and comprehensive rather than limited in both the phylogeny and biological knowledge of WD[D��ZH�DUH�SURSRVLQJ�D�ZHE�EDVHG�RSHQ�VRXUFH�³0ROHFX-ODU� 6\VWHPDWLFV� /LEUDU\� RI� 3URNDU\RWHV´� WR� DFFRPPRGDWH�all species supported by the backbones of their genomic phylogeny and enriched by their related biological and eco-ORJLFDO�NQRZOHGJH��$FWXDOO\��WKLV�/LEUDU\�FRXOG�KDYH�D�JUHDW�LPSDFW�WR�WKH�UHQRYDWLRQ�RI�WKH�FXUUHQW�FODVVL¿FDWLRQ�V\VWHP��,W�UHFUXLWV�PRUH�LQIRUPDWLRQ��JHQHV��IURP�JHQRPH��H�J��FHQ-tral metabolic pathway related genes in addition to genes LQYROYHG�LQ�'1$�UHSOLFDWLRQ��UHFRPELQDWLRQ�DQG�UHSDLU�� WR�HVWDEOLVK� WKH�EDFNERQH�IRU�FODVVL¿FDWLRQ��DQG�WKXV��ZLOO�EH�more comprehensive with regarding to the knowledge of biodiversity.

$W�WKLV�PRPHQW��DOWKRXJK�WKLV�SURSRVDO�LV�UDWKHU�LPDJLQDWLYH�than practical due to limitations of both the availability of enough genome sequences targeting most species that are broadly distributed among the current prokaryotic taxa and DFFXUDWH�JHQRW\SH±SKHQRW\SH�DQQRWDWLRQV�DW�DOO�OHYHOV�RI�EL-ology, ranging from phylogeny to physiology. We recognize that the annotations for genes of genomes currently avail-able often lead to confused or incorrect inferences regarding WKH�UROH�RI�VSHFL¿F�JHQH�SURGXFWV��7KHUHIRUH��ERWK�FKDOOHQJ-es and opportunities are present for today’s prokaryotic tax-onomists. First, a genome-scale metabolic network should be reconstructed with respect to the taxonomic, particularly the chemotaxonomic, characteristics of taxa. The genotypes ELRLQIRUPDWLFDOO\� DQQRWDWHG� VKRXOG� EH� YHUL¿HG� DQG� WUDQV-lated into taxonomic phenotypes. In addition, when some of the phenotypes cannot be accurately correlated with the genotypes directly, tools of functional genomics should be

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131The Bulletin of BISMiS

Xiao-Yang Zhi, Wei Zhao, Wen-Jun Li and Guo-Ping Zhao

employed to study the relationship at the epigenomics lev-HO��6HFRQG��DOO� VKDUHG�JHQHV� �RUWKRORJV��DPRQJVW�GLIIHUHQW�species under one superior taxon could be used to estab-OLVK� D� QHZ� IUDPHZRUN� �D� WKHRUHWLF� V\VWHP���ZKLFK� VKRXOG�EH�UHSHDWHGO\�YHUL¿HG�E\�DGGLWLRQDO�JHQRPH�VHTXHQFHV�DQG�biological information/knowledge. Finally, with the aid of bioinformatics, systems biology and phylogenomics will continuously enrich our biological and evolutionary knowl-edge of the subject species, which, to a certain extent, might EH�WUDQVIRUPHG�WR�³QRYHO´�SKHQRW\SHV�LQÀXHQFLQJ�WKH�FULWH-ULD�IRU�WD[RQRPLF�FODVVL¿FDWLRQ�DQG�LGHQWL¿FDWLRQ�DQG�WKXV��IXUWKHU�HQULFKLQJ�RU�LPSURYLQJ�WKH�/LEUDU\��,Q�VXPPDU\��ZH�VWURQJO\�EHOLHYH� WKDW� DFFXUDWH� DQQRWDWLRQ�RI� IXQFWLRQ�V��RI�JHQH�V��RI�WKH�JHQRPHV�ZLOO�EH�RQH�RI�WKH�PDMRU�WDVNV�RI�IX-ture “genomic taxonomy”. This emerging discipline should attract more bioinformaticians, genomics scientists and mi-crobial geneticists to work closely with the taxonomists to HVWDEOLVK�WKH�0ROHFXODU�6\VWHPDWLFV�/LEUDU\�IRU�3URNDU\RWHV��:H�DOVR�VWURQJO\�EHOLHYH�WKDW�WKLV�HIIRUW�ZLOO�EHQH¿W�QRW�RQO\�the taxonomy but also the biological research for microbes in general.

)RXU�GHFDGHV�DJR��&RZDQ��������VDLG��³7RR�PXFK�DWWHQWLRQ�has been given to nomenclature and too little to the bacteria WKHPVHOYHV�� WKHLU�FKDUDFWHUV��DQG�ZKDW� WKH\�GR�´�$OWKRXJK�the situation has been changing ever since, there still is a ORQJ�GLVWDQFH� WR� WKH� LGHDO�GHVWLQDWLRQ��$W� WKLV�PRPHQW��ZH�may take advantage of genomics and the genome informa-tion it provides to change the status quo of “Too much atten-tion has been given to the difference of microbial characters and too little to what they do either in the cell or in the envi-ronment.” We believe that prokaryotic taxonomy will truly become an essential discipline of biology again as it was in the dawn of modern science.

Rise of the Phoenix, Born of Fire.

Acknowledgements

7KLV�UHVHDUFK�ZDV�VXSSRUWHG�E\�WKH�1DWLRQDO�%DVLF�5HVHDUFK�3URJUDP�RI�&KLQD������&%�������DQG�����&%���������WKH�1DWLRQDO�1DWXUDO�6FLHQFH�)RXQGDWLRQ�RI�&KLQD� ����������DQG�����������DQG�WKH�5HVHDUFK�8QLW�)XQG�RI�/L�.D�6KLQJ�,QVWLWXWH�RI�+HDOWK�6FLHQFHV������������:H�WKDQN�3URIHVVRU�-DPHV�7��6WDOH\�IRU�KLV�KHOSIXO�FRPPHQWV�RQ�RXU�PDQXVFULSW��$QG�ZH�DOVR�DSSUHFLDWH�WKH�FRPPHQWV�PDGH�E\�'U�6KXKXD�;X�DW�&$6�03*�3DUWQHU� ,QVWLWXWH� IRU�&RPSXWDWLRQDO�%LRO-RJ\�� 6KDQJKDL� ,QVWLWXWHV� IRU� %LRORJLFDO� 6FLHQFHV�� &KLQHVH�$FDGHP\�RI�6FLHQFHV�

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$QGDP��&�3��DQG�-�3��*RJDUWHQ��������%LDVHG�JHQH�WUDQVIHU�LQ�PLFURELDO�HYROXWLRQ��1DW��5HY��0LFURELRO��9:����±����

$UEHU��:��������*HQHWLF�YDULDWLRQ��PROHFXODU�PHFKDQLVPV�DQG� LPSDFW� RQ� PLFURELDO� HYROXWLRQ�� )(06� 0LFURELRO��Rev. 24:��±��

%DSWHVWH��(���(�� 6XVNR�� -��/HLJK��'��0DF/HRG��5�/��&KDU-OHERLV� DQG�:�)�� 'RROLWWOH�� ������ 'R� RUWKRORJRXV� JHQH�SK\ORJHQLHV� UHDOO\� VXSSRUW� WUHH�WKLQNLQJ"� %0&� (YRO��Biol. 5:����

%DSWHVWH�� (���0�$��2¶0DOOH\��5�*��%HLNR��0�� (UHVKHIVN\��-�3��*RJDUWHQ��/��)UDQNOLQ�+DOO��)�-��/DSRLQWH�� -��'XSUH��7��'DJDQ��<��%RXFKHU�DQG�:��0DUWLQ��������3URNDU\RWLF�evolution and the tree of life are two different things. Biol. Direct. 4:����

%DURQD�*yPH]�� )��� 3�� &UX]�0RUDOHV� DQG� /�� 1RGD�*DUFtD��������:KDW�FDQ�JHQRPH�VFDOH�PHWDEROLF�QHWZRUN�UHFRQ-VWUXFWLRQV� GR� IRU� SURNDU\RWLF� V\VWHPDWLFV"�$QWRQLH� YDQ�/HHXZHQKRHN��101:���±���

%HXWLQ��/���$��0LNR��*��.UDXVH��.��3ULHV��6��+DE\��.��6WHHJH�DQG� 1�� $OEUHFKW�� ������ ,GHQWL¿FDWLRQ� RI� KXPDQ�SDWKR-JHQLF� VWUDLQV�RI�6KLJD� WR[LQ�SURGXFLQJ�Escherichia coli from food by a combination of serotyping and molecular W\SLQJ� RI� 6KLJD� WR[LQ� JHQHV��$SSO�� (QYLURQ��0LFURELRO��73:�����±�����

%RRQH��'�5�� DQG�5�:��&DVWHQKRO]� �HGLWRUV��� ������ In Ber-JH\¶V�0DQXDO�RI�6\VWHPDWLF�%DFWHULRORJ\���QG�HGQ��YRO�����The Archaea�DQG�WKH�'HHSO\�%UDQFKLQJ�DQG�3KRWRWURSKLF�Bacteria��6SULQJHU��1HZ�<RUN�

%UHQQHU��'�-���1�5��.ULHJ�DQG�-�7��6WDOH\��HGLWRUV���������In %HUJH\¶V� 0DQXDO� RI� 6\VWHPDWLF� %DFWHULRORJ\�� �QG� HGQ��YRO�����7KH�Proteobacteria��6SULQJHU��1HZ�<RUN�

&DSRUDOH��/�+��������1DWXUDO�VHOHFWLRQ�DQG�WKH�HPHUJHQFH�RI�D�PXWDWLRQ�SKHQRW\SH��DQ�XSGDWH�RI� WKH�HYROXWLRQDU\�synthesis considering mechanisms that affect genome YDULDWLRQ��$QQX��5HY��0LFURELRO��57:����±����

&DUGD]]R��%���(��1HJULVROR��/��&DUUDUR��/��$OEHUJKLQL��7��3D-WDUQHOOR�DQG�9��*LDFFRQH��������0XOWLSOH�ORFXV�VHTXHQFH�typing and analysis of toxin genes in Bacillus cereus food-ERUQH�LVRODWHV��$SSO��(QYLURQ��0LFURELRO��74:����±����

&KDQ��0�6���0�&��0DLGHQ�DQG�%�*��6SUDWW��������'DWDEDVH�GULYHQ�PXOWL�ORFXV�VHTXHQFH�W\SLQJ��0/67��RI�EDFWHULDO�pathogens. Bioinformatics. 17:�����±�����

&KDUOHERLV��5�/���5�*��%HLNR� DQG�0�$��5DJDQ�� ������0L-FURELDO�SK\ORJHQRPLFV��EUDQFKLQJ�RXW��1DWXUH��421:�����

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&RKDQ��)�0��DQG�(�%��3HUU\��������$�V\VWHPDWLFV�IRU�GLVFRY-ering the fundamental units of bacterial diversity. Curr. Biol. 17:�5���±5����

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132 The Bulletin of BISMiS

Working towards a Molecular Systematics Library for Prokaryotes

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/DEHGD��'�3��������0XOWLORFXV�VHTXHQFH�DQDO\VLV�RI�SK\WR-pathogenic species of the genus Streptomyces��,QW��-��6\VW��(YRO��0LFURELRO��61:�����±�����

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133The Bulletin of BISMiS

Xiao-Yang Zhi, Wei Zhao, Wen-Jun Li and Guo-Ping Zhao

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5RQJ��;��DQG�<��+XDQJ��������7D[RQRPLF�HYDOXDWLRQ�RI�WKH�Streptomyces griseus clade using multilocus sequence DQDO\VLV�DQG�'1$±'1$�K\EULGL]DWLRQ��ZLWK�SURSRVDO�WR�FRPELQH����VSHFLHV�DQG�WKUHH�VXEVSHFLHV�DV����JHQRPLF�VSHFLHV��,QW��-��6\VW��(YRO��0LFURELRO��60:����±����

6WDFNHEUDQGW��(���)�$��5DLQH\�DQG�1�/��:DUG�5DLQH\��������3URSRVDO�IRU�D�QHZ�KLHUDUFKLF�FODVVL¿FDWLRQ�V\VWHP��Acti-nobacteria�FODVVLV�QRY��,QW��-��6\VW��%DFWHULRO��47:����±����

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6XQ��<���0��:DQJ��+��/LX��-��:DQJ��;��+H��-��=HQJ��;��*XR��.�� /L��%��&DR� DQG�/��:DQJ�� ������'HYHORSPHQW� RI� DQ�2�DQWLJHQ�VHURW\SLQJ�VFKHPH�IRU�Cronobacter sakazakii.

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134 The Bulletin of BISMiS

Working towards a Molecular Systematics Library for Prokaryotes

)DQ��=��4LQ��<��+X��%��=KX��6��:DQJ��;��'LQJ�DQG�*��3��=KDR�������&RPSOHWH�JHQRPH�VHTXHQFH�RI�WKH�ULIDP\FLQ�69�SURGXFLQJ�Amycolatopsis mediterranei�8���UHYHDOHG�its genetic characteristics in phylogeny and metabolism. Cell Res. 20:�����±�����

=KL��;��<���:��-��/L�DQG�(��6WDFNHEUDQGW��������$Q�XSGDWH�RI�WKH�VWUXFWXUH�DQG���6�U51$�JHQH�VHTXHQFH�EDVHG�GH¿QL-tion of higher ranks of the class Actinobacteria, with the proposal of two new suborders and four new families and HPHQGHG�GHVFULSWLRQV�RI� WKH�H[LVWLQJ�KLJKHU� WD[D�� ,QW�� -��6\VW��(YRO��0LFURELRO��59:����±����

Page 53: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

135© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 135–139

Contact detailsDepartment of Microbiology, University of Georgia, Athens GA 30602-2605, USA.

[email protected]

The International Code of Nomenclature of Prokaryotes was a major achievement of the last century. By establishing a clear set of rules, it allowed biologists with many different interests and backgrounds to communicate effectively. Furthermore, it made prokaryotic systematics straightforward and acces-sible. While the Code itself only governs nomenclature and not systematics or taxonomy, many of the minimal standards for descriptions of taxonomic groups proposed by the Ad Hoc Subcommittees far exceed the requirements of the Code and are contrary to both its explicit intent and spirit. They are exclusionary and prevent biologists with serious interests in prokaryotes from describing novel spe-cies. The likely consequences of the widespread implementation of these standards are that many bi-ologists will no longer validate the names of newly described prokaryotes and the literature will once again be full of names of uncertain meaning. Within this context, the application of minimal standards for the evaluation of taxonomic descriptions by journals is an editorial decision and not authorized by the Code. With the availability of inexpensive DNA sequencing, prokaryotic species could be routinely GHVFULEHG�EDVHG�XSRQ�WKHLU�JHQRPLF�VHTXHQFHV��7KHVH�GHVFULSWLRQV�ZRXOG�IXOÀO�DOO�WKH�UHTXLUHPHQWV�of the Code and provide a wealth of insight into the nature of prokaryotes. For these reasons, the genomic sequence should be included in the initial description of novel species whenever practical.

William B. Whitman

Intent of the nomenclatural Code and recommendations about naming new species based on genomic sequences

7KH� GHYHORSPHQW� RI� WKH� ,QWHUQDWLRQDO� &RGH� RI� 1RPHQFOD-WXUH�RI�3URNDU\RWHV��IRUPHUO\�WKH�,QWHUQDWLRQDO�&RGH�RI�1R-menclature of Bacteria), hereafter called the Code, was a major achievement in the study of prokaryotes. First pub-OLVKHG� LQ������ �%XFKDQDQ�HW� DO��� ������� LW� UHVXOWHG� IURP�D�keen appreciation of the importance of nomenclature. By establishing a clear set of rules, it allowed biologists with many different interests and backgrounds to communicate effectively. It made prokaryotic systematics straightforward DQG�DFFHVVLEOH�WR�DOO�ELRORJLVWV��2QH�QR�ORQJHU�KDG�WR�EH�D�specialist to characterize and describe new micro-organisms.

Historical background for writing the Code

The fact that nomenclature seems unimportant today is probably a direct consequence of the success of the Code, and many of the problems it was designed to address no ORQJHU� H[LVW�� +RZHYHU�� HDUO\� LQ� WKH� ODVW� FHQWXU\� WKH� VLWXD-tion was entirely different. The perspective at that time was clearly described by Robert Breed in his presidential address WR�WKH�6RFLHW\�RI�$PHULFDQ�%DFWHULRORJLVWV�LQ�������%UHHG���������%UHHG�ZDV�RQH�RI�WKH�DXWKRUV�RI�WKH�RULJLQDO�FRGH�DQG�

VHUYHG� DV�&KDLUPDQ� RI�%HUJH\¶V�0DQXDO�7UXVW� IURP������WR�������7KHUHIRUH��KH�ZDV�YHU\�NQRZOHGJHDEOH�DERXW� WKH�QRPHQFODWXUH�RI�SURNDU\RWHV��+H�SRLQWV�RXW�WKDW�HDUO\�ELROR-JLVWV�VXFK�DV�/LQQp��������JURXSHG�WKH�SURNDU\RWHV� LQ� WKH�genus Chaos�� UHÀHFWLQJ� WKH� QHDUO\� FRPSOHWH� LJQRUDQFH� RI�WKHLU� SURSHUWLHV��(YHQ�E\� WKH�����V�� WKH� VLWXDWLRQ�ZDV�QRW�much improved. Robert Buchanan, also a co-author of the RULJLQDO�&RGH�DQG�&KDLUPDQ�RI�%HUJH\¶V�0DQXDO�7UXVW�IURP������WR������VWDWHG�WKDW�³WKH�FODVVL¿FDWLRQ�RI�EDFWHULD�LV�LQ�D�FKDRWLF�FRQGLWLRQ´��%XFKDQDQ���������$W�WKDW�WLPH��PDQ\�still argued that prokaryotes did not possess stable charac-teristics and could not be grouped into species in the same ZD\�WKDW�SODQWV�DQG�DQLPDOV�ZHUH�FODVVL¿HG��%UHHG���������Rules taken for granted today, such as the “law of prior-LW\´� ZHUH� QRW� ZLGHO\� UHFRJQL]HG�� .H\� SXEOLFDWLRQV� ZHUH�frequently unavailable, either because they were published in unfamiliar languages, not properly cited, or in journals with very limited circulation. The concept of nomenclatural W\SHV�ZDV�QRW�ZLGHO\�DSSOLHG��6LPLODUO\��WKH�GHVFULSWLRQV�RI�many prokaryotes were often so vague that they could refer to multiple micro-organisms.

The absence of a nomenclatural system caused these enor-PRXV�GLI¿FXOWLHV��)RU�LQVWDQFH��WKH�ODZ�RI�SULRULW\�DVVRFLDWHV�WKH�QDPH�ZLWK� WKH�¿UVW�SXEOLVKHG�GHVFULSWLRQ�RI� WKH� WD[RQ��Without this law, it is possible to use a name to mean an-other taxon or create another name for the same taxon, a practice which used to be commonplace. For instance, the

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136 The Bulletin of BISMiS

Intent of the nomencaltural Code

genus Bacterium was proposed multiple times to refer to YHU\� GLIIHUHQW� PLFUR�RUJDQLVPV� �%UHHG�� ������� )LUVW� SUR-SRVHG�E\�(KUHQEHUJ�LQ������WR�GHVLJQDWH�YDULRXV�VSHFLHV�RI�URGV��VXEVHTXHQW�ZRUNHUV�ZHUH�XQDEOH�WR�¿JXUH�RXW�H[DFWO\�ZKDW�(KUHQEHUJ�GHVFULEHG��,Q�������/HKPDQQ�DQG�1HXPDQQ�WKHQ�XVHG�WKH�WHUP�IRU�QRQVSRUHIRUPLQJ�URGV��DQG�LQ������0LJXOD�XVHG�LW�WR�UHIHU�WR�VSRUHIRUPLQJ�URGV��,Q�������:LQ-slow et al. used it for the colon group with B. coli as the type and listed as synomyms Tyrothrix, Actinobacter� �LQ� SDUW���Klebsiella� �LQ� SDUW���Gliscrobacterium, Aerobacter, Salmo-nella, Pyobacillus��DQG�D�IHZ�RWKHUV��*LYHQ�WKLV�FRQIXVLRQ��the name had little value and was eventually discarded.

The application of priority is possible only when there is consensus as to what constitutes a publication. For this rea-VRQ�� WKH�%DFWHULRORJLFDO�&RGH� ������5HYLVLRQ�� �/DSDJH�HW�DO���������H[SOLFLWO\�VWDWHV�WKDW�D�SXEOLFDWLRQ�IRU�WKH�SXUSRVHV�of nomenclature must be “…generally available, by sale or GLVWULEXWLRQ�� WR� WKH� VFLHQWL¿F� FRPPXQLW\�� SULQWHG� PDWHULDO�IRU� WKH� SXUSRVH� RI� SURYLGLQJ� D� SHUPDQHQW� UHFRUG�´� �5XOH���D��� ,W� DOVR� H[SOLFLWO\� H[FOXGHV� PHHWLQJ� PLQXWHV� DQG� DE-stracts, catalogs of collections, newspaper, and unpublished PDQXVFULSWV��5XOH���E���SUDFWLFHV�ZKLFK�ZHUH�DOVR�FRPPRQ�prior to institution of the Code.

The requirement for valid publication also follows from WKH�ODZ�RI�SULRULW\��1DPHV�DSSHDULQJ�EHIRUH������PXVW�DS-SHDU� RQ� WKH�$SSURYHG�/LVWV� RI�%DFWHULDO�1DPHV� WR� EH�YDO-LGO\�SXEOLVKHG��$IWHU�WKDW�GDWH��QDPHV�PXVW�EH�SXEOLVKHG�LQ�the International Journal of Systematic Bacteriology��,-6%��RU��DIWHU�������WKH�International Journal of Systematic and Evolutionary Microbiology� �,-6(0�� �5XOH� �����9DOLGDWLRQ�requires that descriptions of new taxa published outside the ,-6(0�DSSHDU�RQ�WKH�9DOLGDWLRQ�/LVWV�LQ�WKDW�MRXUQDO��7KLV�rule ensures that the descriptions of new names can be IRXQG� DQG� QRW� XQLQWHQWLRQDOO\� XVHG� DJDLQ��$W� RQH� WLPH�� LW�was common for many universities or regional associations to publish their own journals. By one estimate, there were RYHU�����SXEOLFDWLRQV�LQFOXGLQJ�SDSHUV�RI�LQWHUHVW�WR�QRPHQ-FODWXUH� �6NHUPDQ���������7KLV�FDXVHG�HQRUPRXV�SUREOHPV��)RU� LQVWDQFH��<DVXNH�7HUDVDNL¶V�VXSHUE�GHVFULSWLRQV�RI�VSL-rilla were published in the Bulletin of the Suzugamine Wom-en’s College��7HUDVDNL���������������2QO\�DQ�H[SHUW�RQ�WKHVH�micro-organisms would likely be aware of these or similar publications outside the mainstream literature. Fortunately, LQ� WKLV� FDVH� GHVFULSWLRQV� RI� KLV�PDMRU� WD[RQRPLF� ¿QGLQJV�ZHUH�DOVR�SXEOLVKHG�LQ�WKH�,-6%��7HUDVDNL��������

1RPHQFODWXUDO�W\SHV�ZHUH�RULJLQDOO\�FRQWURYHUVLDO�DQG�RQO\�gradually introduced into common practice. This system re-quires that every name be associated with an example or ³W\SH´�� %UHHG� FUHGLWV� %XFKDQDQ� �%XFKDQDQ�� ����D�� ����E��

����D�� ����E�� ����F�� DV� WKH� ¿UVW� WR� DSSO\� WKH� FRQFHSW� RI�nomenclatural type species consistently in the descriptions RI�JHQHUD� �%UHHG���������7KH��VW�HGLWLRQ�RI�Bergey’s Man-ual�PD\�KDYH�EHHQ�WKH�¿UVW�FRPSUHKHQVLYH�FODVVL¿FDWLRQ�RI�SURNDU\RWHV�WR�GHVLJQDWH�W\SH�VSHFLHV��%HUJH\�HW�DO����������$VVRFLDWLQJ�QDPHV�ZLWK�W\SHV�VWDELOL]HG�WKHLU�XVDJH��+LVWRUL-cal descriptions of many taxa were frequently too vague to GLVWLQJXLVK�VLPLODU�SURNDU\RWHV��$V�PRUH�VRSKLVWLFDWHG�WHVWV�and new taxonomic theories were developed, it became clear that the descriptions could be applied to many differ-HQW�VSHFLHV��1RZ�WKH�QDPHV�UHPDLQHG�DVVRFLDWHG�ZLWK�WKRVH�prokaryotes similar to the type species. The creation of type culture collections to make type strains widely available IROORZHG� ORJLFDOO\� IURP� WKLV� LGHD��1RZ� LW�ZDV�SRVVLEOH� WR�¿[� VSHFLHV� WR� VSHFL¿F�PLFUR�RUJDQLVPV�RU� VDPSOHV��ZKLFK�further reduced the ambiguity. Type strains were not con-VLVWHQWO\� DYDLODEOH� SULRU� WR� WKH� $SSURYHG� /LVWV� RI� %DFWH-ULDO�1DPHV� LQ�������7KLV� OLVW� LQFOXGHG� ODUJHO\�QDPHV�ZLWK�nomenclatural type strains, thus removing nomenclatural VWDQGLQJ�DQG�SULRULW\�RI�WHQV�RI�WKRXVDQGV�RI�QDPHV��6QHDWK�DQG�%UHQQHU���������7KH�VPDOO�QXPEHU�RI�VSHFLHV�ZLWKRXW�type strains was limited to species with distinctive morphol-ogies or other characteristics, such as 3ODQFWRP\FHV�EHNH¿L, and well known symbionts, such as Pasteuria ramosa. Thus, only after this time, was it possible to consistently associ-ate names with actual biological entities, further stabilizing nomenclature.

$OWKRXJK�ZH�UHFRJQL]H�WRGD\�WKDW�WKH�&RGH¶V�V\VWHP�RI�QR-menclature was essential for the development of microbiol-ogy, its implementation took decades. The formation of the ¿UVW� 1RPHQFODWXUDO� &RPPLWWHH� IRU� WKH� ,QWHUQDWLRQDO� 6RFL-HW\�IRU�0LFURELRORJ\��ZKLFK�ODWHU�EHFDPH�WKH�,QWHUQDWLRQDO�8QLRQ�RI�0LFURELRORJLFDO�6RFLHWLHV��RU�,806���ZDV�¿UVW�DX-WKRUL]HG�LQ�������7KH�¿UVW�&RGH�DSSHDUHG�LQ�������%XFKDQ-DQ�HW�DO����������7KH�$SSURYHG�/LVWV�RI�%DFWHULDO�1DPHV�ZDV�QRW�FRPSOHWHG�XQWLO�������6NHUPDQ�HW�DO����������7KH�&RGH�DOVR�XQGHUZHQW�D�PDMRU�UHYLVLRQ� LQ������DQG�KDV�EHHQ�XS-GDWHG�SHULRGLFDOO\��/DSDJH�HW�DO����������)RU�LQVWDQFH��ZLWK�the discovery of the Archaea, the Code was renamed the ,QWHUQDWLRQDO�&RGH�RI�1RPHQFODWXUH�RI�3URNDU\RWHV��DQG�WKH�committee charged with its implementation was renamed WKH�,QWHUQDWLRQDO�&RPPLWWHH�RQ�6\VWHPDWLFV�RI�3URNDU\RWHV��,&63���/DEHGD��������

Intent of the Code

7KH� &RGH� LV� FRPSULVHG� RI� 3ULQFLSOHV�� 5XOHV�� DQG� 5HFRP-PHQGDWLRQV� �%XFKDQDQ� HW� DO��� ������ /DSDJH� HW� DO��� �������7KH�3ULQFLSOHV� IRUP� WKH�EDVLV�RI� WKH�&RGH��7KH�5XOHV� DUH�GHVLJQHG� WR� LPSOHPHQW� WKH� 3ULQFLSOHV� DQG� DUH� ELQGLQJ� RQ�nomenclature. Thus, names that are not consistent with the

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137

William B. Whitman

The Bulletin of BISMiS

Rules have no standing in the Code and are not protected by the law of priority. The Recommendations deal with sub-sidiary points and are intended to serve as guides. They are not binding, and names contrary to the Recommendations cannot be rejected for this reason and can have priority. The SUHDPEOH�WR�WKH�&RGH�DOVR�FRQWDLQV�VRPH�*HQHUDO�&RQVLGHU-ations, which describe the intention of the Code.

Importantly, the Code is for nomenclature and not system-DWLFV�RU� WD[RQRP\��7KLV� LQWHQW� LV� FOHDUO\� VWDWHG� LQ�*HQHUDO�&RQVLGHUDWLRQ����³5XOHV�RI�QRPHQFODWXUH�GR�QRW�JRYHUQ�WKH�delimitation of taxa nor determine their relations. The Rules are primarily for assessing the correctness of names…” �/DSDJH�HW�DO����������/LNHZLVH��3ULQFLSOH���VWDWHV� WKDW� WKH�essential points in nomenclature are stability of names, re-jection of names that cause confusion, and avoidance of the XVHOHVV�FUHDWLRQ�RI�QDPHV��$�IRXUWK�SRLQW�ZDV�UHFHQWO\�DGGHG�>3ULQFLSOH� ����@�� ³1RWKLQJ� LQ� WKLV�&RGH�PD\�EH� FRQVWUXHG�to restrict the freedom of taxonomic thought or action” �'H�9RV� DQG�7U�SHU�� �������/LNHZLVH�� LW� LV� LPSRUWDQW� WKDW�0LQLPDO�6WDQGDUGV�DUH�D�5HFRPPHQGDWLRQ�DQG�QRW�D�5XOH��5HFRPPHQGDWLRQ���E�VWDWHV� WKDW� WKH�³H[DPLQDWLRQ�DQG�GH-VFULSWLRQ��RI�D�QHZ�VSHFLHV��VKRXOG�FRQIRUP�DW�OHDVW�WR�WKH�minimal standards��LI�DYDLODEOH��UHTXLUHG�IRU�WKH�UHOHYDQW�WD[RQ� RI� SURNDU\RWHV�´�+RZHYHU�� WKH� SXUSRVH� RI� WKH�PLQL-mal standards is restricted “to include tests for the establish-ment of generic identity and for the diagnosis of the species, i.e., an indication of the characters which would distinguish VSHFLHV�IURP�RWKHUV�´�7R�HPSKDVL]H�WKLV�SRLQW��1RWH�E�ZDV�DGGHG�ZKLFK�VWDWHV��³,W�LV�WKH�DLP�RI�PLQLPDO�VWDQGDUGV�WR�provide guidance on the description of taxa for taxonomists VHHNLQJ�VXFK�DGYLFH��+RZHYHU��WKHVH�VWDQGDUGV�DUH�QRW�WR�EH�DSSOLHG�LQ�VXFK�D�ZD\�DV�WR�FRQWUDGLFW�3ULQFLSOH�����´��'H�9RV�DQG�7UXSHU���������7KXV�� WKH\�DUH� UHFRPPHQGHG�SUDF-tices and cannot serve as the basis for not validating a new name. Within this context, the application of minimal stan-dards for the evaluation of taxonomic descriptions by the ,-6(0�RU�DQ\�RWKHU�MRXUQDO�LV�DQ�HGLWRULDO�GHFLVLRQ��,W�LV�QRW�authorized by the Code, which does not deal with the cor-rectness of names but only the way in which they are formed �7LQGDOO��������

Minimal standards

Unfortunately, the minimal standards for many taxonomic groups far exceed the requirements and intent of the Code. $V� ,�NQRZ� IURP�SHUVRQDO� H[SHULHQFH�� WKH�SKHQRW\SLF� FKDU-acters included in the minimal standards for methanogens, which I co-authored, is nearly useless in assigning metha-QRJHQV�WR�JHQHUD�RU�GLVWLQJXLVKLQJ�VSHFLHV��$OO�,�FDQ�VD\�LV�that it seemed like a good idea at the time, and I ascribe this failure to the inherent biological properties of these highly

VSHFLDOL]HG�OLWKRWURSKV��ZKLFK�DUH�H[WUHPHO\�GLI¿FXOW�WR�GLV-tinguish on phenotypic grounds, and not to a lack of effort E\�PH�DQG�P\�FROOHDJXHV��0RUH� VHULRXV� DUH� UHFRPPHQGD-tions for standards that require highly specialized and ex-pensive methodologies that are found in only a few labora-WRULHV��7LQGDOO�HW�DO����������7KHVH�VWDQGDUGV�PLVV�WKH�SRLQW��6WDQGDUGV�VKRXOG�EH�SUHSDUHG� IRU� WKH�XVHUV�RI� V\VWHPDWLFV��which includes biologists with a wide range of interests, and not just experts in taxonomy. Clinical microbiologists who LGHQWLI\�QHZ�SDWKRJHQV�PXVW�EH�DEOH�WR�QDPH�WKHP��0LFUR-bial physiologists who isolate novel micro-organisms with unique metabolic capabilities must be able to name them. 0LFURELDO� HFRORJLVWV� ZKR� LVRODWH� PLFUR�RUJDQLVPV� LPSRU-tant in special habitats or environmental processes must be able to name them. These names are needed to communicate effectively about these micro-organisms and the processes which involve them. The goal of descriptions of new species LV�WR�PDNH�SXEOLF�WR�WKH�VFLHQWL¿F�FRPPXQLW\�WKH�GLVFRYHU\�of new organisms. The Code only requires evidence of nov-HOW\��2QFH�WKH�UDWKHU�OLPLWHG�GHPDQGV�RI�WKH�&RGH�DUH�PHW��the descriptions should be allowed to include the properties that made that micro-organism interesting to the investiga-tors who discovered them.

0RVW� LPSRUWDQWO\�� LQ� WKH� FXUUHQW� V\VWHP�� WKHUH� DUH� QR�PD-MRU�FRQVHTXHQFHV�RI�PLVWDNHV��1DPHV�DUH�QRW�WUHDVXUHV�EXW�educated guesses or hypotheses about the nature of the mi-crobial world. They are always open for re-examination on both methodological and theoretical grounds. Because the type strains are now always available, the creation of species which inadvertently duplicate established species �RU�VXEMHFWLYH�V\QRQ\PV��FDQ�HDVLO\�EH�UHPRYHG�IURP�DQ\�taxonomic scheme. This is not sloppy science. Instead, it is the normal process of discovery, where new information is continually re-evaluated.

0LQLPDO�VWDQGDUGV�WKDW�DUH�H[FHVVLYH�DUH�H[FOXVLRQDU\�DQG�prevent biologists with serious interests in prokaryotes from describing novel species. They drive scientists out RI� WKH�¿HOG�DQG� VHULRXVO\�GDPDJH�SURNDU\RWLF� V\VWHPDWLFV��The likely consequence of their widespread adaption is that many biologists will no longer validate the names of newly described prokaryotes. When that happens, the literature will once again be full of names of uncertain meaning, and WKH� GLI¿FXOW�ZRUN� RI� VHYHUDO� JHQHUDWLRQV� RI�PLFURELDO� V\V-WHPDWLVWV� ZLOO� EH� XQGRQH�� 0RUHRYHU�� H[FHVVLYH� VWDQGDUGV�directly contradict the spirit of the Code, which invites par-ticipation by all and provides guarantees through the rules of priority that everyone’s contributions will be recognized. $JDLQ��WKH�SURFHVV�RI�QDPLQJ�D�QHZ�WD[RQ�VKRXOG�EH�VWUDLJKW-forward and easy.

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138 The Bulletin of BISMiS

Intent of the nomenclatural Code

The role of genomic sequencing

:LWK� WKH� DYDLODELOLW\� RI� LQH[SHQVLYH� '1$� VHTXHQFLQJ�� LW�is now possible to routinely describe prokaryotic species EDVHG� XSRQ� WKHLU� JHQRPLF� VHTXHQFHV��0RUHRYHU�� WKH� 3K\-ORJHQRPLF�6SHFLHV�&RQFHSW�SURYLGHV�VWURQJ�WKHRUHWLFDO�VXS-SRUW� IRU� WKLV� DSSURDFK� �6WDOH\�� ������ ������� 6XFK� VSHFLHV�will meet all the criteria of the Code. Type strains will be XQLTXHO\�DQG�XQDPELJXRXVO\�LGHQWL¿HG��DQG�UHGXQGDQF\�RI�QRPHQFODWXUH� ZLOO� EH� LPSRVVLEOH��0RUHRYHU�� WKH� JHQRPLF�VHTXHQFHV�ZLOO�PRUH�WKDQ�VDWLVI\�5HFRPPHQGDWLRQ���E�IRU�PLQLPDO�VWDQGDUGV��1RW�RQO\�ZLOO�WKH\�HVWDEOLVK�WKH�JHQHULF�identity, but they will provide a diagnosis of the species with a precision unimaginable at the time the Code was written. 7KLV�SULQFLSOH�ZDV�UHFRJQL]HG����\HDUV�DJR�LQ�WKH�5HSRUW�RI�WKH�$G�+RF�&RPPLWWHH�RQ�5HFRQFLOLDWLRQ�RI�$SSURDFKHV�WR�%DFWHULDO�6\VWHPDWLFV��ZKLFK�VWDWHG�WKDW�³WKH�FRPSOHWH�'1$�sequence would be the reference standard to determine phylogeny and that phylogeny should determine taxonomy. )XUWKHUPRUH��QRPHQFODWXUH�VKRXOG�DJUHH�ZLWK��DQG�UHÀHFW��JHQRPLF� LQIRUPDWLRQ�´� �:D\QH� HW� DO��� ������� )URP� WKLV�perspective, genomic sequencing may be the preferred ap-SURDFK�IRU�GHVFULELQJ�QHZ�VSHFLHV�LQ�WKH�IXWXUH��$OWKRXJK�RXU�NQRZOHGJH�RI�VSHFLHV�GH¿QHG�E\�JHQRPLF�VHTXHQFH�ZLOO�EH�different from our current phenotypic systems, it will not be less. Instead of knowing their metabolic properties through enzyme activities and growth substrates, we will know their major metabolic pathways through their gene content. We will know which vitamins and amino acids they can make and which must be provided. We will know their nutrients E\�LGHQWL¿FDWLRQ�RI�WUDQVSRUW�V\VWHPV��:H�ZLOO�NQRZ�ZKHWK-er they are oligotrophs, specialists, generalists, or symbionts from their genome complexity. We will know about their quorum-sensing systems, stress responses, and regulatory V\VWHPV��:H�ZLOO�NQRZ�LI�WKH\�SRVVHVV�JDV�YHVLFOHV��ÀDJHOOD��or pili. We will know if their cell envelopes contain peptido-JO\FDQ��RXWHU�PHPEUDQHV��DQG�VXUIDFH�OD\HU�SURWHLQV��0DQ\�of our observations will be ambiguous. By determining JHQHV��ZH�DUH�RQO\�GHWHUPLQLQJ�SRWHQWLDOV��+RZHYHU��WKLV�LV�not much different from systems based upon phenotypic ob-VHUYDWLRQV��ZKLFK�DUH�OLPLWHG�E\�RXU�LQDELOLW\�WR�¿QG�DSSUR-SULDWH�ODERUDWRU\�FRQGLWLRQV��8QGHU�WKH�YHU\�DUWL¿FLDO�FRQGL-tions of the laboratory, the behavior of prokaryotes is very GLIIHUHQW� IURP�ZKDW�KDSSHQV� LQ� WKH�HQYLURQPHQW��$IWHU�DOO��how often are colonies observed outside of the laboratory? /LNH�JHQRPLFV��SKHQRW\SLF�EDVHG�V\VWHPV�SURYLGH�OLWWOH�GL-rect information about the true nature of prokaryotes. They also require sophisticated interpretation to understand the biological entities being studied. Basing species on genomic sequences is different from what we have done, but it is not wrong and does not contradict the Code.

3URNDU\RWHV�DUH�WKH�GRPLQDQW�OLIH�IRUP�RQ�HDUWK��:KLWPDQ��������:KLWPDQ�HW�DO����������:LOO�ZH�NQRZ�OHVV�DERXW�WKHP�when a million prokaryotic species are described solely on the basis of their genomic sequences? If we know the ge-QRPLF�VHTXHQFH�RI��������RI�WKH�PRVW�FRPPRQ�SURNDU\RWLF�commensals of humans, will we know less about human health, nutrition, and evolution than we do now? If we know WKH�JHQRPLF�VHTXHQFH�RI��������RI�WKH�PRVW�FRPPRQ�SUR-karyotic commensals for each of our domestic animals, will we know less about their health and how to care for them? ,I�ZH�NQRZ�WKH�JHQRPLF�VHTXHQFH�RI���������RI�WKH�PRVW�common prokaryotes in soil, will we know less about soil fertility, nutrient cycling, and biochemistry? Will we be less able to feed ourselves or less able to create sustainable ag-ricultural systems with less reliance on fertilizers and pesti-cides? If we know the genomic sequence of a million pro-karyotic species that dominate the oceans, the lakes, rivers and streams, the swamps, marshes and bogs, hydrothermal vents, and deep subsurface, will we have less understanding of life’s diversity, the evolutionary processes taking place all around us, the history of life and how the biosphere formed, or the roles of prokaryotes in our world? Will we be less able to understand and anticipate climate change? When this happens, will we have fewer antibiotics, fewer anticancer drugs, fewer novel enzymes for biotechnology, and fewer metabolic pathways for synthetic biology?

7KH�ZLGHVSUHDG� DSSOLFDWLRQ� RI� WKH� 3K\ORJHQRPLF� 6SHFLHV�Concept will provide vast new insights into the biology of prokaryotes and numerous valuable tools for biotechnology. 7KXV�� UHFHQW�HIIRUWV�E\� WKH�'06=�DQG�-RLQW�*HQRPLFV� ,Q-stitute to sequence the genomes of all the deposited type VWUDLQV�SURYLGH�D�JUHDW�VHUYLFH�WR�ELRORJ\��.OHQN�DQG�*RNHU���������$GGLWLRQDO�HIIRUWV� WR� LQFOXGH�JHQRPLF�VHTXHQFHV� LQ�the initial description of novel species should be encouraged whenever practical. For instance, it would be a relatively simple matter for the large national centers to sequence and DQQRWDWH�JHQRPHV�XSRQ�SUHVHQWDWLRQ�RI�WKH�&HUWL¿FDWLRQ�RI�$YDLODELOLW\�IURP�DW�OHDVW�RQH�LQWHUQDWLRQDO�FXOWXUH�FROOHFWLRQ��7KLV�&HUWL¿FDWLRQ�LV�UHTXLUHG�IRU�WKH�YDOLG�GHVFULSWLRQ�RI�DOO�novel species and ensures that the culture will be available to other investigators.

Acknowledgements

,�WKDQN�-XHUJHQ�:LHJHO�IRU�KLV�FRQVWUXFWLYH�FRPPHQWV�DQG�encouragement. The shortcomings of this paper most likely resulted from me ignoring his advice.

References

%HUJH\��'�+���)�&��+DUULVRQ��5�6��%UHHG��%�:��+DPPHU�DQG�)�0��+XQWRRQ��������%HUJH\¶V�0DQXDO�RI�'HWHUPLQDWLYH�

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139

William B. Whitman

The Bulletin of BISMiS

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141© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 141–148

Contact detailsTUM Emeritus of Excellence, Center of Life and Food Science, Technical University München, Emil-Ramann-Str. 4, D-85350 Freis-ing, Germany

[email protected]

Karl-Heinz Schleifer

3URIHVVRU�'U�'U�K�F��PXOW��2WWR�.DQGOHU��GLVWLQJXLVKHG� botanist and microbiologist

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$V�D�YHU\�\RXQJ�PDQ�KH�ZDQWHG�WR�IROORZ�LQ�WKH�IRRWVWHSV�RI�KLV�GDG�EXW�WKH�6HFRQG�:RUOG�:DU�LQWHUIHUHG�ZLWK�KLV�LQWHQ-WLRQV��+H�KDG�WR�MRLQ�WKH�*HUPDQ�DUP\�DV�D�UDGLR�UHSRUWHU�RQ�WKH�5XVVLDQ�)URQW��$W�WKH�HQG�RI�WKH�ZDU�KH�ZDV�LQ�$XV-tria and escaped by bicycle to the Western Front to avoid FDSWXUH�E\�WKH�5XVVLDQV��$IWHU�VSHQGLQJ�D�IHZ�PRQWKV�LQ�DQ�$PHULFDQ�SULVRQ�FDPS�KH�ZDV�DOORZHG�WR�UHWXUQ�KRPH��%\�then, he was eager to study biology but in the post-war con-IXVLRQ�LW�ZDV�GLI¿FXOW�IRU�VWXGHQWV��0XFK�RI�WKH�XQLYHUVLW\�RI�0XQLFK�KDG�EHHQ�ERPEHG�DQG�WKH�VWXGHQWV�KDG�WR�KHOS�WR�remove rubble from the ruins. There were no scholarships DYDLODEOH�DQG�VWXGHQWV�KDG�WR�¿QG�RWKHU�ZD\V�WR�SD\�IRU�WKHLU�HGXFDWLRQ��1HYHUWKHOHVV��LQ������KH�HQUROOHG�LQ�ERWDQ\��]R-RORJ\�� FKHPLVWU\�� DQG� SK\VLFV� DW� WKH�/XGZLJ�0D[LPLOLDQV�8QLYHUVLW\�LQ�0XQLFK�DQG�¿QDQFHG�KLV�VWXGLHV�E\�JURZLQJ�DQG�VHOOLQJ�FDEEDJH�DQG�ÀRZHUV�LQ�'HJJHQGRUI��+H�PDMRUHG�in botany and, in order to study metabolism and the effect of auxin, he started to grow plant tissue cultures, at that WLPH�D�UDWKHU�QHZ�¿HOG��.DQGOHU���������������+H�UHFHLYHG�KLV�GRFWRU¶V�GHJUHH�ZLWK�KRQRUV� LQ������ �.DQGOHU������D���)URP������ WLOO������KH�ZDV�$VVLVWDQW�3URIHVVRU�RI�ERWDQ\�DW�WKH�8QLYHUVLW\�LQ�0XQLFK�DQG�¿QLVKHG�KLV�³+DELOLWDWLRQ´�LQ�������3ODQW�SK\VLRORJ\�ZDV�KLV�PDMRU�UHVHDUFK�WRSLF�EXW�±�already at that time - he showed some interest in bacteria. In

particular, the presence or absence of cell walls in bacteria FDXJKW�KLV�LQWHUHVW��+H�FRQYLQFHG�D�\RXQJ�VWXGHQW��*HUWUDXG�6FKlIHU��WR�GR�KHU�GRFWRUDWH�XQGHU�KLV�VXSHUYLVLRQ�RQ�/�IRUP�EDFWHULD� DQG� SOHXUR�SQHXPRQLD�OLNH� RUJDQLVPV� �33/2V���7KH�33/2V��ZKLFK�DUH�ZDOO�OHVV��SHQLFLOOLQ�UHVLVWDQW�EDFWH-ULD�� DUH�QRZ�FODVVL¿HG�DV�P\FRSODVPDV��*HUWUDXG�¿QLVKHG�her doctorate with great success, and soon became his wife and mother of three daughters. The two of them published FXWWLQJ�HGJH� SDSHUV� RQ� WKH� SUROLIHUDWLRQ� RI� 33/2V� DQG� /�IRUP�EDFWHULD�E\�D�EXGGLQJ�SURFHVV� �.DQGOHU�DQG�.DQGOHU�������� ������ ������.DQGOHU� HW� DO��� ������� (YHQ� QRZ�� DIWHU�PRUH�WKDQ����\HDUV��WKHVH�SXEOLFDWLRQV�DUH�VWLOO�RI�LQWHUHVW�IRU�UHFHQW�UHVHDUFK�SURMHFWV��/HDYHU�HW�DO����������*HUWUDXG�DQG�2WWR�.DQGOHU�KDYH�EHHQ�KDSSLO\�PDUULHG�IRU�DOPRVW����\HDUV�

Plant physiology

2WWR� .DQGOHU� ZDV� YHU\� LQWHUHVWHG� LQ� SODQW�JURZWK�SUR-PRWLQJ� IDFWRUV� �.DQGOHU�� ������ DQG� SKRWRV\QWKHVLV� �.DQ-GOHU�� ����E���+H� SUHVHQWHG� IRU� WKH�¿UVW� WLPH� H[SHULPHQWDO�

Figure 1. Otto Kandler in 1976.

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142 The Bulletin of BISMiS

Otto Kandler: distinguished botanist and microbiologist

evidence of photophosphorylation using Chlorella cells �.DQGOHU�� ����E�� ������ ������ DQG� WKLV�ZDV� WKH� UHDVRQ� KH�ZDV�RIIHUHG�D�5RFNHIHOOHU�)HOORZVKLS������±�������$W�WKDW�time, radioactively labeled compounds were not available LQ�*HUPDQ\��7KHUHIRUH��KH�GHFLGHG�WR�MRLQ�WKH�ODERUDWRULHV�RI�0DUWLQ�*LEEV�DQG�0HOYLQ�&DOYLQ�LQ�%HUNHOH\��ZKHUH�KH�ZDV�DEOH�WR�XVH�ODEHOHG�FRPSRXQGV�IRU�KLV�H[SHULPHQWV��+H�HQMR\HG�ZRUNLQJ� LQ� &DOLIRUQLD�� +H� WROG�PH� RQFH� WKDW� WKH�blue skies and the pleasant ambient temperature were ideal WR�ZRUN� LQ� WKH� ODERUDWRU\��7RJHWKHU�ZLWK�0DUWLQ�*LEEV�KH�published two important papers on the formation of sugars DV� VXEVHTXHQW� SURGXFWV� RI� WKH�&DOYLQ�&\FOH� �.DQGOHU� DQG�*LEEV��������*LEEV�DQG�.DQGOHU���������/DWHU�RQ��KH�DQG�KLV�group studied the biosynthesis and physiological function of SODQW�VSHFL¿F�ROLJRVDFFKDULGHV�VXFK�DV�DSLRVH��KDPDPHORVH��VWDFK\RVH�� XPEHOOLIHURVH�� VHODJLQRVH� DQG�YHUEDVFRVH� �.DQ-GOHU�DQG�+RSI���������������+H�FRQWLQXHG�KLV�UHVHDUFK�RQ�SKRWRV\QWKHVLV��7DQQHU�HW�DO���������.ORE�HW�DO���������

$W�WKH�HQG�RI�KLV�FDUHHU�KH�ZDV�D�¿HUFH�RSSRQHQW�RI�WKH�VR�FDOOHG� ³:DOGVWHUEHQ´� �IRUHVW� GLHEDFN��� LQLWLDWHG� WKURXJK� D�K\VWHULFDO� GLVFXVVLRQ� WKDW� VWDUWHG� LQ�*HUPDQ\� LQ� WKH� HDUO\�����V� �.DQGOHU�� �������7KHUH�ZDV� DQ� RQJRLQJ�� TXLWH� HPR-WLRQDO�GLVFXVVLRQ�DERXW� WKH�VWDWH�RI� WKH�*HUPDQ�IRUHVW��+H�had been publically discredited and even personally insulted GHVSLWH�KLV� FRQYLQFLQJ� VFLHQWL¿F�DUJXPHQWV� WKDW� IRUHVW�GLH-backs had already occurred in former times. Therefore, he ZDV� TXLWH� SOHDVHG� WKDW� WKH�ZRUOG�NQRZQ� SKLORVRSKHU�.DUO�3RSSHU� VXSSRUWHG� KLV� FULWLFDO� DWWLWXGH� WRZDUGV� WKH� ³JUHHQ�VDJD�RI�:DOGVWHUEHQ´��3RSSHU¶V�SKUDVH��LQ�DQ�LQWHUYLHZ�ZLWK�WKH�*HUPDQ�PDJD]LQH�Spiegel�LQ������

Professional career

8SRQ�KLV�UHWXUQ�IURP�WKH�8QLWHG�6WDWHV�KH�ZDV�GLVVDWLV¿HG�with the poor laboratory conditions at the university and was JODG� WR�¿QG�DQ�RSSRUWXQLW\� WR�EHFRPH�GLUHFWRU�RI� WKH�%DF-WHULRORJLFDO� ,QVWLWXWH�RI� WKH�6RXWK�*HUPDQ�'DLU\�5HVHDUFK�&HQWHU� LQ�)UHLVLQJ�:HLKHQVWHSKDQ� LQ� ������7KLV�ZDV� DFWX-ally a brave decision since he had no inkling of dairy micro-biology but soon he developed an interest in applied micro-biology and biotechnology that he maintained throughout his career.

,Q�������KH�ZDV�DSSRLQWHG�)XOO�SURIHVVRU�DQG�+HDG�RI�WKH�'HSDUWPHQW�RI�%RWDQ\�RI�WKH�7HFKQLFDO�8QLYHUVLW\�0XQLFK�and simultaneously maintained his position as director of the Bacteriological Institute in Freising. It was convenient for me since I was living in Freising and did not have to take WKH� WUDLQ� WR�0XQLFK� WR�GR�P\�GLSORPD�DQG�GRFWRUDO� WKHVLV�XQGHU� WKH� VXSHUYLVLRQ� RI� 2WWR� .DQGOHU�� 7KH� GLVDGYDQWDJH��

however, was that the only time to meet him and discuss VFLHQWL¿F�PDWWHUV�ZDV�RQ�ZHHNHQGV��PDLQO\�RQ�ODWH�RQ�6DWXU-GD\�DIWHUQRRQV�RU�6XQGD\�PRUQLQJV�

,Q�������KH�ZDV�DSSRLQWHG�)XOO�SURIHVVRU�DQG�+HDG�RI�WKH�'HSDUWPHQW�RI�%RWDQ\�RI�WKH�/XGZLJ�0D[LPLOLDQV�8QLYHU-VLW\�DQG�VWD\HG�WKHUH�XQWLO�KLV�UHWLUHPHQW�LQ�������+H�ZDV�DQ�KRQRUDU\�PHPEHU�RI� WKH�*HUPDQ�6RFLHW\�RI�+\JLHQH� DQG�0LFURELRORJ\��+H�ZDV�ERWK�'HDQ�RI�WKH�)DFXOW\�RI�*HQHUDO�6FLHQFHV��780�������DQG�RI�WKH�)DFXOW\�RI�%LRORJ\��/08��������)URP������WR������KH�ZDV�D�PHPEHU�RI�WKH�6HQDWH�RI�WKH�*HUPDQ�6FLHQFH�)RXQGDWLRQ��')*���)URP������WR������KH�ZDV�&KDLUPDQ�RI�WKH�6FLHQWL¿F�$GYLVRU\�%RDUG�RI�WKH�1D-tional Research Center of Biotechnology in Braunschweig. +H�ZDV�DOVR�WKH�SULPH�PRYHU�IRU�WKH�IRXQGDWLRQ�RI�WKH�*HU-PDQ�&ROOHFWLRQ�RI�0LFURRUJDQLVPV�DQG�WKH�IRXQGHU�DV�ZHOO�DV� WKH�(GLWRU�LQ�&KLHI� RI�Systematic and Applied Microbi-ology and served for a long time on the editorial board of $UFKLYHV�RI�0LFURELRORJ\�DQG�=HLWVFKULIW�I�U�3ÀDQ]HQSK\VL-RORJLH��+H�ZDV�HOHFWHG�WR�WKH�*HUPDQ�1DWLRQDO�$FDGHP\�RI�6FLHQFHV��/HRSROGLQD��LQ������DQG�WR�WKH�%DYDULDQ�$FDGHP\�RI�6FLHQFHV�LQ�������+H�UHFHLYHG�WKH�%HUJH\�$ZDUG�LQ������DQG� WKH�)HUGLQDQG�&RKQ�0HGDO�RI� WKH�*HUPDQ�6RFLHW\�RI�+\JLHQH�DQG�0LFURELRORJ\��'*+0��LQ�������+H�UHFHLYHG�KRQRUDU\�GRFWRUDO�GHJUHHV�IURP�WKH�8QLYHUVLW\�*KHQW��%HO-JLXP��LQ������DQG�IURP�WKH�7HFKQLFDO�8QLYHUVLW\�0XQLFK�LQ�������)LJXUH����

+H� LV� DQ� KRQRUDU\�PHPEHU� RI� WKH�$VVRFLDWLRQ� RI�*HQHUDO�DQG�$SSOLHG�0LFURELRORJ\�� WKH� ODUJHVW�PLFURELRORJLFDO� VR-FLHW\�LQ�*HUPDQ\��+H�KDG�VHYHUDO�RSSRUWXQLWLHV�WR�PRYH�WR�RWKHU�SRVLWLRQV�RXWVLGH�RI�%DYDULD�EXW�KH�QHYHU�DFFHSWHG��+H�

Figure 2. Otto and Gertraud Kandler during the confer-ral ceremony of the honorary doctorate at the Technical University of Munich (1985).

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143

Karl-Heinz Schleifer

The Bulletin of BISMiS

is tightly connected to his homeland and the following quo-WDWLRQ�PD\�FRPH�FORVH�WR�KLV�DWWLWXGH��Extra Bavariam nulla vita est, et si est vita, non est ita��7KHUH�LV�QR�OLIH�RXWVLGH�RI�Bavaria, and if yes, not this one).

2WWR�.DQGOHU¶V� SURIHVVLRQDO� SUR¿OH� FUHDWHV� WKH� LPSUHVVLRQ�WKDW�KLV�PDMRU�LQWHUHVWV�DUH�ERWDQ\��+RZHYHU��KLV�VFLHQWL¿F�DFWLYLWLHV� ZHUH� PXFK� EURDGHU� DQG� FHUWDLQO\� KDG� DQ� LQÀX-HQFH� RQ� KLV� WHDFKLQJ� DFWLYLWLHV��+H� FDOOHG� KLPVHOI� D� ELROR-gist. Therefore, he taught, not only general botany and plant physiology, but also ecology, food microbiology and bacte-ULDO�WD[RQRP\��)LJXUH�����+LV�EURDG�VFLHQWL¿F�LQWHUHVWV�FDQ�EH�HDVLO\�MXGJHG�IURP�WKH�WLWOHV�RI�KLV�����SXEOLFDWLRQV��7KH�topics range from plant tissue cultures, plant physiology, photosynthesis, plant oligosaccharides, bacterial cell walls, physiology of bacteria, applied microbiology to “Waldster-EHQ´� DQG� RULJLQ� RI� OLIH� DQG� HYROXWLRQ��+RZHYHU�� LW� KDV� WR�be mentioned that about two thirds of his publications deal ZLWK�PLFURELRORJLFDO�DVSHFWV��.DQGOHU¶V�EURDG�VFLHQWL¿F�DF-WLYLWLHV�DUH�DOVR�UHÀHFWHG�E\�WKH�IDFW�WKDW�IRXU�RI�KLV�IRUPHU�3K'� VWXGHQWV� RU� FRZRUNHUV�ZHUH� DSSRLQWHG� DV� IXOO� SURIHV-VRUV�RI�ERWDQ\�DQG����DV�PLFURELRORJLVWV��+�+��0DUWLQ��+�-��.XW]QHU��5��3ODSS��$��%|FN��.�+��6FKOHLIHU��0��7HXEHU��.��2��6WHWWHU��:��+DPPHV��:��+RO]DSIHO��)��)LHGOHU��+��.|QLJ��-��:LQWHU��DQG�5��+HQVHO��

The chemical composition of bacterial cell walls

2WWR�.DQGOHU�ZDV�RQH�RI�WKH�¿UVW�VFLHQWLVWV�ZKR�VWXGLHG�WKH�FHOO�ZDOO�RI�EDFWHULD��$OUHDG\�LQ������KH�SXEOLVKHG�D�SDSHU�in Nature on the cell-wall composition of Proteus vulgaris �.DQGOHU� HW� DO��� ������ DQG� RI� RWKHU� EDFWHULD� �.DQGOHU� DQG�+XQG���������/DWHU�RQ�KH�LQYHVWLJDWHG�WKH�LQKLELWLQJ�HIIHFWV�of penicillin and cycloserine on the biosynthesis of bacterial FHOO�ZDOOV��5DX�+XQG�DQG�.DQGOHU��������3ODSS�DQG�.DQGOHU������D������E���6XEVHTXHQW�WR�WKH�GHVLJQ�DQG�GHYHORSPHQW�RI�a simple method for the determination of the primary struc-WXUH�RI�SHSWLGRJO\FDQ��6FKOHLIHU�DQG�.DQGOHU���������PRVW�of the currently known peptidoglycan types were described E\�.DQGOHU¶V�JURXS��VHH�6FKOHLIHU�DQG�.DQGOHU���������7KH\�also studied the exogeneous and endogenous effects on the PRGL¿FDWLRQ�RI�SHSWLGRJO\FDQ� �6FKOHLIHU� HW� DO��� ������ DQG�WKH� ELRV\QWKHVLV� RI� SHSWLGRJO\FDQ� �+DPPHV� DQG� .DQGOHU��������� ,Q� ������ .DQGOHU� DQG�+LSSH� GHVFULEHG� WKH� ODFN� RI�peptidoglycan in Methanosarcina barkeri. This was the be-JLQQLQJ�RI�KLV�LQWHUHVW�LQ�DUFKDHDO�UHVHDUFK��VHH�EHORZ��

Bacterial physiology

.DQGOHU¶V� LQWHUHVW� LQ� SODQW� ELRFKHPLVWU\� DQG� SK\VLRORJ\�DOVR�KDG�DQ�LPSDFW�RQ�KLV�EDFWHULRORJLFDO�VWXGLHV��$OUHDG\�LQ�

������KH�GHWHUPLQHG�WKH�DPLQR�DFLG�FRPSRVLWLRQ�RI�K\GURO\-VDWHV�RI�EDFWHULD�E\�SDSHU�FKURPDWRJUDSK\��.DQGOHU�DQG�=H-KHQGHU���������$W�WKH�VDPH�WLPH��KH�FDUULHG�RXW�FRPSDUDWLYH�studies on the metabolism of nucleic acid and respiration of Proteus vulgaris and pleuropneumonia-like organisms �.DQGOHU�HW�DO���������DV�ZHOO�DV�VWXGLHV�RQ�WKH�SK\VLRORJ\�of Caulobacter��+XQG�DQG�.DQGOHU���������,Q�������KH�SXE-OLVKHG� LQ�1DWXUH�D�VWXG\�RQ� WKH�ELRV\QWKHVLV�RI�DFHWRLQ�E\�Leuconostoc citrovorum. �.DQGOHU� DQG� %XVVH�� ������� +H�was also interested in the carbohydrate metabolism of lactic DFLG�EDFWHULD��:HLVV�HW�DO���������6WHWWHU�DQG�.DQGOHU��������.DQGOHU�� ������� FHOOXORPRQDV� �6WDFNHEUDQGW� DQG� .DQGOHU��������DQG�EL¿GREDFWHULD��/DXHU�DQG�.DQGOHU��������

Taxonomy of bacteria

2WWR�.DQGOHU�KDG�D�VWURQJ�LQWHUHVW�LQ�WKH�V\VWHPDWLFV�RI�SODQWV�DQG�HVSHFLDOO\�RI�EDFWHULD��.DQGOHU�DQG�6FKOHLIHU���������$O-UHDG\�LQ������KH�SURSRVHG�WKDW�WKH�DPLQR�DFLG�FRPSRVLWLRQ�of the cell walls of bacteria may be used for the differen-WLDWLRQ�RI�EDFWHULD� LQ�GDLU\�SURGXFWV��.DQGOHU�HW�DO����������6XEVHTXHQWO\�� KH� GHDOW� ZLWK� WKH� FODVVL¿FDWLRQ� RI� VWDSK\OR-FRFFL�DQG�ODFWREDFLOOL��$ER�(OQDJD�DQG�.DQGOHU��������.DQ-GOHU������D���+H�GHVFULEHG�QHZ�VSHFLHV�RI�ODFWREDFLOOL��/DXHU�DQG�.DQGOHU��������:HL��HW�DO���������.DQGOHU�HW�DO�������D������E��.DQGOHU�DQG�.XQDWK���������VWUHSWRFRFFL��&ROOLQV�HW�DO��� ������ ������� FHOOXORPRQDV� �6WDFNHEUDQGW� DQG�.DQGOHU��������������DFHWRPLFURELD��6RXWVFKHN�HW�DO���������DQG�ED-FLOOL��6FKRO]�HW�DO����������+H�DOVR�PDGH�LPSRUWDQW�FRQWULEX-WLRQV�WR�WKH�WD[RQRP\�RI�EL¿GREDFWHULD��.DQGOHU�DQG�/DXHU��������/DXHU�DQG�.DQGOHU���������,Q�������KH�UHFRJQL]HG�WKDW�WKH�DPLQR�DFLG�VHTXHQFH�RI� WKH�SHSWLGRJO\FDQ��PXUHLQ��RI�the bacterial cell wall is a valuable chemotaxonomic marker �.DQGOHU������E���$�OLWWOH�ODWHU��WKH�GLIIHUHQW�SHSWLGRJO\FDQ�types and their taxonomic implication were described in a

Figure 3.�'LJJLQJ�XS�D�VRLO�SURÀOH�IRU�WKH�VWXGHQWV�

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144 The Bulletin of BISMiS

Otto Kandler: distinguished botanist and microbiologist

UHYLHZ�LQ�PRUH�GHWDLO��6FKOHLIHU�DQG�.DQGOHU���������%\�WKH�way, this review is a citation classic and one of the most FLWHG�SDSHUV� LQ�EDFWHULRORJ\� �PRUH� WKDQ������ WLPHV�FLWHG���+H�DOVR�ZURWH�D�UHYLHZ�RQ�WKH�HYROXWLRQ�RI�WKH�V\VWHPDWLFV�RI�EDFWHULD��.DQGOHU������D��DQG�FRDXWKRUHG�D�VWXG\�RQ�WKH�phylogenetic relationship of the genera Thermus and Deino-coccus��+HQVHO�HW�DO���������

Applied microbiology and biotechnology

/RXLV�3DVWHXU�ZDV�RQH�RI�.DQGOHU¶V�VFLHQWL¿F�KHURHV��,�VWLOO�FDQ� UHPHPEHU� WZR�TXRWHV�RI�3DVWHXU�KH�PHQWLRQHG� WR�PH�at several occasions and which are characteristic of his at-titude. “Where observation is concerned, chance favors only the prepared mind” and “there are no such things as applied sciences, only applications of science”. Therefore, KH�ZDV�DOZD\V� IXOO�RI� LGHDV� WR�H[SORLW�KLV� VFLHQWL¿F�¿QG-ings. During his tenure as director of the Bacteriological ,QVWLWXWH� RI� WKH� 6RXWK� *HUPDQ� 'DLU\� 5HVHDUFK� &HQWHU� LQ�Freising-Weihenstephan he focused on dairy microbiology. +H�VWXGLHG�WKH�VKHOI�OLIH�RI�PLON�WKDW�ZDV�KHDWHG�XQGHU�GLI-IHUHQW� FRQGLWLRQV� �.DQGOHU�� ������� GHVLJQHG� QHZ�PHWKRGV�IRU�FKHFNLQJ�WKH�TXDOLW\�RI�UDZ�PLON��.DQGOHU���������GHDOW�ZLWK�IDLOXUHV�GXULQJ�WKH�SURGXFWLRQ�RI�\RJKXUW��.DQGOHU�DQG�)UDQN���������VWXGLHG� WKH�HIIHFW�RI�EDFWHULD�FRQWHQW�RQ� WKH�TXDOLW\�RI�UDZ�PLON��.DQGOHU������D��DQG�WKH�XWLOL]DWLRQ�RI�Lactobacillus acidophilus as starter culture for dairy prod-XFWV��.DQGOHU������E��DV�ZHOO�DV�WKH�SHUFHQWDJH�RI�l�����DQG�d�í��ODFWLF�DFLG�LQ�VDPSOHV�RI�\RJKXUW��.XQDWK�DQG�.DQGOHU���������+H�KROGV�GLIIHUHQW�SDWHQWV�RQ�VWDUWHU�FXOWXUHV�IRU�WKH�SURGXFWLRQ� RI� IHUPHQWHG�PLON� DQG� YHJHWDEOH� �6DXHUNUDXW��SURGXFWV��+H�DOVR�SURSRVHG�PHWKRGV�IRU�VXFFHVVIXOO\�FRP-EDWLQJ�PLFUR�RUJDQLVPV�LQ�FRROLQJ�ZDWHU�V\VWHPV��.DQGOHU���������,Q�������KH�SXEOLVKHG�D�UHYLHZ�RQ�WKH�WD[RQRP\�DQG�WHFKQRORJLFDO� LPSRUWDQFH� RI� ODFWREDFLOOL� �.DQGOHU�� �������0RUHRYHU��KH�LQYHVWLJDWHG�FRQGLWLRQV�IRU�WKH�NLOOLQJ�RI�EDF-WHULDO�VSRUHV�DW�XOWUD�KLJK�WHPSHUDWXUH��0LOOHU�DQG�.DQGOHU��������� /DWHU� RQ� KH� FRQGXFWHG� UHVHDUFK� RQ� WKHUPRSKLOLF�PHWKDQRJHQV�DQG�WKHLU�DELOLW\�WR�SURGXFH�PHWKDQH��ELRJDV��from sewage and other waste. For instance, he investigated WKH�HI¿FLHQF\�DQG�VWDELOLW\�RI�PHWKDQH�IRUPDWLRQ�RI�ZDVWHV�DW�PHVRSKLOLF�DQG�WKHUPRSKLOLF�WHPSHUDWXUHV��.DQGOHU�HW�DO��������� DQG�ZURWH� D� UHYLHZ�RQ�DUFKDHEDFWHULD� DQG� WKHLU� ELR-WHFKQRORJLFDO�LPSOLFDWLRQV��.DQGOHU������E��

The founder of archaebacterial research in Germany

In my opinion, the launching of archaebacterial research in *HUPDQ\�ZDV�SUREDEO\�WKH�PRVW�VXFFHVVIXO�DQG�IDU�UHDFKLQJ�GHFLVLRQ�LQ�KLV�RXWVWDQGLQJ�VFLHQWL¿F�FDUHHU��+H�ZDV�WKH�¿UVW�VFLHQWLVW� RXWVLGH� WKH�8QLWHG� 6WDWHV�ZKR� UHFRJQL]HG� WKH� IX-

ture importance of archaebacterial research. Based on his LQWHUHVW�LQ�EDFWHULDO�FHOO�ZDOOV��VHH�DERYH���KH�DQG�KLV�JURXS�DQDO\]HG� WKH� FHOO�ZDOOV� RI� H[WUHPH�KDORSKLOHV� �6WHEHU� DQG�6FKOHLIHU�� ������ DQG� RI�Methanosarcina barkeri �.DQGOHU�DQG� +LSSH�� ������� %RWK� RUJDQLVPV� ODFNHG� SHSWLGRJO\FDQ��a unique component of the bacterial cell wall. During this WLPH�0DUYLQ�%U\DQW�ZDV�YLVLWLQJ�.DQGOHU�LQ�0XQLFK��7KH\�had planned a joint research project on the cell-wall compo-VLWLRQ� RI� RWKHU�PHWKDQRJHQLF� EDFWHULD��:KLOH�0DUYLQ�%U\-DQW�ZDV�VLWWLQJ�LQ�2WWR�.DQGOHU¶V�RI¿FH��D�OHWWHU�IURP�5DOSK�Wolfe arrived reporting from Carl Woese’s exciting results on the unique phylogenetic position of methanogenic bac-WHULD�ZLWKLQ�SURNDU\RWHV��,Q�������.DQGOHU�ZURWH� WR�:ROIH�and mentioned that methanogens and halophiles may be

“ancient relics” that have branched off from the bulk of the SURNDU\RWHV�EHIRUH�SHSWLGRJO\FDQ�KDG�EHHQ�³LQYHQWHG´��+H�asked Wolfe to send him lyophilized cells of methanogens IRU�DQDO\]LQJ�WKHLU�FHOO�ZDOOV��,Q�-DQXDU\�������.DQGOHU�DW-WHQGHG�D�*RUGRQ�&RQIHUHQFH�RQ�EDFWHULDO�FHOO�ZDOOV�LQ�6DQWD�0RQLFD�DQG�YLVLWHG�5DOSK�:ROIH�LQ�8UEDQD�RQ�KLV�ZD\�EDFN�WR�*HUPDQ\��,W�ZDV�WKH�¿UVW�WLPH�.DQGOHU�PHW�&DUO�:RHVH�and learned about his results of the comparative cataloguing RI���6�U51$�DQG�WKHLU�SK\ORJHQHWLF�LPSOLFDWLRQV��.DQGOHU�was deeply impressed. When he returned from the United 6WDWHV�KH�ZDV�YHU\�H[FLWHG�DQG�WROG�KLV�FR�ZRUNHUV�WKDW�KH�KDV�PHW� ³WKH�'DUZLQ� RI� WKH� ��WK� FHQWXU\´� �)LJXUH� ����+H�was convinced that research on Archaebacteria had a great IXWXUH�DQG�KH�ZDV�VXFFHVVIXO�LQ�SHUVXDGLQJ�WKH�*HUPDQ�UH-search organization to support special research projects for this group of organisms. This was the beginning of a success VWRU\�RQ�DUFKDHEDFWHULDO�UHVHDUFK�LQ�*HUPDQ\�ZLWK�PDQ\�VFL-HQWLVWV�LQYROYHG�VXFK�DV�$XJXVW�%|FN��*HUKDUG�*RWWVFKDON��.DUO�2WWR�6WHWWHU��5DOI�7KDXHU�DQG�:ROIUDP�=LOOLJ�� MXVW� WR�name a few.

,Q�FRQWUDVW�WR�WKH�8QLWHG�6WDWHV��ZKHUH�DUFKDHEDFWHULDO�IXQG-ing was quite poor, this kind of research expanded quickly in *HUPDQ\�GXH�WR�2WWR�.DQGOHU¶V�VWUHQXRXV�HIIRUWV��+H�RUJD-QL]HG�WKH�¿UVW�PHHWLQJ�RQ�DUFKDHEDFWHULD�LQ�0XQLFK�LQ������DQG�DOVR�WKH�¿UVW�LQWHUQDWLRQDO�ZRUNVKRS�RQ�DUFKDHEDFWHULD�LQ� ������:RHVH¶V� SDUWLFLSDWLRQ� LQ� WKHVH� PHHWLQJV� ZDV� DQ�important impulse for further research on archaebacteria in *HUPDQ\��7ZHOYH�SURIHVVRUV�IURP�DFURVV�*HUPDQ\�DWWHQGHG�the meetings. Woese was met with fanfare and a brass band ZKHQ�KH�DUULYHG�LQ�0XQLFK��/HFWXUHV�RI�WKHVH�PHHWLQJV�ZHUH�published as special issues of Systematic and Applied Mi-crobiology��D�MRXUQDO�WKDW�ZDV�ODXQFKHG�E\�.DQGOHU�LQ�������:RHVH�ZDV�VR�LPSUHVVHG�E\�.DQGOHU¶V�DFWLYLWLHV�DQG�HIIRUWV�WKDW�KH�ZURWH�WR�:ROIUDP�=LOOLJ�LQ������³0XQLFK�ZLOO�VRRQ�be even more famous as the world capital for archaebacte-rial research than for its beer” and “a bit of my heart still UHPDLQV�LQ�0�QFKHQ´��6DSS��������

Page 63: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

145

Karl-Heinz Schleifer

The Bulletin of BISMiS

$�ORQJ�ODVWLQJ�IULHQGVKLS�GHYHORSHG�EHWZHHQ�2WWR�.DQGOHU�and Carl Woese. Woese called it a “complementary rela-WLRQVKLS´��$�FORVH�FROODERUDWLRQ�HYROYHG��7KH�8UEDQD�JURXS�DQDO\]HG�WKH���6�U51$�JHQH�VHTXHQFHV�RI�EDFWHULD�DQG�DU-FKDHEDFWHULD��ZKHUHDV� WKH�0XQLFK�JURXS�VWXGLHG�WKHLU�FHOO�ZDOO� FRPSRVLWLRQ�� �.DQGOHU� DQG�.|QLJ���������7KH�FKHPL-cal structure of the unique pseudomurein was elucidated �.|QLJ�DQG�.DQGOHU������D������E��.|QLJ�HW�DO���������DQG�LWV�ELRV\QWKHVLV�LQYHVWLJDWHG��.|QLJ�HW�DO���������+DUWPDQQ�HW�DO���������

To further improve the collaboration with the Urbana group, (UNR�6WDFNHEUDQGW��D�IRUPHU�3K'�VWXGHQW�RI�.DQGOHU��MRLQHG�&DUO�:RHVH¶V�ODERUDWRU\�LQ������ZKHUH�KH�VSHQW�D�YHU\�SUR-ductive year as a postdoc. Upon his return from Urbana, 6WDFNHEUDQGW� JRW� D� SRVLWLRQ� DV� D� UHVHDUFK� DVVRFLDWH� DW� WKH�'HSDUWPHQW�RI�0LFURELRORJ\�DW�WKH�7HFKQLFDO�8QLYHUVLW\�RI�0XQLFK� DQG� LQWURGXFHG� DQG� LPSURYHG� WKH��6� U51$� WHFK-QRORJ\�WRJHWKHU�ZLWK�:ROIJDQJ�/XGZLJ�

2WWR�.DQGOHU��&DUO�:RHVH�DQG�:ROIUDP�=LOOLJ�EHJDQ�D�SHU-sistent mutual discussion about the relationship among the Archaebacteria, Eubacteria and Eucarya. In particular, =LOOLJ¶V� VWXGLHV� RQ�51$�SRO\PHUDVHV� VXSSRUWHG� WKH� IXQGD-PHQWDO�XQLTXHQHVV�RI�DUFKDHEDFWHULD��=LOOLJ�HW�DO����������,Q�������.DQGOHU� UHFRPPHQGHG� VKRUWHQLQJ� WKH� QDPHV� RI� WKH�WKUHH�JURXSV��$IWHU�ORQJ�GHEDWHV�.DQGOHU�DQG�:RHVH�DJUHHG�to name them Archaea, Bacteria and Eucarya.� +RZHYHU��there was still no decision about what to call the taxonomic OHYHO��6HYHUDO�SURSRVDOV�ZHUH�FRQVLGHUHG��H�J��HPSLUH��UHDOP��urkingdom or domain. Finally, they agreed on the term do-PDLQ��:RHVH�HW�DO����������$V�PHQWLRQHG�EHIRUH��2WWR�.DQ-dler was also very interested in the early evolution of life and in one of his last papers he rejected the existence of a

FRPPRQ�³¿UVW�FHOO´��RIWHQ�UHIHUUHG�WR�DV�/8&$�±�ODVW�XQL-YHUVDO�FRPPRQ�DQFHVWRU���+H�SRVWXODWHG�WKDW�HDFK�RI�WKUHH�domains of life had its own progenitor cell which originated IURP� D� ³PXOWLSKHQRW\SLFDO� SRSXODWLRQ� RI� SUH�FHOOV´� �.DQ-GOHU��������

Résumé

2WWR�.DQGOHU��3URIHVVRU�(PHULWXV�RI�%RWDQ\�DW�WKH�/XGZLJ�0D[LPLOLDQV�8QLYHUVLW\�0XQLFK� LV� DQ� LQWHUQDWLRQDOO\�ZHOO�known, highly respected scientist and one of the most out-VWDQGLQJ�PLFURELRORJLVWV�LQ�*HUPDQ\��+H�KDG�D�WUHPHQGRXV�enthusiasm for research on a wide variety of different topics, both in microbiology and plant physiology. In microbiol-ogy, he is particularly well known for his work on bacterial and archaeal cell walls and their implication on taxonomy DQG� SK\ORJHQ\��+H�ZDV� WKH�¿UVW� VFLHQWLVW�ZKR� UHFRJQL]HG�the importance of cell-wall composition for the differentia-tion of Bacteria from Archaea and initiated the successful funding of research on Archaea�LQ�*HUPDQ\��0RUHRYHU��KH�was also interested in the physiology and biochemistry of several groups of bacteria, especially lactic acid bacteria as well as food microbiology and biotechnology such as the optimization of biogas production under mesophilic and WKHUPRSKLOLF�FRQGLWLRQV��+H�ZDV�D�GHGLFDWHG�DQG�H[WUHPHO\�KDUG�ZRUNLQJ�VFLHQWLVW�DQG�KDG�WKH�DELOLW\�WR�¿OO�KLV�VWXGHQWV�with his enthusiasm for research. Therefore, it is not sur-prising that many of his former students and co-workers DGYDQFHG�WR�OHDGLQJ�SRVLWLRQV�LQ�WKH�¿HOG�RI�PLFURELRORJ\��0XFK�RI�2WWR�.DQGOHU¶V�OLIH�ZDV�VKDUHG�ZLWK�KLV�FDULQJ�ZLIH�DQG�IRUPHU�3K'�VWXGHQW��*HUWUDXG��ZKR�LV�HTXDOO\�HQWKXVL-astic about science as her husband, and their three beloved daughters. Despite his numerous activities he always had an open ear for his family.

$OWKRXJK� KH� ZDV� VWURQJ�ZLOOHG�� KLV� FRQFHUQ� IRU� IDLUQHVV��thoroughness, and pride in accomplishment governed his EHKDYLRU� LQ� HYHU\� SHUVRQDO� DQG� SURIHVVLRQDO� VLWXDWLRQ��+H�had exceptionally high standards of performance and his JLIW� IRU� VFLHQWL¿F�DQDO\VLV�ZDV�PRUH� WKDQ�D�PDWFK� IRU� DQ\�SUREOHP��+H�ZDV�DQ�H[WUHPHO\�DFXWH�DQG�UHOLDEOH�FULWLF�DQG�UHSRUWHU�RI�ERWK� VFLHQWL¿F�PDWWHUV�DQG�KXPDQ�DIIDLUV�� ,W� LV�not often that one has the opportunity to share the joy of ex-periences of science with someone who feels the same way. ,�ZDV�IRUWXQDWH�WR�KDYH�KDG�2WWR�.DQGOHU�DV�D�PHQWRU�DQG�VSLULWXDO� IDWKHU��+H� LV�D� UHPDUNDEOH� LQGLYLGXDO��DQG�KH� OHIW�his mark not only on science, but on all those who interacted with him.

Acknowledgements

,�ZRXOG�OLNH�WR�H[SUHVV�P\�JUDWLWXGH�WR�'U�*HUWUDXG�.DQGOHU�DQG�-LP�6WDOH\�IRU�UHDGLQJ�DQG�LPSURYLQJ�WKH�PDQXVFULSW�

Figure 4. Carl Woese, Ralph Wolfe and Otto Kandler (from left to right) relaxing after a hike in the Bavarian alps (1981).

Page 64: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

146 The Bulletin of BISMiS

Otto Kandler: distinguished botanist and microbiologist

References

$ER�(OQDJD��,�*��DQG�2��.DQGOHU������D��=XU�7D[RQRPLH�GHU�*DWWXQJ�Lactobacillus. =HQWUDOEO��%DNWHULRO��,,��119: �±���

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&ROOLQV��0�'���-�$�(��)DUURZ��%�$��3KLOOLSV�DQG�2��.DQGOHU��������Streptococcus garviae sp. nov. and Streptococcus plantarum VS��QRY��-��*HQ��0LFURELRO��129: ����±�����

&ROOLQV��1�'���-�$�(��)DUURZ��9��.DWLF�DQG�2��.DQGOHU��������Taxonomic studies on streptococci of serological groups (��3��8�DQG�9��'HVFULSWLRQ�RI�Streptococcus porcinus sp. QRY��6\VW��$SSO��0LFURELRO��5:����±����

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+DUWPDQQ��(���+��.|QLJ��2��.DQGOHU�DQG�:��+DPPHV��������Isolation of a nucleotided activated disaccharide penta-peptide precursor from Methanobacterium thermoauto-trophicum.�)(06�0LFURELRO��/HWW��61:����±����

+HQVHO��5��:��'HPKDUWHU��2��.DQGOHU��5�0��.URSSHQVWHGW�DQG� (�� 6WDFNHEUDQGW�� ������ &KHPR�WD[RQRPLF� DQG�PR-lecular-genetgic studies on the genus Thermus ±�HYLGHQFH�for a phylogenetic relationship of Thermus aquaticus and Thermus ruber to the genus Deinococcus. ,QW�� -�� 6\VW��Bacteriol. 36: ���±���

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147

Karl-Heinz Schleifer

The Bulletin of BISMiS

the cell walls of Methanosarcina barkeri.�$UFK��0LFUR-biol. 113:���±���

.DQGOHU�� 2�� DQG� +�� +RSI�� ������ 2FFXUUHQFH�� PHWDEROLVP�and function of oligosaccharides. In The Biochemistry of 3ODQWV�� YRO�� �� �HGLWHG� E\� 3UHLVV���$FDGHPLF� 3UHVV��1HZ�<RUN��SS�����±����

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.DQGOHU��*��DQG�2��.DQGOHU��������8QWHUVXFKXQJHQ��EHU�GLH�0RUSKRORJLH�XQG�GLH�9HUPHKUXQJ�GHU�SOHXURSQHXPRQLH�lKQOLFKHQ�2UJDQLVPHQ�XQG�GHU�/�3KDVH�GHU�%DNWHULHQ��,��/LFKWPLNURVNRSLVFKH�8QWHUVXFKXQJHQ��$UFK��0LNURELRO��21:���±����

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.|QLJ��+��DQG�2��.DQGOHU������D��7KH�DPLQR�DFLG�VHTXHQFH�of the peptide moiety of the pseudomurein from Metha-nobacterium thermoautotrophicum.� $UFK�� 0LFURELRO��121: ���±����

.|QLJ��+��DQG�2��.DQGOHU������E��N�$FHW\OWDORVDPLQRXURQ-LF�DFLG��D�FRQVWLWXHQW�RI� WKH�SVHXGRPXUHLQ�RI� WKH�JHQXV�Methanobacterium.�$UFK��0LFURELRO��123: ���±����

.|QLJ��+���2��.DQGOHU�DQG�:��+DPPHV��������%LRV\QWKHVLV�RI� SVHXGRPXUHLQ�� LVRODWLRQ� RI� SXWDWLYH� SUHFXUVRUV� IURP�Methanobacterium thermoautotrophicum.�&DQ��-��0LFUR-biol. 12: ���±����

.|QLJ��+����5��.UDOLN�DQG�2��.DQGOHU��������6WUXFWXUH�DQG�PRGL¿FDWLRQ� RI� SVHXGRPXUHLQ� LQ� Methanobacteriales. =EO��%DNW��+\J��,��$EW��2ULJ��C3: ���±����

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/DXHU��(��DQG�2��.DQGOHU��������0HFKDQLVPXV�GHU�9DULDWLRQ�GHV� 9HUKlOWQLVVHV�$FHWDW�/DFWDW� EHL� GHU� 9HUJlUXQJ� YRQ�*OXFRVH� GXUFK� %L¿GREDNWHULHQ�� $UFK�� 0LNURELRO�� 109: ���±����

/DXHU�� (�� DQG�2��.DQGOHU�� ������Lactobacillus gasseri sp. nov., a new species oft he subgenus Thermobacterium. =HQWUDOEO��%DNWHULRO��$EW��2ULJ��&�1: ��±���

/DXHU��(��DQG�2��.DQGOHU��������'1$�'1$�KRPROJ\��PX-rein types and enzyme patterns in the type strains of the genus %L¿GREDFWHULXP��6\VW��$SSO��0LFURELRO��4:���±���

/HDYHU�� 0��� 3�� 'RPLQJXH]�&XHYDV�� -�0�� &R[KHDG�� 5�$��'DQLHO� DQG� -��(UULQJWRQ�� ������/LIH�ZLWKRXW� D� FHOO�ZDOO�or division machine in Bacillus subtilis.�1DWXUH�460:����

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148 The Bulletin of BISMiS

Otto Kandler: distinguished botanist and microbiologist

KLW]XQJ��0LOFKZLVVHQVFKDIWHQ�22:����±����3ODSS��5��DQG�2��.DQGOHU������D��=XU�:LUNXQJVZHLVH�]HOO-ZDQGKHPPHQGHU� $QWLELRWLFD� EHL� JUDPQHJDWLYHQ� %DN-WHULHQ��,��'LH�:LUNXQJ�YRQ�3HQLFLOOLQ�DXI�GLH�.RQ]HQWUD-WLRQ�YRQ�=HOOZDQGYRUVWXIHQ�EHL�Proteus mirabilis.�$UFK��0LNURELRO��50:����±����

3ODSS�� 5�� DQG�2��.DQGOHU�� ����E�� =XU�:LUNXQVZHLVH� ]HOO-ZDQGKHPPHQGHU� $QWLELRWLFD� EHL� JUDPQHJDWLYHQ� %DN-terien. I. Die Wirkung von d�&\FORVHULQ�DXI�GLH�.RQ]HQ-WUDWLRQ�YRQ�=HOOZDQGYRUVWXIHQ�EHL�Proteus mirabilis und GHVVHQ�/�3KDVH��$UFK��0LNURELRO��50:����±����

5DX�+XQG��$��DQG�2��.DQGOHU��������'LH�:LUNXQJ�YRQ�3HQL-FLOOLQ�DXI�GHQ�(LQEDX�PDUNLHUWHU�$PLQRVlXUHQ�LQ�GLH�=HOO-ZDQG�GHU�%DNWHULHQ��=HQWUDOEO��%DNWHULRO��,�184: ���±���

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6FKOHLIHU��.�+��DQG�2��.DQGOHU��������3HSWLGRJO\FDQ�W\SHV�of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:����±����

6FKOHLIHU�� .�+�� DQG�2�� .DQGOHU�� ������ 3ULPDU\� VWUXFWXUHV�of murein and pseudomurein. In�7KH�7DUJHW�RI�3HQLFLOOLQ��HGLWHG�E\�+DNHQEHFN��+|OWMH�DQG�/DELVFKLQVNL���:DOWHU�GH�*UX\WHU��%HUOLQ��SS����±���

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6FKRO]��7���:��'HPKDUWHU��5��+HQVHO�DQG�2��.DQGOHU��������Bacillus pallidus sp. nov., a new thermophilic species IURP�VHZDJH��6\VW��$SSO��0LFURELRO��9:���±���

6RXWVFKHN��(���-��:LQWHU��)��6FKLQGOHU�DQG�2��.DQGOHU��������$FHWRPLFURELXP� ÀDYLGXP gen. nov., sp. nov., a thermo-philic anaerobic bacterium from sewage sludge, forming DFHWDWH��&2��DQG�+��IURP�JOXFRVH��6\VW��$SSO��0LFURELRO��5: ���±����

6WDFNHEUDQGW�� (�� DQG�2��.DQGOHU�� ������7D[RQRP\� RI� WKH�genus Cellulomonas based on phenotypical characters DQG� '1$�'1$� KRPRORJ\�� ,QW�� -�� 6\VW�� %DFWHULRO�� 29: ���±����

6WDFNHEUDQGW��(��DQG�2��.DQGOHU��������Cellulomonas car-tae�VS��QRY��,QW��-��6\VW��%DFWHULRO��30:����±���

6WHEHU��-��DQG�.�+��6FKOHLIHU��������Halococcus morrhuae��a sulfated heteropolysaccharide as structural component RI�WKH�EDFWHULDO�FHOO�ZDOO��$UFK��0LNURELRO��105:����±����

6WHWWHU�� .�2�� DQG� 2�� .DQGOHU�� ������ 8QWHUVXFKXQJHQ� ]XU�(QWVWHKXQJ� YRQ� dl�0LOFKVlXUH� EHL� /DNWRED]LOOHQ� XQG�&KDUDNWHULVLHUXQJ�HLQHU�0LOFKVlXUHUDFHPDVH�XQG�HLQLJHQ�$UWHQ� GHU� 8QWHUJDWWXQJ� Streptobacterium. $UFK��0LNUR-biol. 94:����±����

7DQQHU��:���0��/|IÀHU�DQG�2��.DQGOHU��������&\FOLF�SKRWR-phosphorylation in vivo and its relation to photosynthetic &2��¿[DWLRQ��3ODQW�3K\VLRO��44:����±����

:HLVV��1���0��%XVVH�DQG�2��.DQGOHU��������'LH�+HUNXQIW�YRQ�*lUXQJVQHEHQSURGXNWHQ� EHL� GHU�0LOFKVlXUHJlUXQJ� YRQ�Lactobacillus acidophilus.�$UFK��0LNURELRO��62:���±���

:HLVV��1���8��6FKLOOLQJHU��0��/DWHUQVHU�DQG�2��.DQGOHU��������Lactobacillus sharpie sp. nov. and Lactobacillus agilis sp. nov., two new species of homofermentative, meso-diami-nopimelic acid-containing lactobacilli isolated from sew-DJH��=HQWUDOEO��%DNWHULRO��2ULJ��&�2:����±����

:RHVH��&�5���2�.DQGOHU�DQG�0��:KHHOLV��������7RZDUGV�D�QDWXUDO�V\VWHP�RI�RUJDQLVPV��SURSRVDOV�IRU�WKH�GRPDLQV�Archaea, Bacteria and Eucarya.� 3URF�� 1DWO��$FDG�� 6FL��8�6�$��87:�����±�����

=LOOLJ��:���5��6FKQDEHO�� -��7X�DQG�.�2��6WHWWHU��������7KH�SK\ORJHQ\�RI�$UFKDHEDFWHULD��LQFOXGLQJ�QRYHO�DQDHURELF�WKHUPRDFLGRSKLOHV�LQ�WKH�OLJKW�RI�51$�SRO\PHUDVH�VWUXF-WXUH��1DWXUZLVVHQVFKDIWHQ�69:����±����

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149© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 149–162

Contact detailsInstitute of Ecology and Evolution, 5289 University of Oregon, Eu-gene, OR 97403, USA.

[email protected]

Richard W. Castenholz

My life as a microbiologist and naturalist

The early years

7KLV�DUWLFOH�LV�IRFXVHG�RQ�HYHQWV�LQ�P\�OLIH�WKDW�LQÀXHQFHG�P\�FDUHHU�DV�D�PLFURELRORJLVW��([FHSW�IRU�D�IHZ�IDPLO\�UHI-erences and photographs, the personal aspects of my life are excluded. The recollections are mainly in chronological order.

,� WXUQHG���� LQ�0D\�RI�������7KH� WKRXJKW�RI� UHWLUHPHQW� LV�repellent and saddening, but inevitable. I don’t want to sit EDFN�DQG�HQMR\�VRPH�VRUW�RI�LQYHQWHG�KREE\��0\�KREE\�LV�and will continue to be observing and investigating photo-trophic micro-organisms in and from strange and sometimes extreme environments. I have had many other avocations, such as jogging, cross-country skiing, backpack camping, and birding, but recently these have suffered as a result of my twin hip replacements.

%XW� LGHQWL¿FDWLRQ�DQG�FODVVL¿FDWLRQ�RI�YDULRXV�REMHFWV�KDV�always been a large part of my interests. These interests be-gan early. When six years old I would sit on our porch or front window and identify the makes of cars going by. For-tunately, it was a quiet suburban street, so this happened only occasionally. I suppose I had some book guide, but I kept a notebook since I was able to spell and read. When I was seven my parents and I went on a trip for several weeks to WKH�ZHVW�FRDVW�E\�UDLO��&KLFDJR�1RUWKZHVWHUQ�8QLRQ�3DFL¿F��in which we had a drawing room with bunks for all of us �SUREDEO\�QRWKLQJ�OLNH�WKLV�H[LVWV�WRGD\���$W�WKDW�WLPH��VHHLQJ�mountains, desert, and prairie made me decide that eventu-DOO\�,�ZRXOG�OLYH�LQ�WKH�:HVW��QRW�&KLFDJR�RU�WKH�0LGZHVW�

,�ZDV�ERUQ�LQ�&KLFDJR�LQ������DQG�OLYHG�LQ�2DN�3DUN��,OOLQRLV��D�ZHVWHUQ�VXEXUE�RI�&KLFDJR���ZLWK�P\�PRWKHU��/LOOLDQ��DQG�father, William, through infancy and youth up through the IRXU�\HDUV� LQ�2DN�3DUN�5LYHU�)RUHVW�+LJK�6FKRRO��:KHQ�,�was old enough to walk around the block or the neighbor-hood, I made a census of dog breeds that I could see in yards. 6LQFH� WKLV�ZDV�DQ�XSVFDOH�VXEXUE��,� WKLQN� WKDW�PRVW�RI� WKH�dogs were pure breeds, and therefore easy to identify. Dur-LQJ�ZLQWHU�RI��WK�JUDGH�,�ZDONHG�RYHU�WKH�ZKROH�VXEXUE�DQG�

counted all the robin nests in the barren elm trees that lined WKH�VWUHHWV��,�EHFDPH�D�ELUGZDWFKHU�LQ������DQG�NHSW�D�UHFRUG�RI�ZKDW�VSHFLHV� ,� VDZ�HYHU\�GD\�XQWLO�������D�\HDU�DIWHU� ,�VWDUWHG�FROOHJH�DW�WKH�8QLYHUVLW\�RI�0LFKLJDQ��,�KDG�HQOLVWHG�IRXU�RI�P\�IULHQGV� LQWR�ELUG� LGHQWL¿FDWLRQ�� ,W� LV� LQWHUHVWLQJ�to look over these notebooks, because I also noted who was ZLWK�PH�RQ� WKH�ZHHNHQG� WULSV��$OPRVW�DOO�RI� WKHVH�IULHQGV�are deceased.

,Q�KLJK�VFKRRO� ,�ZDV�GH¿QLWHO\�D�QHUG��2QH� IULHQG� �:LOO\��was as enthusiastic as I, and we competed with members RI� WKH� &KLFDJR�2UQLWKRORJLFDO� 6RFLHW\� IRU� WKH�PRVW� ELUGV�VLJKWHG��LGHQWL¿HG��DQG�YHUL¿HG�LQ�������+RZHYHU�����\HDU�ROG�SOXV�$P\�*��%DOGZLQ�ZRQ�E\�WKUHH�VSHFLHV�RYHU�P\�OLVW��+HU�DGYDQWDJH�ZDV�WKDW�VKH�ZRUNHG�DOO�QLJKW�DV�D�QXUVH�DW�6W�/XNH¶V� DQG�KDG� WKH�GD\WLPH� IUHH� HYHU\�GD\��6KH�ZDV�D�humorous and gracious person, and during my college days I came back to Chicago regularly and on a couple of occa-VLRQV�WRRN�KHU�WR�WKH�&KLFDJR�6\PSKRQ\��7KHUH�ZHUH�PDQ\�RWKHUV�LQ�WKH�&26�ZKR�EHFDPH�ZHHNHQG�IULHQGV��,W�ZDV�D�ELW�scary to go to the monthly meetings, since they were in the )LHOG�0XVHXP�DW�QLJKW�ZLWK�WKH�HQWU\�DOPRVW�GDUN�DQG�WKH�&DUO�$NHOH\�HOHSKDQWV�ORRPLQJ�

$OWKRXJK�VKRUW�OLYHG��,�DOVR�GHFLGHG�WR�LGHQWLI\�DQG�OLVW�DOO�the native trees and shrubs in one of the major forest pre-serves on the west side of the Chicago suburbs, using a rather detailed book. I was unable to recruit friends for this endeavor, since the summer was very hot and humid.

$QRWKHU� H[WUDFXUULFXODU� DFWLYLW\� GXULQJ� WKH� ¿UVW� RU� VHFRQG�year of high school was a weekly meeting that three of my IULHQGV�DQG�,�KHOG�IRU�DW�OHDVW���PRQWKV��7KLV�ZDV�D�³ELRORJ\�club” in which each of us had responsibility for a group of DQLPDO�SK\OD�RU�ERWDQLFDO�GLYLVLRQV��(DFK�RI�XV�ZRXOG�JLYH�D�

“report” or description and initiate a discussion for each ani-PDO�RU�ERWDQLFDO�JURXS��$OWKRXJK�LW�VRXQGV�VHULRXV�HDFK�HYH-ning was quite entertaining, and I remember the argument as to who should have the responsibility for “sea squirts”.

%HFDXVH� RI�P\� DFTXLUHG� H[SHUWLVH� LQ� ELUG� LGHQWL¿FDWLRQ�� ,�ZDV�LQYLWHG�E\�GLVWDQW�FRXVLQV�0DUJDUHW�DQG�0RUH\�WR�VSHQG�WKH�VXPPHUV�RI������DQG������DW�WKHLU�SODFH�RQ�WKH�/LWWOH�6SRNDQH�5LYHU��QRUWK�RI�6SRNDQH��PDLQO\�WR�WHDFK�WKHP�KRZ�to identify the birds of the area. We became very close until WKHLU�GHDWKV�DERXW����\HDUV�ODWHU�DQG�,�UHPDLQ�VR�ZLWK�WKHLU�VRQ�%DUW�DQG�KLV�ZLIH�/LQGHOO�

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150

My life as a microbiologist and naturalist

The Bulletin of BISMiS

In addition to the bird-watching activity, I had some great WHDFKHUV� LQ�KLJK�VFKRRO��0U�3ULFH��ZKR� WDXJKW�DQFLHQW�KLV-WRU\�DQG�ORRNHG�LQ�SUR¿OH�OLNH�RQH�RI�WKH�(J\SWLDQ�SKDUDRKV��0LVV�+DUGLH��ZKR�VWLPXODWHG�P\�UHDGLQJ�RI�-RVHSK�&RQUDG�DQG�-DPHV�)HQLPRUH�&RRSHU�DV�ZHOO�DV� WKH� UHTXLUHG�'LFN-HQV�DQG�RWKHUV��0LVV�0XLU��ZKR�EURXJKW�/DWLQ�WR�OLIH�E\�KHU�descriptions and slides of Rome where she visited every VXPPHU�� DQG�0LVV�7XUQHU��ZKR� WDXJKW� D� \HDU� RI� SK\VLFDO�JHRJUDSK\�DQG�JHRORJ\��7KHQ�WKHUH�ZDV�P\�IULHQG��0U�0F-0HQDPLQ��ZKR�WDXJKW�D�ZKROH�\HDU�RI�ERWDQ\��'XULQJ�WKDW�year I had already developed an interest in algae and aquatic plants, and was asked by him to illustrate the algal part of his lab manual, which I did.

The interest in natural history developed along with bird watching from my weeks in northern Wisconsin during many summers when I was a teenager. I was invited there �QHDU�6D\QHU��E\�P\�IDWKHU¶V�¿UVW�FRXVLQ�$P\�DQG�KHU�*HU-PDQ�KXVEDQG�/RXLV��D�IRUPHU�IRUHVWHU�DQG�UHWLUHG�HOHFWULFDO�engineer). They were childless and more or less adopted me. 7KH\�RZQHG����DFUHV�DW�WKH�HQG�RI�WKH�URDG�DW�3OXP�/DNH��right across from Wilmotte’s Island with its tall pines and a ODUJH�KRXVH�ZLWK�D�VLGLQJ�RI�SLQH�EDUN��/RXLV�ZDV�D�UHPDUN-able man who taught me the art of silently following porcu-SLQHV��EHDUV��DQG�RWKHU�DQLPDOV�GRZQZLQG��+H�DOVR�NQHZ�WKH�local birds and we went deer spotting almost every evening. :H�¿VKHG�WRJHWKHU�DQG�HYHU\�HYHQLQJ�KH�VDW�ZLWK�D�FLJDU�WKDW�he rolled slowly in his mouth as we conversed about life and VFLHQFH��+RZHYHU�� LW�ZDV� DW� WKLV� WLPH� WKDW� ,� VWDUWHG� VZLP-ming underwater with a face mask and became fascinated by algae and aquatic plants, an interest that continued through-RXW�P\�OLIH��$V�D�UHVXOW��,�JDYH�XS�¿VKLQJ�IRUHYHU�

The undergraduate years

+LJK�VFKRRO�ZDV�DQ�LQWHUHVWLQJ�WLPH�IRU�PH�LQ�VHYHUDO�ZD\V��,W�ZDV�D�SHULRG�RI�JUHDW�LQGHFLVLRQ��$OWKRXJK�,�ZDV�JUHDWO\�LQ-terested in birds and their habits, I thought that the only way to make a living using this skill was to go into the Fish and :LOGOLIH�6HUYLFH��7KHUHIRUH��P\�¿UVW�\HDU�DW�0LFKLJDQ�ZDV�DV�D�ZLOGOLIH�PDQDJHPHQW�PDMRU�WKDW�ZDV�WKHQ�LQ�WKH�6FKRRO�of Forestry. This meant summer at the university forestry camp with forest mensuration, logging practice, engineering GUDZLQJ��DQG�RWKHU�VXEMHFWV�RI�OLWWOH�LQWHUHVW�WR�PH��+RZHYHU��E\� WKH� HQG� RI� WKH�¿UVW� \HDU� DW�0LFKLJDQ� ,� KDG�PDGH� GUDV-tic changes and dropped out of forestry school. I had a full \HDU�RI�ERWDQ\�E\�WZR�JUHDW�WHDFKHUV��)�.��6SDUURZ�WDXJKW�IRU� WKH� LQWURGXFWRU\� VHPHVWHU� ±� LW�ZDV� IDVFLQDWLQJ�KRZ�KH�presented what could have been a very dull course. The sec-RQG�VHPHVWHU�ZDV�E\�(O]DGD�&ORYHU��ZKR�WDXJKW�6\VWHPDWLF�%RWDQ\��6KH�ZDV�WKH�¿UVW�ZRPDQ�WR�UDIW�WKH�&RORUDGR�5LYHU�WKURXJK�WKH�*UDQG�&DQ\RQ��+HU�HQWKXVLDVP�FRQYLQFHG�PH�

that I should major in botany and make a living by teach-LQJ�DQG�GRLQJ�UHVHDUFK�LQ�WKDW�¿HOG��HYHQ�WKRXJK�DW�WKH�WLPH�teaching was a terrifying prospect. This anxiety was some-what relieved by my oral presentation as a sophomore in an evening seminar in an ornithology course.

'U�6SDUURZ�DOORZHG�PH��DV�D�VRSKRPRUH��LQWR�KLV�JUDGXDWH�FRXUVH�RQ�DTXDWLF�ÀRZHULQJ�SODQWV�LQ�ZKLFK�,�WKULYHG��DQG�later into a course on “aquatic fungi”. William Randolph Taylor taught a course in algae and lower plants as well as RQH�LQ�IUHVKZDWHU�DOJDH��$OWKRXJK�KH�ZDV�XQRI¿FLDOO\�YRWHG�the most boring lecturer in the Botany Department, I found the subject and his great knowledge of the subject compel-OLQJ��1RW�RQO\�GLG�,�WDNH�WKHVH�FRXUVHV��EXW�,�VLJQHG�XS�IRU�undergraduate research with Taylor in order to learn the PDULQH�DOJDH�RI�WKH�QRUWK�3DFL¿F�ZKHUH�,�ZDV�H[SHFWHG�WR�JR�ZLWK� WKH�XQLYHUVLW\� H[SHGLWLRQ� WR� WKH�$OHXWLDQV��0\� UH-sponsibility was for collecting and preserving the algae. I ZDV�LQFOXGHG�LQ�WKLV�H[SHGLWLRQ�E\�SURIHVVRU�+DUOH\�%DUWOHWW��³8QFOH� +DUOH\´�� ZKR� IUHTXHQWO\� LQYROYHG� XQGHUJUDGV� LQ�UHVHDUFK�� 8QIRUWXQDWHO\�� WKH� .RUHDQ�:DU� EHJDQ� WKDW� VXP-PHU�DQG�WKH�1DY\�GHFODUHG�WKH�$OHXWLDQV�RII�OLPLWV��&RQVH-TXHQWO\� ,�VSHQW�D�VHFRQG�VXPPHU�ZRUNLQJ�IRU� WKH�86�)RU-HVW�6HUYLFH�IURP�D�SDFN�FDPS�QRUWK�RI�3ULHVW�5LYHU��,GDKR��pulling Ribes� �FXUUDQWV� DQG� JRRVHEHUULHV�� LQ� D�ZKLWH� SLQH�blister control effort. The only reading I had with me was *�0��6PLWK¶V�Cryptogamic Botany, Vol. I (Algae and Fungi), ZKLFK�,�ZHQW�RYHU�VHYHUDO� WLPHV��1RZDGD\V� ,�SUHIHU�JRRG�¿FWLRQ��/DWHU��GXULQJ�WKH�.RUHDQ�:DU�,�MRLQHG�WKH�1DYDO�$LU�Reserve, but was never activated nor advanced above “sea-man recruit”.

,�VSHQW�WKH�QH[W�VXPPHU��������DW�WKH�0LFKLJDQ�ELRORJLFDO�VWDWLRQ�DW�'RXJODV�/DNH��DQG�WKHUH�,�UHDFKHG�P\�WUXH�GHSWK�in the study of algae, taking two courses on freshwater algae IURP�*LOEHUW�0RUJDQ�6PLWK��ZKR�KDG�UHFHQWO\�UHWLUHG�IURP�6WDQIRUG��,Q�KLV�DGYDQFHG�FODVV�ZLWK�RQO\�DERXW�VL[�VWXGHQWV�he ended the day with martinis served in his cottage for all VWXGHQWV�ZKR�ZLVKHG�WR�SDUWDNH��+LV�ZLIH�ZDV�WKH�PRVW�DF-tive spouse at the station, and she taught swimming for all WKH�FKLOGUHQ�RI�IDFXOW\�DQG�VWXGHQWV��,�EHOLHYH�6PLWK�WRRN�D�particular liking to me, for after the session, it turned out WKDW�KH�ZDV�VWD\LQJ�RQ�3OXP�/DNH�DW�D�VLVWHU¶V�FRWWDJH��DQG�I was across the lake at my father’s cousin, so I was invited WR�URZ�RYHU�DQG�KDYH�FRFNWDLOV�ZLWK�KLP�DQG�IDPLO\��/DWHU�LQ�WKH�VXPPHU�,�GURYH�ZLWK�P\�IULHQG�:LOO\�WR�0H[LFR��ZKHUH�ZH� LGHQWL¿HG� PDQ\� QHZ� ELUGV�� DQG� RQ� WKH� ZD\� EDFN� YLD�&DOLIRUQLD�ZH�VWRSSHG�DW�WKH�6PLWK�KRPH�LQ�3DOR�$OWR��ZH�had been invited) and had a home-cooked dinner with him DQG�KLV�ZLIH��'XULQJ�WKDW�YLVLW�KH�SKRQHG�*HRUJH�3DSHQIXVV�at Berkeley by way of introduction and the next day I was VKRZQ�DURXQG�WKH�KHUEDULXP�DQG�GHSDUWPHQW�E\�3DSHQIXVV��

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151

Richard W. Castenholz

The Bulletin of BISMiS

,Q�D�ODWHU�\HDU��DW�RQH�RI�P\�HDUO\�QDWLRQDO�PHHWLQJV��*�0��6PLWK�LQWURGXFHG�PH�WR�VHYHUDO�SURPLQHQW�SK\FRORJLVWV�DV�D�SURPLVLQJ�\RXQJ�VFLHQWLVW�LQ�WKH�¿HOG��+LV�GHDWK�LQ������was a sad event.

The Graduate School years

$IWHU� JUDGXDWLQJ� IURP�0LFKLJDQ� LQ� ������ ,�ZDV� ³VHQW´� E\�7D\ORU�DV�DQ�06�VWXGHQW�WR�WKH�8QLYHUVLW\�RI�0LDPL�0DULQH�6WDWLRQ��DW�WKLV�WLPH�VWLOO�LQ�&RUDO�*DEOHV��LQ�RUGHU�WR�OHDUQ�marine algae of this area with the intention of coming back WR�ZRUN�ZLWK�7D\ORU�IRU�D�3K'�D�\HDU�ODWHU��$W�0LDPL�,�ZDV�on a fellowship that involved my creating a marine algal herbarium for the institute based almost entirely on my own collections. Besides taking courses in marine ecology, phy-cology, and oceanography, I had to do a large number of collecting trips on my own in order to service the new her-EDULXP��(YHU\��±��ZHHNV�,�WRRN�SDUW�LQ�D�UHVHDUFK�WULS�LQWR�WKH�*XOI�6WUHDP�WR�VWXG\�WKH�YHUWLFDO�PLJUDWLRQ�RI�WKH�³GHHS�VFDWWHULQJ�OD\HU´��YDULRXV�LQYHUWHEUDWHV��RYHU�GLHO�SHULRGV�DV�SDUW�RI�WKH�UHVHDUFK�SURJUDP�RI�'U�+LODU\�0RRUH��$V�SDUW�RI�his marine ecology course I did a study on the effects of tidal emergence and submergence times on the growth of the red alga Bostrychia sp. on mangrove roots. I “camped” out sev-eral weekends for this study, in the then undeveloped Bear Cut on Biscayne Bay, cooking lamb’s kidneys and veggies RYHU�RSHQ�¿UHV�

'XULQJ�WKH�ZLQWHU�EUHDN��,�KLWFK�KLNHG�IURP�0LDPL�WR�0DUD-WKRQ��7H[DV��WR�PHHW�D�IHOORZ�SK\FRORJLVW��9HUQRQ�3URFWRU��ZKR�ZDV�ZRUNLQJ�RQ�KLV�3K'�DW�WKH�8QLYHUVLW\�RI�0LVVRXUL��:H�WKHQ�JRW�D�ULGH�WR�WKH�&KLVRV�0RXQWDLQV�LQ�%LJ�%HQG�1D-WLRQDO�3DUN��FDPSLQJ�DQG�FROOHFWLQJ�DOJDH�IURP�HSKHPHUDO�SRQGV��:H�EHFDPH�IULHQGV� LQ������ZKHQ�ZH�ERWK�ZRUNHG�IRU�.DQLNVX�1DWLRQDO�)RUHVW�LQ�QRUWKHUQ�,GDKR��DQG�WHQWHG�DW�3HONH�&DPS��&OHP�:DOODFH�ZDV�D�YHU\�NLQG�DQG�LQWURVSHF-tive camp boss, and he taught everyone who wished to know DOO�WKH�SODQWV�RI�WKH�IRUHVW��2Q�WKH�ZD\�WR�7H[DV��,�KDG�YDUL-ous adventures, the worst being waking up in my sleeping bag next to a large coiled-up diamond back rattlesnake in the woods outside of Chipley, Florida.

,QVWHDG�RI�UHWXUQLQJ�WR�0LFKLJDQ�ZKHUH�,�KDG�DOUHDG\�EHHQ�accepted as a grad student, I decided to try elsewhere for D�3K'��,�ZDV�DFFHSWHG�DW�86&�DQG�%ULWLVK�&ROXPELD�ZLWK�¿QDQFLDO�DLG��EXW�UHDOL]HG�WKLV�ZRXOG�PHDQ�ZRUNLQJ�RQ�PD-ULQH� DOJDO� WD[RQRP\�ZLWK�'DZVRQ� RU� 6FDJHO�� UHVSHFWLYHO\��so I decided to accept a teaching fellowship at Washington 6WDWH�8QLYHUVLW\�DW�3XOOPDQ��KRSLQJ�WR�ZRUN�RQ�VRPH�DVSHFW�of freshwater algal ecology. There was another reason, how-ever. I wanted to be close to my “adopted parents” on the /LWWOH�6SRNDQH��$OWKRXJK� WKHUH�ZDV�QR�RQH�DW�:DVKLQJWRQ�

6WDWH�ZKR�FXUUHQWO\�GLG�UHVHDUFK�LQ�P\�¿HOG��1RH�+LJLQER-WKDP�ZDV�YHU\�NQRZOHGJHDEOH�DQG�WRRN�PH�RQ�DV�KLV�3K'�VWXGHQW��,�ZLOO�QHYHU�UHJUHW�ZRUNLQJ�ZLWK�KLP��+H�WRRN�JUHDW�LQWHUHVW� LQ�P\�UHVHDUFK�DQG�JDYH�H[FHOOHQW�DGYLFH��+H�DQG�KLV�ZLIH�EHFDPH�SDUW�RI�P\� OLIH� DQG� WKDW�RI�P\�¿UVW�ZLIH��0DUJLW�+ROOHUXG��ZKRP� ,�PHW� LQ� 3XOOPDQ� DQG�PDUULHG� LQ�������0\�ZRUN�IRU�WKH�GHJUHH�ZDV�D�VWXG\�RI�WKH�VHDVRQDO�productivity of sessile diatoms in a series of lakes in the /RZHU� *UDQG� &RXOHH�� UDQJLQJ� IURP� IUHVKZDWHU� WR� VDOLQH�PHURPLFWLF�DW�WKH�HQG�RI�WKH����PLOH�FDQ\RQ��7KLV�ZDV�ODWHU�published in Limnology and Oceanography� �H�J�� &DVWHQ-KRO]��������DQG� IDYRUDEO\�GHVFULEHG� LQ�*�(��+XWFKLQVRQ¶V�Treatise in Limnology�� 9RO�� �� �������� SXEOLVKHG� E\� -RKQ�:LOH\��6RQV��6LQFH�GLDWRP�WD[RQRP\�UHTXLUHG�WKH�H[SHU-WLVH�RI� VSHFLDOLVWV�� ,� VSHQW�PRVW�RI� WKH� VXPPHU�RI������DW�WKH�$FDGHP\�RI�1DWXUDO�6FLHQFHV�RI�3KLODGHOSKLD�FKHFNLQJ�P\�LGHQWL¿FDWLRQV�ZLWK�5XWK�3DWULFN��WKHQ�WKH�ZRUOG�H[SHUW�RQ�GLDWRP�WD[RQRP\��$W�:68�WKHUH�ZHUH�VHYHUDO�H[FHOOHQW�WHDFKHUV��7KH\� LQFOXGHG�%RE�+XQJDWH� �PLFURELRORJLVW�par excellence���5H[IRUG�'DXEHQPLUH��RXWVWDQGLQJ�SODQW�HFROR-JLVW���$GROSK�+HFKW��DQG�0DULRQ�2ZQE\��2ZQE\� WDXJKW�D�full year of advanced systematic botany in which all orders of plants worldwide were considered.

$W�WKH�WLPH�RI�P\�GHIHQVH�LQ�������WKHUH�ZHUH�IHZ�SRVW�GRF�RSSRUWXQLWLHV��)LJXUH�����$OWKRXJK�,�DSSOLHG�IRU�D�)XOEULJKW�6FKRODUVKLS� WR�ZRUN�ZLWK�+HLQULFKV�6NXMD� LQ�6ZHGHQ�� WKH�IHZ�RWKHU�RSSRUWXQLWLHV�LQ�P\�¿HOG�ZHUH�WZR�WHPSRUDU\�DFD-

Figure 1. Richard Castenholz with mother, Lillian, and father, William, at time of Dick’s receiving PhD at Wash-ington State University, Pullman 1957.

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My life as a microbiologist and naturalist

The Bulletin of BISMiS

demic positions in the West, and a couple of jobs at state colleges in California, who at that time stated that time for research was not allowed. Therefore, I was extremely fortu-QDWH�LQ�¿QGLQJ�DQ�RSHQLQJ�DW�WKH�8QLYHUVLW\�RI�2UHJRQ��DQ�RSHQLQJ�FDXVHG�E\�WKH�PRYH�RI�SK\FRORJLVW�$O�%HUQDWRZLW]�IURP�2UHJRQ�WR�+DZDLL��,�ZDV�KLUHG�DV�D�WHQXUH�WUDFN�LQVWUXF-tor that was followed a year later as an assistant professor. 0\�ZLIH�DQG�,�KDG�YLVLWHG�2UHJRQ�D�\HDU�HDUOLHU�LQYLWHG�E\�D�IULHQG�ZKRP�,�NQHZ�DW�0LFKLJDQ��-DNH�6WUDXV��,�DP�VXUH�WKDW�-DNH¶V�SUHVHQFH�DW�2UHJRQ�LQÀXHQFHG�WKH�GHFLVLRQ�WR�KLUH�PH�ZKHQ�WKH�¿HOG�KDG�EHHQ�QDUURZHG�WR�WZR��,Q�IDFW�,�NQHZ�-DNH�ZKHQ�,�ZDV�DQ�XQGHUJUDGXDWH�JODVVZDUH�ZDVKHU�DW�0LFKLJDQ�IRU�KLV�3K'�SURMHFW�XQGHU�&DUO�'��/D5XH��SODQW�HFRORJLVW�DQG�SK\VLRORJLVW�IURP�ZKRP�,�KDG�DQ�H[FHOOHQW�FRXUVH��/D5XH��DIWHU�KDYLQJ�KDG�D�KHDUW�DWWDFN�VWLOO�OHG�¿HOG�WULSV�LQ�KLV�SODQW�ecology class, but was carried by students on a homemade sedan chair.

The late 1950s and the 1960s at Oregon

7KXV�� LQ� IDOO� RI� ������ EHJDQ� WKH�¿UVW� DQG� RQO\� SHUPDQHQW�job in my life, a faculty position in the Department of Bi-RORJ\��8QLYHUVLW\�RI�2UHJRQ��WKDW�KDV�QRZ�ODVWHG����\HDUV��0\�WHDFKLQJ�ZDV�LQWHQVLYH�GXULQJ�WKH�¿UVW�FRXSOH�RI�\HDUV��courses in general biology, mycology, phycology, and plant PRUSKRORJ\��0\�FROOHDJXHV� WKHQ�ZHUH�-DNH�6WUDXV��6DQG\�7HSIHU�� 5DOSK� +XHVWLV�� &ODUHQFH� &ODQF\�� )UDQN� 6LSH�� -LP�.H]HU��%UDGOH\�6FKHHU��$UQROG�6KRWZHOO��%RE�0RUULV��3HWHU�)UDQN��/HUR\�'HWOLQJ��DQG�%D\DUG�0F&RQDXJKH\��WKH�HQWLUH�ELRORJ\�IDFXOW\��DOO�GHFHDVHG���,Q������WKH�,QVWLWXWH�RI�0R-OHFXODU�%LRORJ\�ZDV�IRUPHG�E\�$DURQ�1RYLFN�DQG�ODWHU�WKDW�\HDU�)UDQN�6WDKO�ZDV�DGGHG�

By this time I was convinced that studying micro-organisms, whether or not they had medical or commercial importance, was as legitimate as studying any organisms that shared the HDUWK�ZLWK�XV��0\�SRLQW�RI�YLHZ�IURP�WKHQ�RQ�ZDV� WKDW�RI�the micro-organisms themselves and how they managed to survive and thrive in their environments.

,Q� WKH� VXPPHU� RI� ������ ,� WDXJKW� WKH� SK\FRORJ\� FRXUVH� DW�2�,�0�%�� �2UHJRQ�,QVWLWXWH�RI�0DULQH�%LRORJ\�� LQ�&KDUOHV-WRQ��2UHJRQ��$OO�WROG�GXULQJ�P\�¿UVW�\HDU�,�HDUQHG��������D�VXP�WKDW�HQDEOHG�OLIH�ZLWK�DQ�DSDUWPHQW�UHQWDO��$�\HDU�ODWHU��ZH�ERXJKW�D�KRXVH�RQ�DQ�DFUH�RI�ODQG�IRU���������DQG�KDG�RXU�¿UVW�FKLOG��D�ER\�QDPHG�5HDYH�/DUV��,Q������ZH�DGRSWHG�D�ER\�ERUQ�WKDW�\HDU��5DOSK�$OH[��'XULQJ�VXEVHTXHQW�VXP-PHUV�DW�2�,�0�%��WKURXJK������,�WDXJKW�WKH�DOJDO�SDUW�RI�DQ�16)� LQVWLWXWH� LQ�PDULQH� ELRORJ\� IRU� FROOHJH� WHDFKHUV�ZKR�KDG�KDG�QR�PDULQH�H[SHULHQFH��ZKLOH�&DGHW�+DQG�RU�(XJHQH�.R]ORII�LQ�GLIIHUHQW�\HDUV�GLG�WKH�DQLPDO�SRUWLRQ��)LJXUH����

0\�UHVHDUFK�GXULQJ�WKHVH�HDUO\�\HDUV�DW�2UHJRQ�ZDV�RQ�WKH�

ecology of epilithic intertidal marine diatoms and the effect of gastropod grazers on the establishment and maintenance RI� WKHVH� GLDWRP�ELR¿OPV� �H�J��&DVWHQKRO]�� �������$QRWKHU�study established the effect of directional faces and timing of tides on the epilithic diatom species and their abundance.

,Q������RU�������,�WUDYHOOHG�WR�+XQWHU¶V�+RW�6SULQJV�QRUWK�RI�/DNHYLHZ��2UHJRQ��DQG�REVHUYHG�WKH�GLVWLQFW�DQG�DEUXSW�]RQDWLRQ�RI�F\DQREDFWHULD��WKHQ�FDOOHG�EOXH�JUHHQ�DOJDH��DV-sociated with the temperature gradient. I was fascinated by this striking picture and thought that these cyanobacteria PXVW�EH�YHU\�GLI¿FXOW�WR�FXOWXUH��VLQFH�,�FRXOG�QRW�¿QG�PXFK�LQ�WKH�OLWHUDWXUH��+RZHYHU��,�IRXQG�WKDW�LVRODWLRQ�DQG�FXOWXU-LQJ�ZDV� UHODWLYHO\� HDV\��7KXV��P\� ¿UVW� 3K'� VWXGHQW�� -DFN�3HDU\�� EHJDQ� DQG� ¿QLVKHG� KLV� UHVHDUFK� RQ� WKH� F\DQREDFWH-ULD�RI�+XQWHU¶V�+RW�6SULQJV��7KH�RULJLQDO�VPDOO�VWDNHV�WKDW�KH�SODFHG�WR�PHDVXUH�GLVWDQFHV�IURP�WKH�VRXUFH�RI�³-DFN¶V�6WUHDP´�VWLOO�H[LVW��L�H��LQ��������LQ�D�VWUHDP�WKDW�UDQJHG�IURP�a���&� WR� DERXW� ���&��$W� WKLV� WLPH� RU� VKRUWO\� WKHUHDIWHU� ,�shifted in part from marine epilithic diatioms to the physiol-ogy and ecology of thermophilic cyanobacteria. It becomes GLI¿FXOW� WR� GHVFULEH� WKH� SUROLIHUDWLRQ� RI� UHVHDUFK� WKDW� RF-curred after this shift. Tom Brock had already established WKDW�a���&�ZDV�WKH�XSSHU�WHPSHUDWXUH�OLPLW�IRU�F\DQREDFWH-ULD�LQ�<HOORZVWRQH�DONDOLQH�VSULQJV��DQG�WKH�VDPH�OLPLW�VWRRG�IRU�+XQWHU¶V�+RW�6SULQJV�DQG�ODWHU��HDVWHUQ�$VLD��LQ�DOO�FDVHV��a unicellular Synechococcus VS����3K'�VWXGHQW��-DFN�0HHNV��showed in one culture isolate that the growth range of this Synechococcus�ZDV�IURP����&�WR�a���&��WKXV��LW�ZDV�DQ�RE-OLJDWH�WKHUPRSKLOH��0HHNV�DQG�&DVWHQKRO]��������

/DWHU�� LW�ZDV� VKRZQ� WKDW���±���&�ZDV� WKH�XSSHU� OLPLW� IRU�Synechococcus DQG� RWKHU� F\DQREDFWHULD� LQ� ,FHODQG�� 1HZ�=HDODQG��DQG�(XURSH��VLPSO\�EHFDXVH�WKH�KLJK�WHPSHUDWXUH�species of Synechococcus did not exist in those locations �&DVWHQKRO]�� ������ ������ ������� ,Q� IDFW�� QR� WKHUPRSKLOLF�

Figure 2. Richard Castenholz with plankton sample on boat off the Oregon coast, 1960.

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Richard W. Castenholz

The Bulletin of BISMiS

species of Synechococcus has ever been found in Iceland springs, perhaps because of the relatively recent emergence RI�WKH�ODQG�VXUIDFH�IURP�XQGHU�D�WRWDO�LFH�FDS��,Q�+XQWHU¶V�+RW�6SULQJV��3HDU\�VKRZHG�ZLWK�FXOWXUHV�WKDW�WKHUH�ZHUH�DW�least four thermotypes of Synechococcus, indistinguishable by morphology that overlapped in temperature range and RSWLPD� �3HDU\� DQG� &DVWHQKRO]�� ������� /DWHU�� WKHVH� LGHQWL-FDO��RU�VLPLODU�WKHUPRW\SHV��DQG�WKH�KLJK�WHPSHUDWXUH�IRUP�ZHUH� VKRZQ� E\� D� ��6� U'1$�EDVHG� SK\ORJHQ\� WR� KDYH�HYROYHG�IURP�PRGHUDWH�WHPSHUDWXUH�W\SHV��0LOOHU�DQG�&DV-WHQKRO]��������

,Q������,�SDUWLFLSDWHG�LQ�WKH�,QWHUQDWLRQDO�/LPQRORJLFDO�&RQ-JUHVV� LQ�9LHQQD��P\�¿UVW� LQWHUQDWLRQDO�PHHWLQJ��&RPSDUHG�ZLWK�SUHVHQW�GD\� FRQIHUHQFHV� WKLV� RQH�ZDV�PDJQL¿FHQW�� ,W�UDQ�IRU�QHDUO\�D�ZHHN�LQ�9LHQQD��2QH�HYHQLQJ��LQ�D�QHDUE\�small village, new wine was available gratis at all the cellars. 2QH�GD\� WKHUH�ZDV�D�¿HOG� WULS� WR�/DNH�%DODWRQ�DQG� WR� WKH�(VWHUKD]\�3DODFH�LQ�(LVHQVWDGW�WR�OLVWHQ�WR�D�+D\GQ�TXDUWHW�LQ�WKH�YHQXH�ZKHUH�+D\GQ�FRPSRVHG�DQG�H[HUFLVHG�KLV�RU-FKHVWUD��,Q�DGGLWLRQ�WKHUH�ZDV�D���GD\�WULS�WKURXJK�WKH�ODNHV�RI�WKH�6DO]NDPPHUJXW�ZLWK�WKH�¿QDO�VHVVLRQV�RI�WKH�FRQJUHVV�LQ�6DO]EXUJ��0\�SUHVHQWDWLRQ�ZDV�VWLOO�RQ�GLDWRPV��DQG�GXU-ing this meeting I met some of the great limnologists and diatomologists.

7KH�ZRUN�ZLWK�GLDWRPV�FRQWLQXHG�GXULQJ�P\�¿UVW�VDEEDWLFDO�OHDYH� LQ�����±�����DW� WKH�%LRORJLVN�6WDWMRQ�DW�(VSHJUHQG��QHDU�%HUJHQ��1RUZD\��7KHUH� ,�PHDVXUHG� WKH�VHDVRQDO�SHUL-RGLFLW\�RI�VHVVLOH�PDULQH�GLDWRPV��&DVWHQKRO]���������$W�WKLV�

time I was well indoctrinated in the taxonomy of diatoms, DQ�³DUW´�OHDUQHG�ZHOO�IURP�5XWK�3DWULFN�LQ�3KLODGHOSKLD��7KH�YHQWXUH� LQWR� GLDWRP� HFRORJ\� RQ� WKH�1RUZHJLDQ� FRDVW�ZDV�P\�ODVW�IRU�GLDWRPV��6KRUWO\�DIWHU��LQ�������,�ZDV�SURPRWHG�to associate professor with tenure. During these early years P\�UHVHDUFK�ZDV�VXSSRUWHG�E\�16)��PXFK� ODWHU�E\�1$6$�as well.

,Q�������,�PDGH�P\�¿UVW�KRW�VSULQJ�H[SORUDWRU\�WULS�WR�<HO-ORZVWRQH�1DWLRQDO�3DUN��)LJXUHV���DQG�����7KHUH�,�PHW�7RP�Brock who had already begun his extensive work. Together ZH� H[SORUHG�PDQ\� KRW� VSULQJV�� XQRI¿FLDOO\� QDPLQJ� VRPH��Because of his height and great walking pace I had to run VRPHWLPHV�WR�NHHS�XS�ZLWK�KLP��,W�ZDV�QRW�XQWLO������WKDW�I seriously began culture isolations and temperature mea-VXUHPHQWV�LQ�<HOORZVWRQH��WRJHWKHU�ZLWK�WKUHH�3K'�VWXGHQWV�XQGHU�P\� GLUHFWLRQ� �%HY� 3LHUVRQ�� -DFN�0HHNV�� DQG� /DUU\�+DOIHQ��SOXV�WZR�XQGHUJUDGV�DQG�RQH�GRJ��7LQ\��DQG�FDPS-ing gear, all in one standard station wagon.

Late 1960s and the 1970s

,�KDG�VZLWFKHG�HQWLUHO\�DIWHU������WR�D�VWXG\�RI�WKH�FRPPX-nity ecology and physiological ecology of photosynthetic bacteria of hot springs, primarily cyanobacteria, but also of anoxygenic phototrophic bacteria. These studies eventually UHVXOWHG�LQ�RYHU����SXEOLFDWLRQV�LQYROYLQJ�WKH�HFRORJ\��SK\V-LRORJ\��DQG�EHKDYLRU�RI�RUJDQLVPV�RI�+XQWHU¶V�+RW�6SULQJV��H�J��&DVWHQKRO]��������:DUG�DQG�&DVWHQKRO]��������:DUG�HW�DO���������

Figure 3. Richard Castenholz with mother, Lillian, grandmother, Bertha Wandrey, and Reave, 7 years, and 5DOSK����\HDUV��DW�WKH�1RUWKHUQ�3DFLÀF�WUDLQ�GHSRW�LQ�Livingston, Montana, 1966.

Figure 4. Richard Castenholz with older son, Reave, and younger son, Ralph, at Big Lake, Oregon, 1967.

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/DWH�LQ�WKH�VXPPHU�RI������,�ÀHZ�WR�6ZLW]HUODQG�DQG�SUH-sented an annotated list of the cultured cyanobacteria in my FROOHFWLRQ�DW�D�PHHWLQJ�DW�WKH�OLPQRORJLFDO�VWDWLRQ�DW�.DVWD-QLHQEDXP�RQ�/DNH�/XFHUQH��7KH�KRVW�ZDV� WKH� UHPDUNDEOH�2WWR� -DDJ�ZKR� WUDQVODWHG� DOO� WKH� WDONV� LQ� )UHQFK� DQG�*HU-PDQ�LQWR�(QJOLVK�IRU�WKH�EHQH¿W�RI�%ULDQ�:KLWWRQ��7�9��'HVL-NDFKDU\��DQG�P\VHOI��7KH�86�PRRQ�ODQGLQJ�ZDV�DQQRXQFHG�IURP�WKH�FRFNSLW�RQ�WKH�RXWZDUG�ÀLJKW�RYHU�WKH�$WODQWLF�

7KH�\HDU������ZDV�YHU\�HYHQWIXO��)LUVW��WKHUH�ZDV�DQ�LQWHU-QDWLRQDO�PHHWLQJ�RQ�F\DQREDFWHULD�LQ�0DGUDV��,QGLD�KRVWHG�E\�7�9��'HVLNDFKDU\��0DQ\�QHZ�FROOHDJXHV�ZHUH�PHW�DV�ZHOO�DV�RWKHUV�DOUHDG\�NQRZQ��H�J��7RP�%URFN��%ULDQ�:KLWWRQ���This allowed me to travel and collect from hot springs in the QRUWKHUQ�VWDWH�RI�+LPDFKDO�3UDGHVK��KRVWHG�E\�D�FROOHDJXH�LQ�&KDQGLJDKU��2Q�WKH�UHWXUQ�,�VWRSSHG�LQ�-DSDQ��KDG�D�SUL-YDWHO\�FKDXIIHXUHG�WULS�E\�WKH�IDWKHU�RI�D�VWXGHQW�LQ�2UHJRQ��covering many hot springs from which several collections and isolates were obtained, including the type genus and species of &KORURÀH[XV�DXUDQWLDFXV�3LHUVRQ�DQG�&DVWHQKRO]�

7KH�\HDU�DOVR�LQFOXGHG�D�UHVHDUFK�WULS�WR�<HOORZVWRQH�ZLWK�VWXGHQWV�� DQG� D�1$6$�VSRQVRUHG� ��ZHHN� WULS� E\� ��ZKHHO�bus and plane to almost all volcanic and thermal spring sites LQ�,FHODQG��LQFOXGLQJ�DQ�LQWLPDWH�YLHZ�RI�0W�+HNOD�HUXSWLQJ��The participants included volcanologists, geochemists, and microbiologists. They also included Tom Brock, and two RI�P\� FXUUHQW� DQG� SDVW� 3K'� VWXGHQWV�� &RQUDG�:LFNVWURP�DQG�5LFKDUG�6KHULGDQ�� UHVSHFWLYHO\��0DQ\� FROOHFWLRQV� DQG�isolates were made, including some from the recently emer-JHQW�YROFDQLF�LVODQG�RI�6XUWVH\��2QH�RI�WKH�JUHDW�SOHDVXUHV�ZDV�EDWKLQJ�LQ�ZDUP�ZDWHU�LQ�RQH�RI�WKH�ODYD�¿VVXUHV�QHDU�0\YDWQ�

%\�������,�KDG�UHDFKHG�IXOO�SURIHVVRUVKLS�DQG�LQ������ZDV�DZDUGHG�D�*XJJHQKHLP�)HOORZVKLS� WKDW� ,�XVHG�GXULQJ�P\�second sabbatical, one that took me to the University of $XFNODQG�� 1HZ� =HDODQG�� ZLWK� 9DOHQWLQH� &KDSPDQ� DV� P\�KRVW��0\�IDPLO\�DQG�,�WRRN�WKH�VORZ�URXWH�WR�1HZ�=HDODQG��WUDYHOLQJ�E\� VKLS� �WKH�Orsova), and it enabled me to com-plete a research paper during the voyage. It was an especial-O\� HQMR\DEOH� WULS��)URP�$XFNODQG� ,� IUHTXHQWO\�YLVLWHG�� WKH�hot spring area of Rotorua, Waimangu, and elsewhere, and much research was accomplished, including the demonstra-WLRQ�LQ�WKH�¿HOG�RI�VXO¿GH�GHSHQGHQW�DQR[\JHQLF�SKRWRV\Q-thesis in a cyanobacterium, a process demonstrated about WKH�VDPH�WLPH�LQ�D�FXOWXUH�E\�<HKXGD�&RKHQ�LQ�,VUDHO��H�J��&DVWHQKRO]���������������,Q�UHVHDUFK�FRPSOHWHG�LQ�1RUZD\�GXULQJ�D�ODWHU�VDEEDWLFDO�LQ�����±������WKH�VDPH�F\DQREDF-WHULD�IURP�1HZ�=HDODQG�ZHUH�VKRZQ�LQ�FXOWXUH�WR�SKRWRV\Q-WKHVL]H�DQR[\JHQLFDOO\��H�J��&DVWHQKRO]�DQG�8WNLOHQ�������

�)LJXUH�����7KH� UHWXUQ� IURP�1HZ�=HDODQG� LQYROYHG�D� VWRS�LQ�1RUZD\��WKHQ�LQ�,FHODQG�ZKHUH�PRUH�FROOHFWLQJ�ZDV�GRQH��(YHQWXDOO\� ,�DUULYHG�DW� WKH�0DULQH�%LRORJLFDO�/DE��:RRGV�+ROH��0DVVDFKXVHWWV��ZKHUH�,�ZDV�RQH�RI�WKH�LQVWUXFWRUV�LQ�WKH�PLFURELDO�HFRORJ\�FRXUVH��IRXQGHG�WKDW�VXPPHU�E\�+RO-JHU�-DQQDVFK��,�OHDUQHG�PXFK�IURP�+ROJHU�DQG�5DOSK�:ROIH��QRW�OHDVW��KRZ�WR�VDLO��LQ�+ROJHU¶V�FDWERDW��8SRQ�UHWXUQLQJ�WR�(XJHQH��,�DQG�D�FRXSOH�RI�FROOHDJXHV�ERXJKW�D����IRRW�RSHQ�sailboat, and I have sailed ever since, in larger and larger ERDWV��FXUUHQWO\�D����IW�6HDZDUG��EXW�RQO\�D�IHZ�WLPHV�LQ�WKH�RSHQ�VHD��2Q�RQH�XQIRUWXQDWH���GD\�QLJKW�VDLOLQJ�IURP�2U-HJRQ�WR�9DQFRXYHU�,VODQG�WKH�RQO\�IRRG�WKH�WKUHH�RI�XV�KDG�ZDV�FKRFRODWH��FDQG\��SXGGLQJ��FDNH��HWF����7KH�UHDVRQ�IRU�this situation is too complex to explain.

7KH� ����V� FRQWLQXHG�ZLWK� UHVHDUFK� RQ� VXO¿GH�� EXW� RQH� RI�the main events was the discovery of &KORURÀH[XV and its FKDUFWHUL]DWLRQ�E\�3K'��VWXGHQW�%HY�3LHUVRQ�DQG�P\VHOI��H�J��3LHUVRQ�DQG�&DVWHQKRO]������������D������E���7KLV�RSHQHG�up an entirely new category of anoxygenic phototrophic EDFWHULD�WKDW�GLG�QRW�¿W�WKH�PROG�RI�DQ\�SUHYLRXVO\�GHVFULEHG�group. This eventually led to the discovery, mainly by other researchers, of other genera and species in this group that is now referred to as the phylum &KORURÀH[L��%RRQH�HW�DO���

Figure 5. Richard Castenholz, sampling on edge of 60°C, pH 3 Waimangu “Cauldron”, New Zealand, 1971.

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Richard W. Castenholz

The Bulletin of BISMiS

�������7KH� RUDQJH�FRORUHG� XQGHUPDW� LQ�PRVW� DONDOLQH� KRW�VSULQJV� �XS� WR�DERXW����&��ZHUH� WKRXJKW�SUHYLRXVO\� WR�EH�KHWHURWURSKLF�³ÀH[LEDFWHULD´��EXW�RQO\�ZKHQ�3LHUVRQ�UHFRUG-HG�DQ�DEVRUSWLRQ�VSHFWUXP�WKDW�ZHQW�ZHOO�RYHU�����QP�GLG�we discover that bacteriochlorophyll c��a����QP�PD[��DQG�bacteriochlorophyll a �����DQG�����QP�PD[��ZHUH�SUHVHQW�and also that photoheterotrophy was the principal mode of metabolism in &KORURÀH[XV.

2WKHU�ZRUN�GXULQJ� WKH�����V� LQFOXGHG�D�PRUH�GHWDLOHG�GH-VFULSWLRQ� RI� WKH� VSHFLHV� SDWWHUQ� LQ� +XQWHU¶V� +RW� 6SULQJV�along the thermal gradient, and the characterization of ther-mal ranges of an undescribed thermophilic ostracod, an ani-mal that established by grazing the lower border of Oscilla-toria and &KORURÀH[XV�DW�DERXW���±���&��ZKLFK�LV�DOVR�WKH�upper limit for this ostracod that forms dense populations below this temperature. The result was the establishment of ostracod-resistant/ostracod-dependent populations of two RWKHU� F\DQREDFWHULDO� VSHFLHV� EHORZ� ���&� �H�J��:LFNVWURP�DQG�&DVWHQKRO]��������������

,Q�����±���,�WRRN�D�WKLUG�VDEEDWLFDO��VXSSRUWHG�LQ�SDUW�E\�D�)XOEULJKW�DZDUG��DW�WKH�8QLYHUVLW\�RI�2VOR��%OLQGHUQ��KRVWHG�E\�-RKQ�2UPHURG��7KHUH�,�ZRUNHG�SULPDULO\�ZLWK�+DQV�8W-NLOHQ��D�3K'�VWXGHQW�RI�-RKQ¶V��RQ� WKH�XVH�RI�VXO¿GH�E\�D�VSHFLHV�RI�F\DQREDFWHULD�LVRODWHG�HDUOLHU�IURP�1HZ�=HDODQG��'XULQJ�WKH�VXPPHU�RI������,�WUDYHOOHG�WR�,VUDHO�IRU�UHVHDUFK�DQG�D�PHHWLQJ��DQG�LQ������DOVR�JDYH�WDONV�DW� WKH�'DKOHP�&RQIHUHQFH�LQ�%HUOLQ��DW�'XQGHH��:�'�3��6WHZDUW��KRVW���DQG�LQ�*|WWLQJHQ��1RUEHUW�3IHQQLJ��KRVW��

'XULQJ�WKH�HDUO\�����V�/DUU\�+DOIHQ�ZRUNHG�RQ�PRWLOLW\�DQG�its mechanism in the gliding cyanobacterium Oscillatoria princeps, and came to a description of the mechanism not far from a current theory as proposed by at least one other investigator, but differing greatly from a hypothesis of an-RWKHU�JURXS��H�J��+DOIHQ�DQG�&DVWHQKRO]��������&DVWHQKRO]��������

The 1980s

,Q� WKH� ����V� ,� EUDQFKHG� LQWR� D� EURDG� YDULHW\� RI� UHVHDUFK�subjects. These included a study of hypersaline cyanobac-WHULDO�PDWV� LQ� WKH� DUHD� RI�*XHUUHUR�1HJUR��0H[LFR� �-DYRU�DQG�&DVWHQKRO]��������D�GHPRQVWUDWLRQ�RI�WKH�GLHO�YHUWLFDO�migration of the cyanobacterium, Oscillatoria terebriformis, LQ� +XQWHU¶V� +RW� 6SULQJV� DQG� HOVHZKHUH� �H�J�� &DVWHQKRO]��������5LFKDUGVRQ�DQG�&DVWHQKRO]���������6WHSKHQ�*LRYDQ-QRQL��D�3K'�VWXGHQW�LQ�P\�ODE��ZRUNHG�RQ�D�YDULHW\�RI�SURM-HFWV�EHIRUH�KH�¿QLVKHG��*LRYDQQRQL�HW�DO�������E��3LHUVRQ�HW�DO����������EXW�IRFXVHG�RQ�Isosphaera pallida for his thesis. Isosphaera �ex Isocystis), a common inhabitant of moderate

WHPSHUDWXUHV�LQ�QXPHURXV�KRW�VSULQJV�LQ�1RUWK�$PHULFD�DQG�elsewhere, originally thought to be a cyanobacterium, was VKRZQ�E\�6WHSKHQ�WR�EH�DQ�DHURELF�KHWHURWURSK�RI�WKH�Planc-tomycetes with some unusual properties such as gas vesicles DQG�SKRWRWD[LV��H�J��*LRYDQQRQL�HW�DO�������D��

,�VSHQW�WKH�VXPPHUV�RI������DQG������WHDFKLQJ�LQ�WKH�0L-FURELDO�'LYHUVLW\� FRXUVH� DW�0%/��:RRGV�+ROH�� XQGHU� WKH�GLUHFWLRQ� RI� +DUODQ� +DOYRUVRQ�� ,W� ZDV� WKHUH�� ZRUNLQJ� RQ�SURMHFWV�ZLWK�7RP� 6FKPLGW� DQG�.HQ�1ROO� �VWXGHQWV� WKHQ��that I realized the importance for survival of light-regulated vertical migration of cyanobacteria in mats. This led to sev-HUDO�\HDUV�RI�UHVHDUFK�LQ�WKLV�¿HOG��,Q������DQG�DJDLQ�LQ������,�VSHQW�VHYHUDO�ZHHNV�DW�WKH�8QLYHUVLW\�RI�$DUKXV��'HQPDUN��ZLWK�1LHOV�3HWHU�5HYVEHFK�DQG�%R�-¡UJHQVHQ��¿UVW�WR�OHDUQ�KRZ�WR�PDNH�DQG�XVH�2� microelectrodes and then to look at vertical migrations of cyanobacteria in benthic mats in the /LPIMRUG��,Q���������\HDUV�DIWHU�P\�PDUULDJH�WR�3K\OOLV�/DU-VRQ��,�ZHQW�DJDLQ�WR�1HZ�=HDODQG�RQ�D�VDEEDWLFDO�OHDYH��WKLV�WLPH�WR�WKH�7DXSR�5HVHDUFK�/DE�DW�WKH�LQYLWDWLRQ�RI�:DUZLFN�9LQFHQW��3K\OOLV� DQG� ,� WUDYHOOHG�H[WHQVLYHO\��EXW�PDLQO\� WR�the Rotorua region. During this stay I studied the “behavior”, including vertical migration, of Oscillatoria cf. boryana in a VXO¿GH�ULFK�WHSLG�SRQG��7KH�UHVXOWV�OHG�WR�WKH�FRQFOXVLRQ�WKDW�VXO¿GH�GHSHQGHQW�DQR[\JHQLF�SKRWRV\QWKHVLV�WRRN�SODFH�LQ�the early hours of light, but was replaced by a shift to oxy-genic photosynthesis with increasing light intensity during WKH�GD\��&DVWHQKRO]�HW�DO���������

'XULQJ� WKH�1HZ�=HDODQG� VWD\� ,� DOVR� GLVFRYHUHG� D� VXO¿GH�rich warm stream that harbored a thick mat of thermophilic Chlorobium��L�H��D�SRSXODWLRQ�WKDW�RFFXUUHG�XS�WR����&��&DV-WHQKRO]�HW�DO����������7KLV�EDFWHULXP�ZDV� ODWHU� LVRODWHG�E\�0LNH�0DGLJDQ�DQG�GHVFULEHG�E\�:DKOXQG�HW�DO����������DQG�is now known as Chlorobaculum tepidum, a completely se-quenced, highly used model for the green sulfur bacteria.

,W�ZDV�LQ�������WKDW�%LOO�6FKRSI�FDPH�WR�(XJHQH�DQG�LQYLWHG�PH�WR�EHFRPH�D�PHPEHU�RI�WKH�3UHFDPEULDQ�3DOHRELRORJ\�5HVHDUFK�*URXS��335*���$V�D�FRQVHTXHQFH�,�ZDV� LQ�1HZ�=HDODQG�D�VHFRQG�WLPH�LQ������ZLWK�D�QXPEHU�RI�WKH�PHP-EHUV�RI�WKDW�JURXS��LQFOXGLQJ�'DYH�'HV�0DUDLV��%R�-¡UJHQVHQ��-RKQ�%DXOG��%RE�+RURG\VNL��DQG�'DYH�:DUG��$�ODUJH�FRP-SLODWLRQ�RI�ZRUN�GRQH�E\�PRVW�PHPEHUV�RI�WKH�335*�ZDV�SXEOLVKHG�DV�7KH�3URWHUR]RLF�%LRVSKHUH��D�0XOWLGLVFLSOLQDU\�6WXG\��6FKRSI�DQG�.OHLQ�������

,Q�2UHJRQ��3K'�VWXGHQW�'RXJ�1HOVRQ�ZRUNHG�RXW� WKH�KHW-erotrophic metabolism and behavior of Beggiatoa� LQ�+XQW-HU¶V� +RW� 6SULQJV� �1HOVRQ� DQG� &DVWHQKRO]�� ����D�� ����E���������DQG�3K'�VWXGHQW�7RLYR�.DOODV�GHWHUPLQHG�LQ�WKH�ODE�that thermophilic cyanobacteria of the genus Synechococ-

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My life as a microbiologist and naturalist

The Bulletin of BISMiS

cus�GLG�QRW�DWWDLQ�DQ�RSWLPXP�S+�IRU�JURZWK�EHORZ�DERXW����DOWKRXJK�VWUDLQV�RFFXUUHG�LQ�DQG�ZHUH�LVRODWHG�IURP�WKHU-PDO�ZDWHUV� DV� ORZ� DV� S+����� �H�J��.DOODV� DQG�&DVWHQKRO]��������� ,Q� DGGLWLRQ�� GXULQJ� WKH� ����V� 3K'� VWXGHQW�:DOWHU�'RGGV�FRPSOHWHG�D�VWXG\�RI�D�FROG�ZDWHU���±��&���QLWURJHQ�limited spring pool that maintained a large population of a huge colony, syctonemin-containing Nostoc that was shown to be dependent on a snail species that “cleaned” the colony surface by grazing on “epi-Nostoc´�GLDWRPV��H�J��'RGGV�DQG�&DVWHQKRO]��������

$W�WKH�HQG�RI�WKH�����V�:DUZLFN�9LQFHQW�LQYLWHG�PH�WR�MRLQ�KLP�IRU�D�VHDVRQ�LQ�$QWDUFWLFD������±������ZLWK� WKH�1HZ�=HDODQG�$QWDUFWLF�3URJUDP��7KXV�� LQ�'HFHPEHU� RI� ����� ,�DUULYHG�DW�6FRWW�%DVH�YLD�&KULVWFKXUFK��MXVW�LQ�WLPH�IRU�D�ULRW-RXV�DQG�UDWKHU�OHZG�1HZ�<HDU¶V�(YH�SDUW\��2Q�1HZ�<HDU¶V�GD\�GR]HQV�RI�QXGH�PDOH�DQG�IHPDOH�.LZLV�GXQNHG�WKURXJK�D�VHDO�KROH�LQWR�WKH�í��&�VHDZDWHU�DQG�VXUYLYHG��1R�SKRWRV�were allowed, but somehow a large number appeared in the 6FRWW�%DVH�EDU�WKH�QH[W�GD\��:H�ZHUH�D�SDUW\�RI�WKUHH��0DO-FROP�'RZQHV��:DUZLFN�� DQG�P\VHOI� �)LJXUH�����$IWHU�P\�survival training we helicoptered to Bratina Island on the HGJH�RI� WKH�5RVV� �0F0XUGR�� ,FH�6KHOI��:H�ZHUH�FDPSHG�WKHUH�IRU�PRVW�RI���ZHHNV��EXW�ZLWK�D���GD\�FROOHFWLQJ�DQG�UHVHDUFK�WULS�WR�&DSH�5R\GV��ZLWK�DFFHVV�WR�WKH�6KDFNOHWRQ�

hut) and later to the dry valleys, particularly the Taylor and 9LFWRULD�9DOOH\V��$W�%UDWLQD�ZH�PDSSHG�RXW�D�URXWH�RI�D�IHZ�hours over the melt ponds of the ablation moraine of the ice shelf, distinguishing each pond by chemical characteristics and type of cyanobacterial mat that dominated. We named WKH�SRQGV�DW�WKDW�WLPH��EXW�&DVWHQKRO]�3RQG�HYHQWXDOO\�EH-FDPH�VKRUWHQHG�WR�³&DVWHQ�3RQG´��,W�LVQ¶W�SHUPDQHQW��LQ�DQ\�case, since, as part of the ice shelf, it will eventually end XS�LQ�WKH�5RVV�6HD��ORQJ�DIWHU�P\�OLIH�VSDQ��1RW�RQO\�ZHUH�cultures established, but photosynthetic measurements and R[\JHQ�SUR¿OHV�ZHUH�PDGH� LQ�PDQ\�RI� WKH�PDWV� �H�J��9LQ-FHQW�HW�DO����������)RU�WKH�PDQ\�ZHHNV�RI�FDPSLQJ�LQ�6FRWW�3RODU�WHQWV�DW�%UDWLQD�,VODQG�ZH�ZHUH�LVVXHG�GRXEOH�VOHHSLQJ�bags, enormous coats and warm hats, all of which I found WRR�ZDUP�� ,�ZDV� RYHUKHDWHG� GXULQJ�PRVW� RI� WKH�$QWDUFWLF�DGYHQWXUH��)LJXUH����

'XULQJ�WKH�����V�,�KDG�EHFRPH�DQ�DVVRFLDWH�PHPEHU�RI�WKH�%HUJH\¶V�0DQXDO�7UXVW��DQG�LQ������WKH��UG�YROXPH�RI�WKH�Bergey’s Manual of Systematic Bacteriology was published and this volume covered the cyanobacteria for which my FRQWULEXWLRQ�ZDV�VXEVWDQWLDO��6WDOH\�HW�DO���������

The 1990s

,Q�WKH�HDUO\�����V�3K'�VWXGHQW�)HUUDQ�*DUFLD�3LFKHO�DQG�,�EHJDQ� D� ORQJ�WHUP�SURMHFW� RQ�89�SURWHFWLRQ� LQ� WKH� F\DQR-EDFWHULD��¿UVW�ZLWK�WKH�FKDUDFWHUL]DWLRQ�DQG�SURWHFWLYH�IXQF-tion of the extra-cellular sheath pigment scytonemin that DEVRUEV�PDLQO\�LQ�WKH�89$�DQG�89&�VSHFWUDO�UHJLRQV��H�J��*DUFLD�3LFKHO�DQG�&DVWHQKRO]��������*DUFLD�3LFKHO���������/DWHU�� DIWHU� WKH� VWUXFWXUH� RI� VF\WRQPHLQ� ZDV� GHWHUPLQHG��3URWHDX� HW� DO��� ������ZRUN� FRQWLQXHG�ZLWK� WKH� VRPHZKDW�dubious function of cytoplasmic mycosporine-like amino

Figure 6. Camp at Bratina Island, Antarctica, January 1990. From left to right: Malcolm Downes, Richard Cas-tenholz, and Warwick Vincent.

Figure 7. Richard Castenholz measuring O2�SURÀOH�LQ�cyanobacterial mat with microelectrode, Bratina Island, Antarctica, January 1990.

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157

Richard W. Castenholz

The Bulletin of BISMiS

DFLGV� �H�J��*DUFLD�3LFKHO� HW� DO��� ������ �)LJXUH� ����:H� DQG�others have shown the key role of scytonemin in increasing ¿WQHVV�XQGHU�FRQGLWLRQV�RI�KLJK�VRODU�LUUDGLDQFH��HVSHFLDOO\�KLJK�89� �H�J��&DVWHQKRO]�DQG�*DUFLD�3LFKHO���������������6HYHUDO�SDSHUV�IROORZHG��DQG�ODWHU�LQ�WKH�����V�WKH�UROH�RI�RWKHU�HQYLURQPHQWDO�IDFWRUV�EHVLGHV�89$�LQ�WKH�UHJXODWLRQ�of scytonemin synthesis in cyanobacteria were revealed E\�3K'�VWXGHQWV�-HVVH�'LOORQ�DQG�(ULFK�)OHPLQJ��H�J��'LO-ORQ� DQG�&DVWHQKRO]�� ������)OHPLQJ� DQG�&DVWHQKRO]�� �������������'XULQJ�WKH�ODWH�����V�3K'�VWXGHQWV�-HVVH�'LOORQ�DQG�6FRWW�0LOOHU�DQG�06�VWXGHQWV�6WHSKDQ�%UHQRZLW]�DQG�&KULV�Wingard conducted photosynthetic studies of cyanobacte-ULDO�PDWV� LQ�<HOORZVWRQH� LQ� UHVSRQVH� WR�89� UDGLDWLRQ� DQG�WKH�SUHVHQFH�RU�DEVHQFH�RI�VF\WRQHPLQ��H�J��%UHQRZLW]�DQG�&DVWHQKRO]��������'LOORQ�HW�DO���������

%HVLGHV� WKH� LQYHVWLJDWLRQ� RI� 89�SURWHFWLYH� FRPSRXQGV��ZRUN�LQ�WKH�ODWH�����V�VKRZHG�WKH�GHWULPHQWDO�HIIHFW�RI�89�radiation in the absence of protective shielding pigments. 6FRWW�0LOOHU� �3K'� VWXGHQW�� VKRZHG� WKLV� QHJDWLYH� HIIHFW� LQ�thermophilic Synechococcus�XQGHU�¿HOG�FRQGLWLRQV��0LOOHU�HW�DO����������DQG�&ODXGLD�.UXVFKHO��D�UHVHDUFKHU�IURP�*HU-PDQ\��DQG�)HUUDQ�*DUFLD�3LFKHO�VKRZHG�WKH�OHWKDO�RU�LQKLEL-WRU\�HIIHFW�RI�IXOO�OLJKW�DQG�89�RQ�¿ODPHQWRXV�F\DQREDFWHULD�that failed to escape by downward migration the high day-time solar radiation in soft microbial mats of hypersaline ZDWHUV�QHDU�*XHUUHUR�1HJUR��0H[LFR� �*DUFLD�3LFKHO� HW� DO���������.UXVFKHO�DQG�&DVWHQKRO]���������/DWHU��WKLV�EHQH¿FLDO�downward migration was also demonstrated in soft mats of

D�FROG�VDOLQH�SRQG�LQ�$QWDUFWLFD�LQ�������EXW�PRYHPHQW�ZDV�DW�D�PXFK�VORZHU�UDWH��H�J��1DGHDX�HW�DO���������

,Q������,�DWWHQGHG�P\�¿UVW�%HUJH\¶V�0DQXDO�7UXVW�PHHWLQJ�LQ�3UDJXH�DV�D� IXOO�PHPEHU�� ,� UHPDLQHG�D� IXOO�PHPEHU�XQ-WLO� WKH�FRPSXOVRU\�UHWLUHPHQW�DJH�RI����LQ�������+RZHYHU��LQ�WKDW�\HDU�WKH�¿UVW�YROXPH�RI�WKH��QG�HGLWLRQ�RI�Bergey’s Manual of Systematic Bacteriology was published, in which again I contributed a large portion the cyanobacterial sec-WLRQ�DORQJ�ZLWK�VHYHUDO�FROOHDJXHV��0XFK�RI�LW�ZDV�ZULWWHQ�RU�HGLWHG�GXULQJ�P\���PRQWK�VWD\�DW�WKH�,QVWLWXW�3DVWHXU�LQ�ODWH������DQG�HDUO\������ZLWK�5RVL�5LSSND�DQG�0LNH�+HUG-PDQ��%RRQH�HW�DO����������,Q������,�ZDV�DZDUGHG�WKH�%HUJH\�0HGDO�IRU�'LVWLQJXLVKHG�$FKLHYHPHQW�LQ�%DFWHULDO�7D[RQR-P\��)LJXUH����

$V� D� UHVXOW� RI� DQRWKHU� LQYLWDWLRQ� ,� UHWXUQHG� WR�$QWDUFWLFD��6FRWW�%DVH��DQG�%UDWLQD�,VODQG�LQ�WKH�����±�����VHDVRQ��$W�WKLV�WLPH�&OLYH�+RZDUG�:LOOLDPV�ZDV�P\�KRVW��DJDLQ�ZLWK�WKH�1HZ�=HDODQG�SURJUDP��7KH�RUJDQL]DWLRQ�ZDV�DOVR�DEOH�WR�VXSSRUW�WKH�WULS�RI�P\�3K'�VWXGHQW��7UDFLH�/\QQ�1DGHDX��DV�DQ�DVVLVWDQW��$JDLQ��ZH�FDPSHG�DW�%UDWLQD�,VODQG�LQ�WHQWV��EXW�with the addition of a closed outhouse, since a female was FDPSLQJ�WKHUH�IRU�WKH�¿UVW�WLPH��7KH�UHVXOWV�RI�WKLV�UHVHDUFK�trip was the demonstration, as mentioned above, of vertical migration of Oscillatoria� LQ�6DOW�3RQG� �5RVV� ,FH�6KHOI��� D�FDVH�ZKHUH�RQO\�WKH�ORZHVW�OLJKW�RU�DUWL¿FLDO�GDUNQHVV�ZRXOG�EULQJ�WKLV�VXEVXUIDFH�SRSXODWLRQ�WR�WKH�VXUIDFH��1DGHDX�HW�DO����������7KH�UDWHV�RI�SKRWRV\QWKHVLV�ZLWK�UHVSHFW�WR�WHP-SHUDWXUH�DQG�LQKLELWRU\�89�UDGLDWLRQ�ZHUH�DOVR�PHDVXUHG�LQ�WKH�¿HOG�DQG�ODWHU�DV�FXOWXUHV�LQ�WKH�ODE��1DGHDX�DQG�&DVWHQ-KRO]���������2QH�RI�WKH�VXUSULVHV�ZDV�WKDW�DOPRVW�DOO�VWUDLQV�of cyanobacteria from the ponds photosynthesized and grew DW�PD[LPDO�UDWHV�DW����&�RU�KLJKHU�LQ�WKH�¿HOG�DQG�FXOWXUH�and all very poorly at temperatures normally encountered in QDWXUH��L�H����&�WR�UDUHO\���&���,W�ZDV�YHU\�GLI¿FXOW�WR�NHHS�WKH�EDWKV�KHDWHG� LQ� WKH�¿HOG�H[SHULPHQWV��ZDWHU�KDG� WR�EH�boiled continuously in the cooking hut before running out and pouring it into the outdoor water baths. The cultures VWLOO� UHPDLQ� DW� ���&�DQG�DW�í���&� LQ� WKH�&&0((�FXOWXUH�FROOHFWLRQ�DW�2UHJRQ�

0\� FXOWXUH� FROOHFWLRQ� RI� F\DQREDFWHULD� DQG� PLFUR�DOJDH�had been established over many years from many locations and habitats, including a large number of isolates from hot springs over much of the globe, from hypersaline waters, HQGROLWKLF� KDELWDWV� DQG� IURP�$QWDUFWLF� IUHVK�ZDWHUV��:LWK�the addition of the collection of extreme habitat phototrophs IURP�(��,PUH�)ULHGPDQQ�LQ������RYHU������VWUDLQV�DUH�QRZ�EHLQJ�PDLQWDLQHG� LQ� WKH� ODE�� >7KH�82�&XOWXUH�&ROOHFWLRQ�RI�0LFURRUJDQLVPV�IURP�([WUHPH�(QYLURQPHQWV��&&0((���KWWS���FXOWXUHV�XRUHJRQ�HGX�@

Figure 8. Richard Castenholz lifting scytonemin-rich Lyngbya�PDW�IURP�LQWHUWLGDO�PXG�ÁDW��/DJXQD�*XHUUHUR�Negro, Baja California Sur, Mexico, in the 1990s.

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158

My life as a microbiologist and naturalist

The Bulletin of BISMiS

,Q�WKH�����V�DQG�����V�,�DOVR�EHFDPH�LQYROYHG�LQ�WKH�FRQWUR-versy on what constitutes a species in the cyanobacteria, and KRZ�VKRXOG�WKH\�EH�QDPHG��L�H��E\�WKH�,QWHUQDWLRQDO�&RGH�RI�%RWDQLFDO� 1RPHQFODWXUH� RU� WKH� ,QWHUQDWLRQDO� &RGH� RI� 1R-menclature of Bacteria). I do not wish to go into this now. I realize I am in disagreement with many others, including $DURQ�2UHQ�DQG�-LUL�.RPiUHN��,Q�VKRUW��,�ZLOO�EH�KDSS\�IRU�some years to come with simply giving numbers to species RU�VWUDLQV�RI�F\DQREDFWHULD��H�J��Synechocystis�3&&��������EXW� XVLQJ� PRUSKRORJLFDOO\� GH¿QHG� QDPHV� RI� JHQHUD� �H�J��&DVWHQKRO]�DQG�1RUULV��������

The 2000s

,Q� WKH�VXPPHU�RI������,�ZDV�DSSRLQWHG� WKH�¿UVW�³9LVLWLQJ�6FKRODU´�RI� WKH�7KHUPDO�%LRORJ\� ,QVWLWXWH��0RQWDQD�6WDWH�University, Bozeman. During that time I gave a series of ten lectures on hot spring biology and the history of micro-ELDO�UHVHDUFK�LQ�<HOORZVWRQH��,Q�DGGLWLRQ��DV�ZDV�H[SHFWHG��,�FRQGXFWHG�UHVHDUFK��PDLQO\�ZLWK�D�SRVW�GRF�RI�7LP�0F'HU-PRWW¶V��7UDF\�1RUULV��,W�ZDV�D�ORQJ�WHUP�SURMHFW�WKDW�VKRZHG�WKDW�F\DQREDFWHULDO�PDWV�LQ�WKH���±���&�UDQJH�WKDW�ZHUH�VHY-HUDO�ZHHNV�RU�PRQWKV�XQGHU�89�VKLHOGLQJ�¿OWHUV�GLG�QRW�VH-OHFW�IRU�RSSRUWXQLVWLF�89�VHQVLWLYH�F\DQREDFWHULD��DOWKRXJK�this result may have been a consequence of the lack of in-oculum of novel thermophilic species in the environment. 3&5�DQG�GHQDWXULQJ�JUDGLHQW� JHO� HOHFWURSKRUHVLV� �'**(��

was used to be nearly certain of the absence of new species RU�VWUDLQV��XVLQJ���6�U'1$�VHTXHQFHV��1RUULV�HW�DO����������,�ZRUNHG�RXW�RI�%R]HPDQ�DJDLQ�LQ�WKH�VXPPHU�RI������LQ�D�follow-up to this project and the initiation of another project on acidophilic algae.

,Q�������7UDF\�1RUULV��KDYLQJ�¿QLVKHG�KHU�SRVW�GRF�DW�0RQ-WDQD� 6WDWH�� FDPH� WR�(XJHQH� WR� WHDFK� LQ�PLFURELRORJ\� DQG�EHJLQ�D�SRVW�GRF�XQGHU�P\�GLUHFWLRQ�DV�DQ�15&�$VVRFLDWH��+HU� FKRLFH�RI� UHVHDUFK�ZDV�RQH� LQ�ZKLFK� ,� KDG� DQ� HDUOLHU�LQWHUHVW��L�H��RI�SKRWRWURSKV�LQ�WKH�ROG�WUDYHUWLQH��OLPHVWRQH��VSULQJ� GHSRVLWV� RI� WKH�0DPPRWK� WHUUDFHV� LQ�<HOORZVWRQH�DQG� DFURVV� WKH� <HOORZVWRQH� 5LYHU� DERYH� *DUGLQHU�� 0RQ-WDQD��6RPH�GHSRVLWV�ZHUH� IURP�D� IHZ� WKRXVDQG� WR� VHYHUDO�KXQGUHG�WKRXVDQG�\HDUV�DJR��7HUUDFH�0RXQWDLQ���0RVW�VLWHV�had bands of endolithic cyanobacteria and microalgae one to a few mm below the rock surface, a habitat well-known LQ� VDQGVWRQHV� LQ� WKH�GU\�YDOOH\V�RI�$QWDUFWLFD� DQG� VHYHUDO�RWKHU� VXEVWUDWHV� LQ� YDULRXV� JOREDO� ORFDWLRQV��$� ODUJH� QXP-ber of these endolithic phototrophs were isolated and cul-WXUHG��1RQH� IURP� WKH� DQFLHQW� WHUUDFHV�ZHUH� VLPLODU� �XVLQJ���6�U'1$�VHTXHQFHV��WR�WKH�F\DQREDFWHULD�LQ�WKH�DFWLYH�KRW�VSULQJV� �1RUULV� DQG� &DVWHQKRO]�� ������� 7KHVH� HQGROLWKLF�phototrophs resulted from secondary inoculation and inva-sion, and were shown to be highly tolerant of desiccation

Figure 9.�3DUWLFLSDQWV�DQG�VSRXVHV�DW�%HUJH\·V�0DQXDO�7UXVW�PHHWLQJ�RQ�D�ÀHOG�WULS�DW�2FWRSXV�6SULQJ��<HOORZVWRQH�National Park, 1995. Standing (left–right): Rita Colwell, Joseph Tully, Karl Schleifer, Jan Ursing, Brita Ursing, Noel Krieg, John Holt, Joan Sneath, Marion Murray, Peter Sneath, Gerti Schleifer, Sonja Staley, and Jim Staley; kneeling (left–right): Stan Williams, Robert Murray, Elaine Krichevsky, Micah Krichevsky, and Richard Castenholz. David Boone took the photo.

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159

Richard W. Castenholz

The Bulletin of BISMiS

DQG�IUHH]LQJ��ERWK�FRQGLWLRQV�SUHYDOHQW�LQ�<HOORZVWRQH��(P-LO\�.QRZOHV��06�VWXGHQW��VKRZHG�WKDW� WKH�SUHVHQFH�RI�H[-tracellular polysaccharides from endolithic cyanobacteria could enhance the desiccation tolerance of other endolithic SKRWRWURSKV�WKDW�ODFNHG�(36��,W�ZDV�REYLRXV��DQG�ODWHU�FRQ-¿UPHG�E\�RWKHUV��WKDW�WKH�HQGROLWKLF�QLFKH�SURYLGHV�SURWHF-WLRQ�IURP�KLJK�OLJKW�LQWHQVLW\��DQG�89�UDGLDWLRQ���SURWHFWLRQ�from grazing and wind abrasion, but it is likely that growth LV�YHU\�VORZ�LQ�WKLV�FRQ¿QHG�HQYLURQPHQW�HYHQ�ZKHQ�PRLVW�DQG�ZLWK�SUREDEOH�QXWULHQW�OLPLWDWLRQ��)LJXUHV����DQG�����

,Q� WKH� VXPPHU� RI� ����� 7UDF\� 1RUULV� DQG� ,� EHJDQ� WR� LVR-ODWH� DQG� FXOWXUH� ³F\DQLGLD´� �D� JHQHUDO� WHUP� IRU� WKH� WKUHH�described genera of the rhodophytan order, Cyanidiales), namely Cyanidium, Galdieria, and Cyanidioschyzon. These unicellular algae are known to occur only in acid waters �S+��±���DQG�XVXDOO\�DW� WHPSHUDWXUHV� IURP�DERXW����&� WR����&��7KH\� FRQVWLWXWH� WKH� RQO\� NQRZ�SKRWRWURSKV� LQ� VXFK�conditions. Their physiology, ecology, and biogeography constitute the subject of most of my current research. Dur-ing this decade cultures of “cyanidia” were isolated from PDQ\�VLWHV�LQ�-DSDQ���������1HZ�=HDODQG�������DQG�������DQG� ,FHODQG� ������� DQG� PDQ\� VWUDLQV� IURP� <HOORZVWRQH�acidic environments that include streams, acidic thermal VRLOV�� ULPV� RI� VWHDP� YHQWV� �IXPDUROHV��� DQG� QDUURZ� EDQGV�LQ�PRLVW�VLOLFHRXV�URFNV�LQ�DFLGLF�DUHDV��L�H��HQGROLWKV���7KH�UHVXOWV�DPDVVHG�E\�06�VWXGHQW�-XOLH�7RSOLQ�VKRZHG��XVLQJ�WKH�QXFOHDU���6�U'1$�DQG� WKH�FKORURSODVWLF� UEF/�JHQH�VH-quences, that only two genotypes of cyanidia occurred in WKH�<HOORZVWRQH�FROOHFWLRQV��RQH�FORVH�WR�Galdieria sulphu-raria and the most abundant strain nearly identical to Cy-anidioschyzon merolae.�+RZHYHU��LW�ZDV�DSSDUHQW�WKDW�WKLV�

most abundant type had no morphological resemblance to Cyanidioschyzon merolae��7RSOLQ�HW�DO����������/DWHU�SKHQR-typic and genetic evidence suggested that the abundant type IURP�<HOORZVWRQH�VKRXOG�SUREDEO\�EH�UHIHUUHG�WR�D�QHZ�VSH-cies of the genus Galdieria�ZLWK�PDQ\�³HFRW\SHV´��$PRQJ�several strains differences have been shown in tolerance to DUVHQLWH��$V�,,,���DUVHQDWH��$V�9���DOXPLQLXP��PHUFXU\��DQG�other potentially toxic substances common in some of the QDWXUDO�DFLGLF�HQYLURQPHQWV�RI�<HOORZVWRQH��7KLV�ZRUN�LV�LQ�SURJUHVV�ZLWK�06�VWXGHQWV�&KULVWLH�/RZHOO�DQG�&KHOVH\�,LGD��+RZHYHU��WKH�JHQH�VHTXHQFHV�RI���6�U'1$�DQG�rbcL were VXI¿FLHQWO\�GLIIHUHQW�WR�GLVWLQJXLVK�PDQ\�RI�WKH�VWUDLQV�IURP�-DSDQ��1HZ�=HDODQG��3KLOLSSLQHV��DQG�,FHODQG�IURP�WKRVH�RI�<HOORZVWRQH�DQG�IURP�HDFK�RWKHU��7RSOLQ�HW�DO���������&DV-WHQKRO]�DQG�0F'HUPRWW���������2WKHU�ZRUN�LQ�FROODERUDWLRQ�ZLWK�7LP�0F'HUPRWW��3URIHVVRU��0RQWDQD�6WDWH�8QLYHUVLW\���&RULQQH�/HKU��IRUPHU�0RQWDQD�6WDWH�8QLYHUVLW\�SRVW�GRF���DQG� 'DQD� 6NRUXSD� �3K'�� 0RQWDQD� 6WDWH� 8QLYHUVLW\�� KDV�VKRZQ� WKDW�89�UDGLDWLRQ� LV�SUREDEO\�DQ�HFRW\SH�GHWHUPLQ-ing environmental factor, and that during summer daytime SHULRGV��89�UDGLDWLRQ�KDV�DQ�LQKLELWRU\�HIIHFW�RQ�SKRWRV\Q-WKHVLV��/HKU�HW�DO���������

Epilogue

2QH�RI�WKH�PDLQ�UHVHDUFK�TXHVWLRQV�,�KDYH�DVNHG�WKURXJKRXW�P\�FDUHHU�LV��KRZ�GR�YDULRXV�PLFUR�RUJDQLVPV�WROHUDWH�DQG�adapt to environmental extremes? These extremes include KLJK�DQG�ORZ�WHPSHUDWXUH��ORZ�S+��KLJK�VDOLQLW\�DQG�GHVLF-FDWLRQ��IUHH]LQJ��KLJK�VRODU�LUUDGLDQFH��HVSHFLDOO\�89���WR[LF�

Figure 10. Richard Castenholz at Nakabusa Hot Springs, Japan, in 2003 at the site where Satoshi Hanada iso-lated anoxygenic 5RVHLÁH[XV�FDVWHQKRO]LL, a new genus and species of the &KORURÁH[L.

Figure 11. Former PhD students of Richard Castenholz at meeting of Phototrophic Prokaryotes, Pau, France, 2006. From left to right: Erich Fleming, Ferran Garcia-Pichel, Jack Meeks, Richard Castenholz, Bev Pierson, and Toivo Kallas.

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OHYHOV�RI�VXO¿GH�DQG�RWKHU�SRWHQWLDOO\�SRLVRQRXV�FRPSRXQGV��$QRWKHU� LQWHUHVW� WKURXJKRXW�P\� VWXGLHV�ZDV� WKH� GHJUHH� WR�which endemism occurs among hot spring micro-organisms. The subject of endemism in microbial distributions has been somewhat controversial for many years, but recently many SRVLWLYH�H[DPSOHV�KDYH�EHHQ�SXW�IRUZDUG��6LQFH�KRW�VSULQJ�FOXVWHUV��HVSHFLDOO\�WKHUPDO�DFLGLF�FOXVWHUV��DSSHDU�LQ�PDQ\�ways as islands often separated by large regional or conti-nental distances it should be expected that geographic en-demism should appear in these habitats, if anywhere, espe-FLDOO\�VLQFH�GLI¿FXOWLHV�LQ�ORQJ�GLVWDQFH�GLVVHPLQDWLRQ�H[LVW�for many of these thermophiles. It has now been shown by others and by results of some of my work that endemism exists among thermophiles, at least at continental distances �H�J��&DVWHQKRO]��������0LOOHU�HW�DO���������:DUG�DQG�&DVWHQ-KRO]��������:DUG�HW�DO���������7RSOLQ�HW�DO����������)LJXUHV������������DQG�����

,Q�-DQXDU\������,�UHFHLYHG�DQ�DZDUG�SUHVHQWHG�DW�WKH�16)�5&1�7%,� FRQIHUHQFH�� DW� 0DPPRWK� +RW� 6SULQJV�� <HOORZ-VWRQH�1DWLRQDO�3DUN��³LQ�DSSUHFLDWLRQ�IRU�VHPLQDO�FRQWULEX-WLRQV�WR�UHVHDUFK�LQ�WKH�JHRWKHUPDO�V\VWHPV�RI�<HOORZVWRQH�1DWLRQDO�3DUN´��/DWHU�LQ������,�UHFHLYHG�WKH�$PHULFDQ�6R-FLHW\� IRU�0LFURELRORJ\�86)&&�-��5RJHU�3RUWHU�$ZDUG� IRU�VWXGLHV�RI�PLFURELDO�GLYHUVLW\�� ,Q������ ,�ZDV�HOHFWHG�D� IHO-ORZ�RI�WKH�$PHULFDQ�$FDGHP\�RI�0LFURELRORJ\��DQG�LQ�WKH�����V� ,�EHFDPH�D�)HOORZ�RI� WKH�$PHULFDQ�$VVRFLDWLRQ� IRU�WKH�$GYDQFHPHQW�RI�6FLHQFH��$$$6��

'XULQJ�P\� FDUHHU�� HQWLUHO\� DW� WKH�8QLYHUVLW\� RI�2UHJRQ�� ,�have taught several subjects, including microbiology, fresh-water biology, plant morphology and portions of general and FRUH�ELRORJ\��*UDGXDWH�VHQLRU� OHYHO� FRXUVHV�KDYH� LQFOXGHG�SK\FRORJ\��SKRWRV\QWKHWLF�SURNDU\RWHV��ZLWK�%LOO�6LVWURP���life in extreme environments, and freshwater ecology. The

last-named course has been offered in most alternate years VLQFH�WKH�����V�DQG�KDV�DOZD\V�EHHQ�P\�IDYRULWH��,Q�VSULQJ������,�KDG�RQH�RI�WKH�EHVW�SUHSDUHG��LQWHUHVWHG��DQG�FRQJH-QLDO�JURXSV�RI����VWXGHQWV�WKDW�,�FDQ�UHPHPEHU��7KH�6DWXU-GD\�¿HOG�WULSV�LQ�ZKLFK�WKH�ZKROH�FODVV�LV�ODXQFKHG�LQ�UDIWV�or boats have sampled physical, chemical, and biological IHDWXUHV�RI�IUHVKZDWHU�FRDVWDO�ODNHV��D�VWUDWL¿HG�PHVRWURSKLF�lake, an alpine oligotrophic lake, a naturally hyper-eutro-phic lake, a saline soda lake, a perennial cold spring pond, and an alkaline hot spring, the last four locations as part RI�DQ�RYHUQLJKW�FDPSLQJ� WULS� WR�HDVWHUQ�2UHJRQ��$OWKRXJK�emphasis these days is on molecular biology, exposure to natural habitats and their organisms is still appreciated by many students.

During all of these years I have been proud to be part of WKH�%LRORJ\�'HSDUWPHQW�DW�WKH�8QLYHUVLW\�RI�2UHJRQ�DQG�WKH�PRUH� UHFHQWO\� IRUPHG� ,QVWLWXWH� RI� (FRORJ\� DQG� (YROXWLRQ�DV�ZHOO��$OO�PHPEHUV�RI�WKH�IDFXOW\��LQFOXGLQJ�WKRVH�,�FRP-PRQO\� LQWHUDFWHG�ZLWK�� IRU� RYHU� ��� \HDUV� KDYH� EHHQ� KHOS-ful and congenial, a comment that few faculty members of any institution can make. I have had especially productive DQG�HQMR\DEOH�FROODERUDWLRQV�ZLWK�0LFKHOOH�:RRG�DQG� WKH�ODWH�%LOO�6LVWURP�� ,�KDYH�PHQWRUHG����3K'�VWXGHQWV��PRVW�of whom have tenured academic positions, although a few are retired or deceased. They have been friends as well as VWXGHQWV��7KHUH�KDYH�DOVR�EHHQ�PDQ\�06�VWXGHQWV�� WZR�RI�whom are still active in my lab.

,�ZLVK�WR�WKDQN�WKH�16)�IRU�DOPRVW�FRQWLQXRXV�VXSSRUW�DQG�DOVR�� IRU� D� SRUWLRQ� RI�P\� FDUHHU�� WKH�1$6$�$VWURELRORJ\�3URJUDP�

Figure 12. Richard Castenholz at Octopus Spring, Yel-lowstone National Park, July 2008.

Figure 13. Richard Castenholz’s Freshwater Ecology class at Hunter’s Hot Springs, Oregon, in May 2008, plus Professor Brendan Bohannan center in back.

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References

%RRQH��'�5���5�:��&DVWHQKRO]�DQG�*�0��*DUULW\� �HGLWRUV���������%HUJH\¶V�0DQXDO�RI�6\VWHPDWLF�%DFWHULRORJ\���QG�HGQ��YRO�����7KH�Archaea and the Deeply Branching and 3KRWRWURSKLF�Bacteria��6SULQJHU��1HZ�<RUN�

%UHQRZLW]��6��DQG�5�:��&DVWHQKRO]��5�:��������/RQJ�WHUP�HIIHFWV� RI�89� DQG� YLVLEOH� LUUDGLDQFH� RQ� QDWXUDO� SRSXOD-WLRQV�RI�D�VF\WRQHPLQ�FRQWDLQLQJ�F\DQREDFWHULXP��Calo-thrix�VS����)(06�0LFURELRO��(FRO��24:���������

&DVWHQKRO]�� 5�:�� ������ 6HDVRQDO� FKDQJHV� LQ� WKH� DWWDFKHG�DOJDH�RI�IUHVKZDWHU�DQG�VDOLQH�ODNHV�LQ�WKH�/RZHU�*UDQG�&RXOHH��:DVKLQJWRQ��/LPQRO��2FHDQRJU��5:��±���

&DVWHQKRO]��5�:��������7KH�HIIHFW�RI�JUD]LQJ�RQ�PDULQH�OLW-WRUDO�GLDWRP�SRSXODWLRQV��(FRORJ\�42:����±����

&DVWHQKRO]��5�:��������6HDVRQDO�HFRORJ\�RI�QRQ�SODQNWRQLF�PDULQH�GLDWRPV�RQ�WKH�ZHVWHUQ�FRDVW�RI�1RUZD\��6DUVLD�29:����±����

&DVWHQKRO]�� 5�:�� ������ 7KH� EHKDYLRU� RI�Oscillatoria ter-ebriformis�LQ�KRW�VSULQJV��-��3K\FRO��4:���±����

&DVWHQKRO]�� 5�:�� ������7KH� WKHUPRSKLOLF� F\DQRSK\WHV� RI�

,FHODQG� DQG� WKH� XSSHU� WHPSHUDWXUH� OLPLW�� -�� 3K\FRO�� 5: ���±����

&DVWHQKRO]��5�:��������7KHUPRSKLOLF�EOXH�JUHHQ�DOJDH�DQG�the thermal environment. Bacteriol. Rev. 33:����±����

&DVWHQKRO]�� 5�:�� ������7KH� HIIHFW� RI� VXO¿GH� RQ� WKH� EOXH�JUHHQ�DOJDH�RI�KRW�VSULQJV��,��1HZ�=HDODQG�DQG�,FHODQG��-��3K\FRO��12:���±���

&DVWHQKRO]��5�:��������7KH�ELRJHRJUDSK\�RI�KRW�VSULQJ�DO-JDH� WKURXJK�HQULFKPHQW�FXOWXUHV��0LWW�� ,QW��9HUHLQ��/LP-nol. 21:����±����

&DVWHQKRO]��5�:�� ������0RWLOLW\� DQG� WD[HV� RI� F\DQREDFWH-ria. In�7KH�%LRORJ\�RI�&\DQREDFWHULD��HGLWHG�E\�&DUU�DQG�:KLWWRQ���%ODFNZHOO��2[IRUG��SS�����±����

&DVWHQKRO]�� 5�:�� ������ (QGHPLVP� DQG� ELRGLYHUVLW\� RI�WKHUPRSKLOLF� F\DQREDFWHULD�� 1RYD�+HGZLJLD� %HLK� 112: ��±���

&DVWHQKRO]�� 5�:�� DQG� +�&�� 8WNLOHQ�� ������ 3K\VLRORJ\� RI�VXO¿GH�WROHUDQFH�LQ�D�WKHUPRSKLOLF�F\DQREDFWHULXP��$UFK��0LFURELRO��138:����±����

&DVWHQKRO]��5�:�� DQG�7�%��1RUULV�� ������5HYLVLRQDU\� FRQ-cepts of species in the cyanobacteria and their applica-WLRQV��$OJRO��6WXG��117:���±���

&DVWHQKRO]��5�:��DQG�7�5��0F'HUPRWW��������7KH�&\DQLGL-DOHV�� HFRORJ\�� ELRGLYHUVLW\�� DQG� ELRJHRJUDSK\�� In Red $OJDH� LQ� WKH�*HQRPLF�$JH��&HOOXODU�2ULJLQ��/LIH� LQ�([-WUHPH�+DELWDWV�DQG�$VWURELRORJ\��HGLWHG�E\�6HFNEDFK�DQG�&KDSPDQ���6SULQJHU��1HZ�<RUN��SS�����±����

&DVWHQKRO]��5�:���-��%DXOG�DQG�%�%��-¡UJHQVHQ��������$QR[-\JHQLF�PLFURELDO�PDWV�RI�KRW�VSULQJV��WKHUPRSKLOLF�Chlo-robium�VS��)(06�0LFURELRO��(FRO��74:����±����

&DVWHQKRO]�� 5�:��� %�%�� -¡UJHQVHQ�� (�� '¶$PHOLR� DQG� -��%DXOG�� ������ 3KRWRV\QWKHWLF� DQG� EHKDYLRUDO� YHUVDWLOLW\�of the cyanobacterium Oscillatoria boryana��LQ�D�VXO¿GH�

Figure 14. Richard Castenholz at Norris Geyser Basin, Yellowstone National Park, in July 2010 with students, left to right: Tyler Roberts, Ashley Pacelli, and Christie Lowell.

Figure 15. Richard Castenholz at Mushroom Spring, Yel-lowstone National Park in September 2011.

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tosynthetic activity in modern microbial mat-building communities. In�7KH�3URWHUR]RLF�%LRVSKHUH��D�0XOWLGLV-FLSOLQDU\�6WXG\��HGLWHG�E\�6FKRSI�DQG�.OHLQ���&DPEULGJH�8QLYHUVLW\�3UHVV��1HZ�<RUN��SS�����±����

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'RGGV��:�.��DQG�5�:��&DVWHQKRO]��������7KH�HIIHFW�RI�JUD]-ing and light on the growth of Nostoc pruniforme��F\DQR-EDFWHULD���%ULW��3K\FRO��-��23:����±����

)OHPLQJ��(�'��DQG�5�:��&DVWHQKRO]��������(IIHFWV�RI�QLWUR-JHQ� VRXUFH� RQ� WKH� V\QWKHVLV� RI� WKH� 89�VFUHHQLQJ� FRP-pound, scytonemin, in the cyanobacterium Nostoc punc-tiforme 3&&��������)(06�0LFURELRO��(FRO��63:����±����

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*DUFLD�3LFKHO��)��DQG�5�:��&DVWHQKRO]��������&KDUDFWHUL]D-tion and biological implications of scytonemin, a cyano-EDFWHULDO�VKHDWK�SLJPHQW��-��3K\FRO� 27:����±����

*DUFLD�3LFKHO��)���1��6KHUU\�DQG�5�:��&DVWHQKRO]��������(Y-idence for an ultraviolet sunscreen role of the extracellu-lar pigment scytonemin in the terrestrial cyanobacterium, Chlorogloeopsis�VS��3KRWRFKHP��3KRWRELRO��56:���±���

*DUFLD�3LFKHO��)���&�(��:LQJDUG�DQG�5�:��&DVWHQKRO]��������(YLGHQFH�UHJDUGLQJ�WKH�89�VXQVFUHHQ�UROH�RI�D�P\FRVSR-rine-like compound in the cyanobacterium Gloeocapsa VS��$SSO��(QYLURQ��0LFURELRO��59:����±����

*DUFLD�3LFKHO��)���0��0HFKOLQJ�DQG�5�:��&DVWHQKRO]��������Diel migrations of microorganisms within a benthic, hy-SHUVDOLQH�PDW�FRPPXQLW\��$SSO��(QYLURQ��0LFURELRO��60: ����±�����

*LRYDQQRQL��6�-���(��6FKDEWDFK�DQG�5�:��&DVWHQKRO]������D��

Isosphaera pallida, gen. and comb. nov., a gliding, bud-GLQJ�HXEDFWHULXP�IURP�KRW�VSULQJV��$UFK��0LFURELRO��147: ���±����

*LRYDQQRQL��6�-���1�3��5HYVEHFK��'�0��:DUG�DQG�5�:��&DV-WHQKRO]�� ����E�� 2EOLJDWHO\� SKRWRWURSKLF� &KORURÀH[XV��SULPDU\� SURGXFWLRQ� LQ� DQDHURELF� KRW� VSULQJ�PDWV��$UFK��0LFURELRO��147:���±���

+DOIHQ��/�1��DQG�5�:��&DVWHQKRO]��������*OLGLQJ�PRWLOLW\�in the blue-green algae, Oscillatoria princeps��-��3K\FRO��7:����±����

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-¡UJHQVHQ��%�%���5�:��&DVWHQKRO]�DQG�%�.��3LHUVRQ��������The microenvironment within modern microbial mats. In�7KH�3URWHUR]RLF�%LRVSKHUH��D�0XOWLGLVFLSOLQDU\�6WXG\��HGLWHG� E\� 6FKRSI� DQG� .OHLQ��� &DPEULGJH� 8QLYHUVLW\�3UHVV��1HZ�<RUN��SS�����±����

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165© BISMiS 2011

Contact detailsInfectious Diseases Section (111 F), VA Medical Center West Los Angeles, Los Angeles, CA 90073, USA.

VLGÀQHJROG#JPDLO�FRP

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 165–180

Sydney M. Finegold

A little kid from Far Rockaway grows up

,� ZDV� ERUQ� ���$XJXVW� ����� LQ� 6W� -RVHSK¶V� +RVSLWDO�� )DU�5RFNDZD\�� D� EHDFK� FRPPXQLW\� RI� 1HZ� <RUN� &LW\�� :H�PRYHG�WR�/RV�$QJHOHV�MXVW�EHIRUH�P\���WK�ELUWKGD\��KDYLQJ�OLYHG� LQ�1HZ�<RUN�DQG�1HZ�-HUVH\� LQ� WKH� LQWHULP�� ,�GRQ¶W�UHPHPEHU�PXFK�DERXW�P\�OLIH�EHIRUH�/�$��H[FHSW�WKDW�,�HQ-MR\HG�SOD\LQJ�VWLFNEDOO�DQG�.LFN�WKH�&DQ��0\�'DG�DQG�ROGHU�EURWKHU��+DUROG��ZHQW�WR�/�$��DERXW�D�\HDU�EHIRUH�P\�0RP��P\�VLVWHU��3HDUO�DQG�,�MRLQHG�WKHP��0\�'DG�IRXQG�VRPH�RGG�MREV�DQG�ZDV�DEOH�WR�VDYH�HQRXJK�WR�SD\�IRU�RXU�WULS�E\�*UH\-KRXQG�EXV��0\�'DG�ZDV�D�SKDUPDFLVW��EXW�ORVW�KLV�GUXJVWRUH�LQ�WKH�*UHDW�'HSUHVVLRQ��+H�ZHQW�WR�/�$���WKH�³ODQG�RI�PLON�DQG�KRQH\´�� KRSLQJ� WR�¿QG� D� MRE��&DOLIRUQLD�� DW� WKDW� WLPH��PDGH�WKH�3KDUPDF\�H[DPLQDWLRQ�WRXJK�WR�NHHS�SKDUPDFLVWV�from other states from passing it and taking jobs away from California pharmacists.

0\�'DG�ZDV�ERUQ�LQ�5XVVLD��DV�ZDV�P\�0RP��0\�'DG�KDG�become a Rabbi in Russia, but his heart was not really in it DQG�KH�JDYH�LW�XS��+H�ZRUNHG�LQ�D�VZHDW�VKRS�IRU����D�ZHHN�LQ�1HZ�<RUN��EXW�PDQDJHG�WR�VWXG\�DQG�JHW�DGPLWWHG�WR�WKH�SKDUPDF\�VFKRRO�DW�&ROXPELD�8QLYHUVLW\��+H�GLG�ZHOO�DQG�was automatically admitted to medical school at Columbia but turned it down because it had been very hard for him ¿QDQFLDOO\�GXULQJ�KLV�HDUOLHU�VFKRRO�\HDUV�DQG�KH�ZDV�WU\LQJ�to save enough money to bring his family over from Russia, which he ultimately did. I never appreciated it earlier in my OLIH�EXW� ,� HYHQWXDOO\� FDPH� WR� UHDOL]H� WKDW� KH�ZDV� D� WHUUL¿F�UROH�PRGHO��0\�PRWKHU�ZDV�D�UROH�PRGHO�DV�ZHOO��6KH�ZDV�D�pharmacist in Russia but never pursued that vocation here. 6KH�ZDV�D�EHDXWLIXO�ZRPDQ��YHU\�ZDUP�DQG�IULHQGO\��D�JUHDW�cook, and just a good all-around person. When times were really bad for us, she loaded up a couple of valises with no-WLRQV� �QHHGOHV�� WKUHDG�� WLVVXHV��HWF���DQG�ZDONHG�IURP�GRRU�to door selling what she could. It was very tough work and GHPHDQLQJ��EXW�VKH�QHYHU�FRPSODLQHG��0\�EURWKHU��+DUROG��ZDV�ZDUP�DQG�IULHQGO\�DOVR��QHYHU�FRXOG�¿QG�ZRUN�WKDW�LQ-terested him and didn’t want to study, but he would give \RX�WKH�VKLUW�RII�KLV�EDFN��+H�ZDV�D�JRRG�OHIW�KDQGHG�WHQQLV�player with a hop serve that never bounced the way you H[SHFWHG�LW�WR��+H�GLHG�RI�DVWKPD�DW�DJH�����0\�VLVWHU��3HDUO��

D�EHDXWLIXO�\RXQJ�ZRPDQ��ZDV�D�GLHWLWLDQ��8&/$�JUDGXDWH��ZKR�GLHG�WUDJLFDOO\�DW�WKH�DJH�RI����LQ�DQ�DXWR±WUDLQ�ZUHFN�ZKHUH�WKHUH�ZDV�QR�JUDGH�FURVVLQJ�RU�JDWHV��6KH�ZDV�RQ�KHU�ZD\�WR�ZRUN�DW�D�ORFDO�KRVSLWDO�ZLWK�D�FROOHDJXH�GULYLQJ��6KH�was my closest friend at that time. I was away at medical school when this happened. I cried openly for hours when I heard about it, much more than I had ever cried all my life. 3HDUO�ZDV�D�OHIW\�DOVR�DQG�D�YHU\�JRRG�WHQQLV�SOD\HU�,�VKDUHG�my family’s hard times, of course. I had various odd jobs WKURXJKRXW�MXQLRU�KLJK�VFKRRO�DQG�KLJK�VFKRRO�±�KHOSLQJ�P\�father in his gardening jobs, and working for a chemist who PDQXIDFWXUHG�YDULRXV�IRRG�LWHPV�LQ�KLV�JDUDJH��,�PDGH����cents an hour and it really made me feel good. The food coloring he made was not exciting but his faux maple syrup DQG�IRRG�VHDVRQLQJ��YHU\�PXFK�OLNH�/DZU\¶V�VDOW��ZHUH�GHOL-FLRXV��'HVSLWH�VXFK�VQDFNV��,�ZDV�D�YHU\�VNLQQ\�OLWWOH�NLG��0\�SDUHQWV�HYHQWXDOO\�ZHQW�RQ�UHOLHI��ZLWK�JUHDW�UHOXFWDQFH��0\�siblings and I were pleased. We got a large salt pork roast ZKLFK�P\�SDUHQWV�UHIXVHG�WR�HDW�EXW�ZH�ORYHG�LW��$QG�,�JRW�

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166

A little kid from Far Rockaway grows up

The Bulletin of BISMiS

D�EUDQG�QHZ�SDLU�RI� FRUGXUR\V�� WKH\�ZHUH�D�ZHLUG�RUDQJH�FRORU��EXW�,�ZDV�GHOLJKWHG�ZLWK�WKHP��1HYHUWKHOHVV��P\�SDU-ents decided we should struggle along without help from the relief program after just a week or so on it. I remember some XQXVXDO�LQFLGHQWV�IURP�P\�KLJK�VFKRRO�GD\V��,Q�WKH�¿UVW��,�encountered a man who asked if I would like to join his church. When I saw the really nice-looking gray uniform I ZRXOG�JHW��,�VDLG��³6XUH´��:KHQ�,�JRW�KRPH�ZLWK�P\�XQLIRUP��P\�SDUHQWV�TXLFNO\��EXW�QLFHO\��VTXDVKHG�WKDW�LGHD��$QRWKHU�incident came up after my parents had a major argument. 0\�PRWKHU��XQFKDUDFWHULVWLFDOO\��WULHG�WR�SRLQW�RXW�WKDW�P\�father was a bad man by showing me a newspaper clipping about him serving jail time for beating up a bus driver. When I asked my dad about it, he told me that the bus driver was EXJJLQJ�KLP�EHFDXVH�RI�KLV�-HZLVK�DFFHQW��0\�PRP¶V�LGHD�EDFN¿UHG�EHFDXVH� ,�ZDV� UHDOO\� SURXG�RI�P\�GDG� IRU�ZKDW�KH�GLG��$�WKLUG�LQFLGHQW�FDPH�XS�LQ�FRQQHFWLRQ�ZLWK�D�NLGV¶�EDVNHWEDOO�WHDP�,�SOD\HG�RQ�IRU�WKH�ORFDO�7HPSOH��P\�RQO\�DI¿OLDWLRQ�ZLWK�WKH�7HPSOH�ZDV�WKLV�NLGV¶�FOXE�ZLWK�ORWV�RI�VSRUWV��,�DP�SUHWW\�PXFK�VHFXODU���,�GLGQ¶W�JHW�WR�SOD\�PXFK�basketball because I was the shortest kid in the club, bur one GD\�ZH�ZHUH�VXSSRVHG�WR�SOD\�D�FOXE�LQ�/RQJ�%HDFK�DQG�QR�one had access to a car. When they asked me if I had a car, ,�WROG�WKHP�,�FRXOG�ERUURZ�P\�GDG¶V�ÀDWEHG�WUXFN²DQ�ROG�6WDU�PRGHO�ZLWK�D�SXOO�RXW�LJQLWLRQ�VZLWFK�LQVWHDG�RI�D�NH\��,�KDG�D�GULYHU¶V�OLFHQVH�HYHQ�WKRXJK�,�ZDV�RQO\����EHFDXVH�in those days if you had to help drive the family around you

could get licensed. I didn’t tell my dad that I was doing this. :H�MXVW�SLOHG�DOO�WKH�NLGV�RQ�WKH�ÀDW�EHG�LQ�EDFN�DQG�WRRN�RII��$V�ZH�GURYH�WKURXJK�WKH�FLW\�RI�%HOO��ZH�ZHUH�SXOOHG�RYHU�by a motorcycle policeman. I hadn’t remembered to take my driver’s license and the truck had no registration slip in WKH�JORYH�FRPSDUWPHQW��6R�WKH\�KDXOHG�XV�LQWR�MDLO��:KHQ�,�was asked if I had my dad’s permission to take the truck, I VDLG��³2I�FRXUVH´��:HOO� WKH\�FDOOHG�P\�GDG�DQG��EOHVV�KLV�heart, he said yes when asked about letting me use the truck. They made him come out to pick us up and to bring his reg-LVWUDWLRQ�FHUWL¿FDWH�ZLWK�KLP��6R��ZH�VSHQW���KRXUV�RU�VR�LQ�MDLO�DQG�QHYHU�JRW�WR�/RQJ�%HDFK�WR�SOD\�WKH�JDPH��/DWHU��DW�home, I got a lecture about how dangerous it was to carry a EXQFK�RI�\RXQJ�NLGV�RQ�WKH�ÀDWEHG�RI�WKH�WUXFN�ZLWK�QRWKLQJ�to hold on to.

,�ZDV�RQO\��IW���������LQ�WDOO�ZKHQ�,�HQWHUHG�KLJK�VFKRRO��EXW�JDLQHG�H[DFWO\�RQH�IRRW� LQ�KHLJKW�GXULQJ�P\���\HDUV� WKHUH��The highlight of my high school period was playing on the tennis team and earning my letter two of the three years I SOD\HG��0\�SDUHQWV�KDG�ERXJKW�PH�D� WHQQLV� UDFNHW� IRU�P\���WK�ELUWKGD\��D�YHU\�ELJ�GD\�IRU�-HZLVK�ER\V��:H�ZHUH�YHU\�poor still at that point, and I’m sure they skimped on many a meal to be able to pay for the racket. I still regard this as WKH�YHU\�EHVW�SUHVHQW�,�KDYH�UHFHLYHG�LQ�P\�HQWLUH� OLIH��$V�I learned more about tennis, I realized that that racket was a pretty cheap one. But I loved it dearly and it got me into tennis head over heels. I also realized later that my folks took careful note of my spending weekends at the nearby

Sydney Finegold’s parents, Sam and Jennie, in their 30s.

Sydney Finegold’s sister, Pearl, in 1944, aged 20.

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167

Sydney M. Finegold

The Bulletin of BISMiS

([SRVLWLRQ�3DUN�ZKHUH�3DQFKR�*RQ]DOHV�ZDV�SOD\LQJ�DV�D�teenager and beating all the adults there. I never had had les-VRQV�EXW�,�ZDWFKHG�3DQFKR�DQG�RWKHUV�SOD\LQJ�DQG�SLFNHG�XS�D�ORW�DERXW�WKH�JDPH�WKDW�ZD\���7KLV�EHFDPH�D�ZD\�RI�OLIH�IRU�PH��,�UHDOL]HG�WKDW�,�FRXOG�OHDUQ�D�ORW�E\�MXVW�ZDWFKLQJ��DQG�listening to, people.)

,�KDG�DOZD\V�KHDUG�D�ORW�DERXW�8&/$�DQG�GUHDPHG�RI�JRLQJ�there someday. I applied to only that one school and luckily ZDV�DGPLWWHG��,�SDVVHG�WKH�DGPLWWDQFH�(QJOLVK�H[DP��ZKLFK�PRVW�SHRSOH�GLG�QRW�� WKDW�ERRVWHG�P\�FRQ¿GHQFH�FRQVLGHU-DEO\�DQG�VDYHG�PH�IURP�QHHGLQJ�WR�WDNH�UHPHGLDO�(QJOLVK�LQ-stead of something more interesting. I met with a counselor VRRQ�DIWHU�,�VWDUWHG��,�ZDV�DVNHG�ZKDW�,�SODQQHG�WR�GR�ZLWK�my life. I told her that I didn’t know, but I loved science and WHDFKLQJ� �DQG�DOVR�PHGLFLQH��EXW� WKDW�ZDV�RXW�RI� WKH�TXHV-WLRQ�EHFDXVH� ,�ZRXOG�QHYHU�EH�DEOH� WR�DIIRUG� LW���6KH� VDLG�there was a big need for botany teachers and that should ¿OO� WKH�ELOO�QLFHO\� IRU�PH�� ,�ZDV�GXELRXV�DERXW�KHU�FKRLFH��but agreed to it. I hated it from the beginning, although I have a few good memories. The entire class loved to joke DERXW�WKH�GHSDUWPHQW�FKDLU�ZKRVH�¿UVW�QDPH�ZDV�)ORUDEHOOH�DQG�ZKR� DOZD\V�ZRUH� D� GDUN�JUHHQ� VPRFN��ZH� FDOOHG�KHU�

“chlorophyll”. In my second year, I took a course in general bacteriology, as part of the Botany major. I fell in love with it immediately and promptly changed my major to bacteriol-RJ\��,�ZDV�LQ�KHDYHQ�DQG�IRU�WKH�¿UVW�WLPH�LQ�P\�OLIH�,�EHJDQ�to study.

$V� D� IUHVKPDQ�� ,� KDG� D� SDUW�WLPH� MRE� LQ� DQ� H[SHULPHQWDO�horticulture orchard. I had no idea what research was, I am ashamed to say, but the oranges were very large and deli-cious and I was still a starving kid, so I kept eating them XQWLO�WKH\�FDXJKW�PH�RQH�GD\�DQG�¿UHG�PH��,�GHDUO\�KRSH�WKDW�I didn’t ruin too many experiments. When I became a bacte-riology major, we made our own media and I soon learned that beef extract was delicious on crackers, or even by itself. $QG�� WDON� DERXW� OXFN� �ZKLFK� KDV� IROORZHG�PH� WKURXJKRXW�my life), I was invited to take a part-time job testing the VZLPPLQJ�SRRO�ZDWHU�IRU�FROLIRUP�FRXQWV��HWF���LQ�WKH�*LUOV¶�*\P���,�VWD\HG�RXW�RI�VFKRRO�IRU���\HDU�DIWHU�P\�IUHVKPDQ�\HDU�WR�KHOS�ZLWK�P\�¿QDQFHV��,�OLYHG�DW�KRPH�DQG�WKHUH�ZDV�QR� WXLWLRQ��MXVW�DQ�,QFLGHQWDO�)HH�RI��������SHU�\HDU� IRU�D�gym locker, towels, football tickets, etc.), but I was ashamed of the few clothes I had and needed snack money, movie PRQH\�� HWF�� ,� HDUQHG� ���� D�PRQWK�� ,� ERXJKW�P\� ¿UVW� VXLW��VHFRQG�KDQG�� DQG�P\�¿UVW�ZDWFK� >DOVR� VHFRQG�KDQG� �SXQ�QRW�LQWHQGHG�@��EXW�ZLWK�D�JUHHQ�FU\VWDO���DQG�D�ORW�RI�VHFRQG�hand furniture for my parents. I took philosophy, which was a very stimulating subject, and psychology both semesters

Sydney Finegold (right) with high school tennis doubles partner Frank Hite.

Sydney Finegold’s brother, Harold, in 1941.

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168

A little kid from Far Rockaway grows up

The Bulletin of BISMiS

LQ�WKH�8&/$�([WHQVLRQ�'LYLVLRQ�LQ�WKH�HYHQLQJV�GXULQJ�WKDW�year so that I would keep my tie-in with learning and be sure WR�UHWXUQ�WR�VFKRRO�DIWHU���\HDU��ZKLFK�,�GLG��/DWHU��DW�8&/$��I got a really classy job typing manuscripts for a famous FKHPLVWU\�SURIHVVRU��0D[�'XQQ��,W�ZDV�DQ�1<$��1DWLRQDO�<RXWK�$GPLQLVWUDWLRQ�� MRE� DQG�SDLG���� FHQWV� DQ�KRXU� �ELJ�WLPH� VWXII��� ,� SOD\HG� WHQQLV� DW�8&/$�� ,� IHOW� WKDW� ,�ZDV� DQ�RUGLQDU\� SOD\HU�� EXW� ,� WULHG� KDUG� �HVSHFLDOO\� DJDLQVW�86&��DQG�HDUQHG�P\�IURVK�QXPHUDOV�DQG�WZR�YDUVLW\�OHWWHUV��2QH�of the more exciting things to happen to me in my life was ZKHQ�,�ZHQW�XS�WR�WKH�$WKOHWLF�2I¿FH�WR�SLFN�XS�P\�IURVK�QXPHUDOV������IRU�������ZKHQ�,�ZRXOG�KDYH�JUDGXDWHG�LI�,�KDG�QRW�VWD\HG�RXW� WR�ZRUN� WKDW���\HDU���$V�,�FDPH�RXW�RI�WKH�RI¿FH��JULQQLQJ�IURP�HDU�WR�HDU��ZKRP�VKRXOG�,�PHHW�EXW�-DFNLH�5RELQVRQ��RQH�RI�WKH�¿QHVW�DWKOHWHV�DQG�¿QHVW�SHUVRQV�WR�HYHU�OLYH��+H�QRW�RQO\�OHWWHUHG�HYHU\�\HDU�LQ�DOO�IRXU�VSRUWV�LQ�ZKLFK�KH�SDUWLFLSDWHG��EDVHEDOO��IRRWEDOO��EDVNHWEDOO��DQG�WUDFN��EXW�KH�ZDV�RQH�RI�HDFK�WHDP¶V�VWDU�SOD\HUV��KH�ZHQW�RQ�WR�EUHDN�WKH�FRORU�OLQH�LQ�PDMRU�OHDJXH�EDVHEDOO��+H�EHDPHG�DW�PH�DQG�VDLG��³+H\��WKDW¶V�WHUUL¿F��NLG��&RQJUDWXODWLRQV�´��I was so excited I almost fell down the stairs. I certainly got some perspective after that chance encounter.

2I�LQWHUHVW�LV�WKH�IDFW�WKDW�,�KHDUG�YHU\�OLWWOH�DERXW�DQDHURELF�bacteria or anaerobic infections even though I was a bacte-ULRORJ\�PDMRU� DW� D�¿UVW�FODVV�XQLYHUVLW\��:H�GLGQ¶W� VHH� �RU�smell) them in any of the labs. and they were discussed only in terms of the major clostridial infections or intoxications �WHWDQXV�� ERWXOLVP�� DQG� JDV� JDQJUHQH��� DQG� EULHÀ\� DW� WKDW��7KHRGRUH�%HFNZLWK� �FKDLU��DQG�0HULGLDQ�%DOO�ZHUH� LQVSLU-ing teachers and they, and the program generally for bacteri-ology majors, made me know that I made the right decision to adopt that major.

,�ZDV�OXFN\�HQRXJK�WR�ZLQ�D������&DOLIRUQLD�6WDWH�VFKRODU-VKLS�RQH�\HDU��WKDW�ZDV�D�UHDO�JRGVHQG�DQG�PDGH�D�KXJH�GLI-ference in my life.

,�MRLQHG�WKH�0DULQH�&RUSV�UHVHUYH�LQ�RUGHU�WR�VWD\�LQ�VFKRRO�and avoid being drafted into the military. I knew about the OHJHQGDU\�IHDWV�RI�WKH�8�6��0DULQHV�EXW�GLGQ¶W�UHDOO\�KDYH�D�FOXH�DV�WR�KRZ�WKH\�¿W�LQWR�WKLQJV�DQG�H[DFWO\�ZKDW�WKH\�GLG��$IWHU�¿QLVKLQJ�ERRW�FDPS��LQ�ZKLFK�,�ZRUNHG�P\�KHDG�RII��DQG�JDLQHG�VRPH����SRXQGV�RI�PXVFOH���,�WUDQVIHUUHG�WR�WKH�1DY\�EHFDXVH�,�KDG�OHDUQHG�WKDW�WKH�1DY\�SURYLGHG�PHGLFDO�VHUYLFHV�IRU� WKH�0DULQHV��0\�¿UVW�DVVLJQPHQW� LQ� WKH�1DY\�ZDV�DV�D�1DY\�&RUSVPDQ�DQG�,�ZDV�SXW�LQ�WKH�FOLQLFDO�ODER-UDWRU\�RI�WKH�86�1DYDO�+RVSLWDO�LQ�/RQJ�%HDFK��&$��7KHUH�,�PHW� DQ� LQVSLULQJ�SDWKRORJLVW��/HRQ�5RVRYH��0'� �ZKRVH�VRQ��0LFKDHO��LV�DQ�RXWVWDQGLQJ�KHPDWRORJLVW�RQ�WKH�PHGLFDO�IDFXOW\�DW�8&/$���/HRQ�5RVRYH�GLG�DOO�WKH�DXWRSVLHV�DQG�,�watched him do the dissections on virtually all of them, and

soaked up his discussions of the disease and the cause of GHDWK��,Q�WKH�DEVHQFH�RI�DQ�,QIHFWLRXV�'LVHDVH�SK\VLFLDQ��WKH�VSHFLDOW\�ZDV�QRW�HVWDEOLVKHG�IRU�DQRWKHU����\HDUV�RU�VR���'U�5RVRYH��D�UHDO�UROH�PRGHO��ZDV�WKH�$WWHQGLQJ�3K\VLFLDQ�IRU�WKUHH�PHGLFDO�ZDUGV��D�SQHXPRQLD�ZDUG��D�UKHXPDWLF�IHYHU�ward, and a ward with patients with miscellaneous infec-WLRQV��LQ�DGGLWLRQ�WR�KLV�SDWKRORJ\�GXWLHV��7KLV�ZDV������DQG������DQG�:RUOG�:DU�,,�ZDV�RQJRLQJ��3HQLFLOOLQ�KDG�MXVW�EHHQ�discovered and virtually all of it was reserved for the mili-WDU\��,�KDG�ZKDW�,�FRQVLGHUHG�D�YHU\�SUHVWLJLRXV�MRE��,�ZDV�to collect all the urine from all patients treated with peni-cillin in order that the drug might be recovered for use in DGGLWLRQDO�SDWLHQWV��WKH�PDQXIDFWXULQJ�SURFHVV�ZDV�VWLOO�QRW�XS�WR�VSHHG���,�KDG�SQHXPRQLD�LQ�������W\SH�XQNQRZQ��DQG�had failed therapy with sulfonamides. They started me on penicillin at what would now be considered pediatric dos-DJH� ±� ������� XQLWV� HYHU\� �� KRXUV��$QG� WKH\�ZRXOG� FKHFN�on me after each dose because they were not yet sure what side effects might be encountered. I responded dramatically. 7KHUH�ZDV�DQRWKHU�FDVH�WKDW�LQWULJXHG�PH�±�D�\RXQJ�GHQWDO�RI¿FHU�ZKR�KDG�D�UXSWXUHG�DSSHQGL[�DQG�WKHQ�GHYHORSHG�JDV�JDQJUHQH�RI�WKH�DEGRPLQDO�ZDOO��$OO�RI�WKH�PHGLFDO�RI¿FHUV�conferred on this patient and agreed the prognosis was prob-ably hopeless, but they clearly needed to drain an associated abscess and debride all necrotic tissue. They hoped that with penicillin, they might possibly save him. I knew this young PDQ�EHFDXVH�KH�SOD\HG�WHQQLV��KH�ZDV�&DSWDLQ�RI�WKH�WHDP�DW�8&/$���+H�PDGH�ZKDW�HYHU\RQH�FRQVLGHUHG�D�PLUDFXORXV�recovery. I heard about him playing in a big tennis tourna-ment just a year or two ago and felt very happy about it.

,�ZDV� IRUWXQDWH� WR� EH� DSSRLQWHG� WR� WKH�1DY\� ,QGHSHQGHQW�'XW\� 6FKRRO� LQ� 1RUIRON�� 9LUJLQLD�� 7KLV� ZDV� D� ��PRQWK�course, quite intensive, on all aspects of medicine, other than major surgery, that might be encountered in a battle such as a beach assault or other situations in the military when a physician was not available. I thoroughly enjoyed this program and it was to prove very useful to me later. Fol-ORZLQJ�WKLV��,�ZDV�UHDVVLJQHG�WR�WKH�1DYDO�+RVSLWDO�LQ�/RQJ�Beach, California.

I was happy to see a notice on the bulletin board one day that WKH�1DY\�ZDV�JRLQJ�WR�VHOHFW�FDQGLGDWHV�IRU�PHGLFDO�VFKRRO�WKURXJK�WKH�9����SURJUDP�DQG�UHTXHVWLQJ�VHDPHQ�ZKR�ZHUH�LQWHUHVWHG�DQG�TXDOL¿HG�WR�DSSO\��,�ZDV�QRW�D�SUH�PHG�PDMRU�in college but my bacteriology major did qualify me, luck-ily. We had to list our top three choices and mine were Cal, 6WDQIRUG��DQG�:LVFRQVLQ��ZKLFK�KDG��DQG�VWLOO�KDV��DQ�H[FHO-OHQW�PLFURELRORJ\�SURJUDP���(YHQWXDOO\�,�KHDUG�WKDW�,�ZDV�VHOHFWHG� DQG� VKRXOG� DZDLW� RUGHUV� WR� SURFHHG� WR�*DOYHVWRQ��7H[DV��+RZHYHU��ZKHQ� ,� UHFHLYHG�PLOLWDU\�RUGHUV�QRW� ORQJ�DIWHU�WKDW�WKH\�ZHUH�WR�VHUYH�LQ�OLHX�RI�D�SK\VLFLDQ�RQ�DQ�/67�

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169

Sydney M. Finegold

The Bulletin of BISMiS

�/DQGLQJ�6KLS�7DQN���,�ZDV�FUXVKHG�WR�ORVH�WKH�RSSRUWXQLW\�of medical school, but the following day those orders were VXSHUVHGHG�E\�RUGHUV� IRU�PHGLFDO� VFKRRO��2QFH�DJDLQ��P\�luck held out.

,�NQHZ�QRWKLQJ�DERXW�*DOYHVWRQ�EHIRUHKDQG��EXW�,�IRXQG�WKH�FLW\��WKH�VWDWH�DQG�WKH�SHRSOH�ZRQGHUIXO��H[FHSW�IRU�WKH�FOL-PDWH�±�RSSUHVVLYH�KXPLGLW\���,W�LV�ZKHUH�,�PHW�P\�ZLIH�DQG�PRWKHU�RI�P\�WKUHH�FKLOGUHQ��0DU\�/RXLVH�6DXQGHUV��D�EHDX-tiful and most wonderful person, in my freshman class. We enjoyed discussing our classes and projects, and our jobs. 0DU\�ZDV�DV�SRRU�DV�,�ZDV�DQG�ZH�ERWK�ZRUNHG�ZKLOH�JR-LQJ�WKURXJK�PHG�VFKRRO��/XFNLO\��,�KDG�WKH�VR�FDOOHG�*,�%LOO�because of my prior military service and we could get by 2.�ZLWK�RXU�WZR�VPDOO�SDUW�WLPH�MREV��0DU\�ZRUNHG�IRU�'U�0RUULV�3ROODUG�GRLQJ�PRXVH�VWXGLHV�RI�SROLRP\HOLWLV�DQG�,�ZRUNHG�IRU�'U�(GJDU�3RWK��D�VXUJHRQ�ZKR�KDG� LQWURGXFHG�the so-called intestinal sulfonamides for preoperative prep-DUDWLRQ� RI� WKH� ERZHO� SULRU� WR� FRORQLF� VXUJHU\��0DU\� DQG� ,�married between semesters of our second year and had a ��ZHHNHQG�KRQH\PRRQ�LQ�+RXVWRQ�

2XU�¿UVW�FKLOG��-RH��ZDV�ERUQ�LQ�*DOYHVWRQ�QHDU�WKH�HQG�RI�RXU�LQWHUQVKLS�WKHUH�DW�WKH�86�0DULQH�+RVSLWDO��D�KRVSLWDO�IRU�PHUFKDQW�VHDPHQ���-RH¶V�PLGGOH�QDPH�LV�*UHJRU\�LQ�KRQRU�RI�5D\PRQG�*UHJRU\��WKHQ�&KDLU�RI�,QWHUQDO�0HGLFLQH�DQG�D�PRVW�LQVSLULQJ�LQWHUQLVW�DQG�WHDFKHU��-RH�DWWHQGHG�8&/$��

DQG�REWDLQHG�D�0DVWHU¶V�GHJUHH�LQ�DXWRPRWLYH�HQJLQHHULQJ��DQG�EXLOW� WKH�¿UVW�ZRUNLQJ�K\GURJHQ�FDU��+H�VXEVHTXHQWO\�GHFLGHG�RQ�D�FDUHHU�LQ�EXVLQHVV�DQG�REWDLQHG�DQ�0%$��ZLWK�KRQRUV��IURP�+DUYDUG��+H�DQG�KLV�ZLIH�.LP��D�QXUVH�SUDFWL-WLRQHU��OLYH�QHDU�PH�±�LQ�6DQWD�%DUEDUD��7KHLU�WZR�FKLOGUHQ��Chris and Brie, graduated from the University of California, 6DQ�'LHJR��%ULH�KDV�ZRUNHG�IRU�YDULRXV�QRQ�SUR¿W�FRPSD-nies providing assistance to downtrodden people, mostly in developing countries and has travelled and lived extensively LQ�$IULFD� DQG�/DWLQ�$PHULFD��6KH�ZDV� D� JRRG� DWKOHWH� DQG�FRXOG� WDNH�KHU�ROG�6DDE�FDU�DSDUW�DQG�SXW� LW�EDFN� WRJHWKHU�DJDLQ��-RH�KDG�WDXJKW�KHU�KRZ��RI�FRXUVH��&KULV�MXVW�REWDLQHG�KLV�0%$�IURP�WKH�8QLYHUVLW\�RI�&DOLIRUQLD��%HUNHOH\��DQG�LV�QRZ�ZRUNLQJ�IRU�*RRJOH��$W�8&�6DQ�'LHJR��KH�ZDV�DQ�$FDGHPLF�$OO�$PHULFDQ�ZDWHU� SROR�SOD\HU� DQG� WKH� VWDU� RI�the team.

'U�3RWK�ZDV�DQ�DFFRPSOLVKHG�VXUJHRQ�DQG�VRPHWKLQJ�RI�DQ�HQJLQHHU��+H�KDG�SHFDQ�WUHHV�LQ�KLV�EDFN\DUG�DQG�LQYHQWHG�a machine to automatically shell them with whole nuts as the end product. The apparatus he designed was a moving belt on which pecans were automatically “fed” one at a time ZLWK�WKH�VDPH�H[DFW�GLVWDQFH�EHWZHHQ�WKH�QXWV��$W�RQH�SRLQW��as they moved along, a little drill came down and drilled a small hole in the shell. Further down the line, acetylene gas ZDV�LQMHFWHG�LQWR�WKLV�KROH�DQG�¿QDOO\�D�VSDUN�ZDV�GLUHFWHG�at the hole and the shell blew off leaving an undamaged SHFDQ��+H�GHVLJQHG�DQG�EXLOW�D�VLPLODU�DVVHPEO\�DSSDUDWXV�for automatically feeding dogs meatballs, containing one or DQRWKHU�GUXJ�KH�ZDV�WHVWLQJ��WR�WKH�GRJV�HYHU\���RU���KRXUV��The apparatus consisted of a number of cages in two rows, ZLWK� RQH� GRJ� SHU� FDJH�� (DFK� FDJH� KDG� D�PHWDO� WXEH�ZLWK�holes on each side so that he could place a series of medi-cated meatballs in the tubes, each meatball separated from the next one in the tube by a metal pin that was connected to a chain that moved at just the right speed to drop one

Sydney and Mary Finegold with their two eldest children, Joe and Pat, in 1952.

Sid’s son Joe with wife, Kim.

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170

A little kid from Far Rockaway grows up

The Bulletin of BISMiS

PHDWEDOO�LQWR�HDFK�FDJH�DW�H[DFWO\�WKH�SURSHU�LQWHUYDO����RU���KRXUV���$Q�DQLPDO�WHFKQLFLDQ�ZRXOG�LQVHUW�D�SROLVKHG�KROORZ�glass tube equipped with a suction bulb into the rectum of the dogs to obtain fecal specimens for microbiologic stud-LHV��P\�MRE���:H�XVHG�D�YDULHW\�RI�PHGLD�GHVLJQHG�WR�VHOHFW�RXW�SDUWLFXODU�JURXSV�RI�EDFWHULD��2Q�WKH�ZKROH��WKH�PHGLD�were appropriate and organisms recovered on the plate me-GLD�ZHUH�LGHQWL¿HG�DQG�FRXQWHG��7KH�RQH�ÀDZ�LQ�WKH�VHWXS�ZDV�WKH�RQH�XVHG�IRU�UHFRYHU\�RI�DQDHURELF�EDFWHULD��'U�3RWK�used Brewer plates with the lid dipping down into the bot-tom of the dish to minimize the air space above the Brewer thioglycollate agar that was used. It was not recognized that most so-called aerobes in humans are facultative and grow DW�OHDVW�DV�ZHOO�DQDHURELFDOO\��RU�EHWWHU��WKDQ�DHURELFDOO\�DQG�there was no setup for subculture in different atmospheres. $Q\WKLQJ�WKDW�JUHZ�RQ�WKH�%UHZHU�SODWHV�ZDV�FDOOHG�DQ�DQ-DHUREH��DQG�QRW�IXUWKHU�FODVVL¿HG����,�UHFRJQL]HG�WKH�ÀDZ�LQ�later years when I began to work on anaerobes and bowel ÀRUD�LQ�VHULRXV�IDVKLRQ��

While in medical school, I decided it would be important to study what impact antimicrobial agents had on the bowel ÀRUD��0\�ZLIH� DQG� ,� DQG� DQRWKHU� FODVVPDWH� DOO� WRRN� YDUL-ous antimicrobials and provided stool specimens for study. There were no IRBs in those days and no one cleared proj-HFWV�RU�IROORZHG�WKHP�IRU�SUREOHPV��/XFNLO\��ZH�GLGQ¶W�HQ-FRXQWHU�DQ\�VLGH�HIIHFWV�RI�QRWH�DQG�¿QDOO\�UHSRUWHG�RXU�UH-sults in the Texas Reports on Biology and Medicine��(YHQ�WRGD\��WKH�)'$�VWLOO�GRHV�QRW�LQVLVW�WKDW�SKDUPDFHXWLFDO�FRP-panies dealing with drugs that are not absorbed after oral administration provide pertinent pharmacologic and micro-biologic data.

I talked to various of my medical school professors about

what opportunities there might be in academic medicine that would permit me to use my microbiology training. They all VDLG� WKDW� WKHUH� ZHUH� QR� VSHFL¿F� GLVFLSOLQHV� IRU� WKDW� EDFN-ground except in microbiology per se��EXW�WKDW�,�VKRXOG�¿QG�someone who was doing research on microbes and join that team for a residency in internal medicine. I had heard of /RXLV�:HLQVWHLQ�LQ�%RVWRQ�DQG�OLNHG�ZKDW�,�KDG�UHDG�RI�KLV�papers so I made an appointment to meet with him, using most of our meager savings to make that trip. When I got there, I found out that Dr Weinstein was busy and could not see me, but sent one of his Fellows to meet with me. The Fellow was very nice, but I was really put off to not even get to meet Weinstein, so I dropped that program from my OLVW��1H[W�,�ZHQW�WR�VHH�'U�:HVOH\�6SLQN�DW�WKH�8QLYHUVLW\�RI�0LQQHVRWD�DQG�KLV�\RXQJHU�FROOHDJXH��'U�:HQGHOO�+DOO�DW� WKH� 0LQQHDSROLV� 9HWHUDQV�$IIDLUV� �9$� +RVSLWDO��� 7KH\�were both friendly people, clearly very bright and produc-tive, and most enthusiastic. These were qualities I had found LPSRUWDQW� LQ�P\�\RXQJ�FDUHHU��6R��,�HQGHG�XS�DFFHSWLQJ�D�SRVLWLRQ� WKHUH��GULYLQJ�XS� WKHUH� IURP�*DOYHVWRQ�ZKHQ� -RH�ZDV���ZHHNV�ROG�� ,�ZRUNHG�SULPDULO\� DW� WKH�9$�ZKHUH�'U�6SLQN�PDGH� URXQGV�ZLWK�'U�+DOO� LQ�D�SURJUDP� WKDW�ZDV�D�medical residency, but they used the words “infectious dis-eases” and made rounds once or twice weekly on patients ZLWK� WKHVH�HQWLWLHV��6R�� LQ�HVVHQFH�� LW�ZDV�D�FRPELQHG�SUR-JUDP�DOWKRXJK�LW�ZDV�QRW�ODEHOHG�DV�VXFK��0\�¿UVW�\HDU�WKHUH�was purely clinical, with both internal medicine and some LQIHFWLRXV�GLVHDVH�SUREOHPV��$W�WKH�EHJLQQLQJ�RI�P\�VHFRQG�year, I was offered a position as head of infectious diseases DW�WKH�0LQQHDSROLV�*HQHUDO�+RVSLWDO��D�FRXQW\�IDFLOLW\�ZLWK�a contagious disease unit where patients with that type of in-fectious diseases were isolated and which received patients from around the city. I was given the Faculty title of Instruc-WRU�RI�0HGLFLQH�DQG�ZDV�JLYHQ�D�ODE�ZLWK�D�WHFKQLFLDQ�DQG�D�GLVKZDVKHU��ERWK�RI�ZKRP�HDUQHG�PRUH�WKDQ�,�GLG��,�GLG�QRW�have a clue as to how I should go about setting up my labo-UDWRU\��'U�%XUWRQ��%XG��:DLVEUHQ��ZKR�SUHFHGHG�PH�DW�³WKH�*HQHUDO´�YHU\�NLQGO\�VSHQW�PXFK�RI�WKH�ZHHNHQG�EHIRUH�KH�left with me, teaching me something about contagious dis-eases, how to set up a lab, and what might be an interesting IRFXV�IRU�P\�¿UVW�YHQWXUH�RQ�P\�RZQ�LQWR�IRUPDO�UHVHDUFK��DQWLELRWLF�VXVFHSWLELOLW\�WHVWLQJ�LV�ZKDW�KH�UHFRPPHQGHG���,�would have been totally lost if Bud had not interrupted his packing, etc., to coach me as much as he could for the good part of that weekend.

0\�0LQQHDSROLV�H[SHULHQFH�ZDV�QRWDEOH�LQ�WKUHH�UHVSHFWV�LQ�SDUWLFXODU��)LUVW��RXU�GDXJKWHU�3DWULFLD��3DW��ZDV�ERUQ�WKHUH�LQ�������VHFRQGO\��ZH�KDG�D�PDMRU�RXWEUHDN�RI�SROLRP\HOL-WLV� LQ�0LQQHDSROLV� WKDW� \HDU�ZLWK�PDQ\� EXOEDU� FDVHV�� DQG�

Sid with granddaughter Brie, daughter Pat, and her husband, Michael.

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171

Sydney M. Finegold

The Bulletin of BISMiS

thirdly, I saw an interesting case of pleural empyema that was to affect my subsequent career.

3DW�ZDV��DQG�VWLOO�LV��D�SXUH�GHOLJKW²ZDUP�DQG�IULHQGO\�DQG�YHU\�EULJKW��6KH�LV�FXUUHQWO\�3URIHVVRU�RI�)UHQFK�DW�'DOKRX-VLH�8QLYHUVLW\�LQ�+DOLID[��DQG�ZDV�'HSDUWPHQWDO�&KDLU�RQ�WZR�RFFDVLRQV�DQG�KDV�ZRQ�VHYHUDO�8QLYHUVLW\�KRQRUV���3DW�DQG�KHU�KXVEDQG��0LFKDHO��D�3URIHVVRU�RI�&DQDGLDQ�+LVWRU\�DW�'DOKRXVLH��KDYH�WZR�FKLOGUHQ�DOVR��0LVW\�REWDLQHG�D�0DV-ter’s degree at the University of Toronto and became an ex-SHUW�DUFKLYLVW��6KH�LV�FXUUHQWO\�DUFKLYLQJ�LPSRUWDQW�KLVWRULFDO�GRFXPHQWV�DW�D�PXVHXP�LQ�:LQQLSHJ��$QG\�KDV�QRW�\HW�VHW-WOHG�RQ�D�FDUHHU��EXW�KDV�VKRZQ�H[FHOOHQW�WDOHQW�LQ�WKH�¿HOGV�RI�PXVLF��SOD\LQJ�WKH�FHOOR�DQG�HOHFWULF�JXLWDU�LQ�D�EDQG�WKDW�KH�RUJDQL]HG��DQG� LQ� WKHDWHU�DUWV��+H�REWDLQHG�D�&DQDGLDQ�government grant to write and perform a play that was well UHFHLYHG�LQ�0RQWUHDO�ZKHUH�KH�QRZ�OLYHV�

The polio cases from all over the city were referred to our &RQWDJLRXV�'LVHDVH�8QLW�DW�0LQQHDSROLV�*HQHUDO�+RVSLWDO��$W�WKDW�WLPH�³LURQ�OXQJV´�ZHUH�XVHG�IRU�SDWLHQWV�ZLWK�UHVSLUD-WRU\�SDUDO\VLV��WKH\�RYHUÀRZHG�WKH�URRPV�DQG�FURZGHG�DOO�WKH�KDOOZD\V��1RZ��RI�FRXUVH��ZH�FDQ�XVH�WKH�VPDOO�EHGVLGH�respirators for such cases and care of that type of patient is much simpler as a result. If the bulbar polio patient required a tracheotomy to permit easier and safer handling of secre-WLRQV��LW�ZDV�YHU\�GLI¿FXOW�WR�PDNH�WKH�UHTXLUHG�FRQQHFWLRQ�WR�WKH�LURQ�OXQJ��WKLV�ZDV�EHIRUH�LQWXEDWLRQ�ZDV�XVHG�H[FHSW�for the operating room and it would not have been suitable for long-term airway management anyway).

The case of empyema was a puzzle. Frank pus that was foul-smelling was obtained on thoracentesis of the pleural space. There were numerous polymorphonuclear leukocytes on *UDP�VWDLQ��EXW�QR�UHFRJQL]DEOH�EDFWHULDO�IRUPV��WKHUH�ZHUH�EL]DUUH� *UDP�QHJDWLYH� VWDLQLQJ� SOHRPRUSKLF� IRUPV�� ,� SUH-sented the case to our monthly statewide Infectious Diseases 6HPLQDU�DQG�QR�RQH�LQ�WKH�DXGLHQFH�NQHZ�ZKDW�ZDV�JRLQJ�on in the patient, who was clearly quite ill. The attendees at WKH�FRQIHUHQFH�ZHUH�IURP�WKH�6WDWH�+HDOWK�'HSDUWPHQW��WKH�8QLYHUVLW\�RI�0LQQHVRWD�LQIHFWLRXV�GLVHDVH�VSHFLDOLVWV��QRW�yet called that as it still was not an established specialty) and microbiologists, and miscellaneous hospitals, including the 0LQQHDSROLV�*HQHUDO�+RVSLWDO��)LQDOO\��VLQFH�QR�RQH�FRXOG�offer any plausible diagnoses or plan of action, one of my fellow residents in internal medicine timidly suggested that PD\EH� LW�ZDV�DQ�DQDHURELF� LQIHFWLRQ��(DUOLHU��KH�KDG�EHHQ�D� VWXGHQW� DW� -RKQV�+RSNLQV� 6FKRRO� RI�0HGLFLQH�� +H� VDLG�he remembered one of the faculty there talking about how GLI¿FXOW�DQDHURELF�LQIHFWLRQV�ZHUH�WR�GLDJQRVH�RQ�RFFDVLRQ�and that they often produced a foul odor and the organisms

PLJKW�EH�GLI¿FXOW�WR�UHFRJQL]H�RQ�*UDP�VWDLQ�DQG�GLI¿FXOW�WR�JURZ��1R�RQH�NQHZ�KRZ�WR�UHVSRQG�WR�WKHVH�FRPPHQWV�

,� VKRXOG� DOVR� FRPPHQW� RQ� WKH�0LQQHDSROLV� ZHDWKHU�� 7KH�winters were tough, especially since I bought a house, from D�GHSDUWLQJ�WUDLQHH��ZKLFK�ZDV�RQ�D�FRUQHU��WKHUHIRUH��WZLFH�as much snow to shovel) and which had a driveway that went down steeply to our garage. It was on a street that the snow plow visited regularly and every time it went by we KDG�D�KXJH�DFFXPXODWLRQ�RI�VQRZ�LQ�WKH�GULYHZD\�

6RRQ�DIWHU�,�VWDUWHG�P\�WKLUG�\HDU�LQ�0LQQHDSROLV��,�ZDV�FDOOHG�back into military service because I had no active duty after JRLQJ�WR�PHGLFDO�VFKRRO��IRU�RQH�VHPHVWHU�XQGHU�WKH�1DY\�9����SURJUDP��HYHQ�WKRXJK�,�KDG�RYHU���\HDUV�RI�DFWLYH�GXW\�before I received that appointment. This time I was allowed WR�WUDQVIHU�WR�WKH�$UP\�ZKHUH�,�ZDV�D�5HJLPHQWDO�6XUJHRQ��WKLV�FDOOHG�IRU�D�UDQN�RI�0DMRU��EXW�DOO�UDQNV�ZHUH�IUR]HQ�VR�,�ZHQW�LQ�DV�D�)LUVW�/LHXWHQDQW���,�ZDV�ZLWK�WKH���WK�,QIDQ-WU\�5HJLPHQW�LQ�WKH�6HFRQG�,QIDQWU\�'LYLVLRQ��$IWHU�WUDLQLQJ�DW�)RUW�6DP�+RXVWRQ�LQ�6DQ�$QWRQLR��7H[DV��ZKHUH�0DU\¶V�IDPLO\�OLYHG��P\�UHJLPHQW�ZDV�VKLSSHG�WR�*RWHPED��-DSDQ��DW�WKH�IRRW�RI�0W�)XML�ZKLFK�,�FRXOG�VHH�LQ�DOO�LWV�VSOHQGRU�from the window of my barracks. I was Commander of the 0HGLFDO�&RPSDQ\�RI�WKH���WK�5HJLPHQW��,�VHW�XS�D�SK\VLFDO�training program and an educational program to prepare for VHUYLFH�LQ�WKH�¿HOG�LQ�.RUHD�DV�D�EDFNXS�WR�DQRWKHU�,QIDQWU\�XQLW�WKDW�ZDV�DOUHDG\�WKHUH��$OWKRXJK�ZH�GLG�QRW�KDYH�PDQ\�SDWLHQWV��,�VHW�XS�D�PLOLWDU\�¿HOG�KRVSLWDO�WR�KDYH�WKDW�H[SHUL-ence. There were only three interesting patients during the WLPH�ZH�ZHUH�LQ�-DSDQ�±�D�\RXQJ�ER\�ZKR�ZDV�EURXJKW�LQ�by his father after drowning in a small body of water near WKHLU�KRPH� �XQIRUWXQDWHO\��KH�ZDV�GHDG�RQ�DUULYDO�DQG�ZH�ZHUH� XQDEOH� WR� UHVXVFLWDWH� KLP��� D� SDWLHQW� ZKR� KDG� UHQDO�shutdown after being given a bottle of distilled water intra-

Mary and Sydney Finegold some time in the 1960s.

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172

A little kid from Far Rockaway grows up

The Bulletin of BISMiS

YHQRXVO\�LQVWHDG�RI�QRUPDO�VDOLQH��ZH�DLU�HYDFXDWHG�KLP�WR�D�ODUJHU�IDFLOLW\�ZKHUH�KH�PDGH�DQ�XQHYHQWIXO�UHFRYHU\���DQG�PH�LQ�ZKRP�,�GLDJQRVHG�*HUPDQ�PHDVOHV��$QRWKHU�LQWHUHVW-ing experience I had was driving military jeeps and a two-ton truck on the opposite side of the road from our custom in WKH�YLOODJH�RI�*RWHPED�DQG�WR�<RNRKDPD��,�GLG�WKLV�MXVW�IRU�IXQ��LW�ZDV�QRW�LQ�P\�MRE�GHVFULSWLRQ��

:H�WKHQ�VKLSSHG�RXW�WR�.RUHD�ZKHUH�ZH�ZHUH�VWDWLRQHG�LQ�3XVDQ�� DW� WKDW� WLPH�D� VPDOO� FLW\�ZKLFK�ZDV�YHU\�SRRU� DQG�ZLWK� SRRU� VDQLWDWLRQ��PRVW� RI� WKH� KRXVHV� KDG�ÀDWWHQHG� WLQ�FDQV�IRU�URRIV��6RRQ�ZH�PRYHG�RXW�LQWR�SRVLWLRQ�EHKLQG�WKH�RWKHU�LQIDQWU\�XQLW��7KH�DUWLOOHU\�¿UH�IURP�WKH�HQHP\�ZDV�UH-DOO\�ORXG�DQG�HDFK�VKHOO�VKRRN�WKH�JURXQG��LW�ZDV�YHU\�VFDU\��EXW�ZH�GLG�QRW�VXIIHU�DQ\�FDVXDOWLHV�DQG�HYHQWXDOO\��DIWHU����months altogether overseas) my tour of duty was up and I ZDV�VHQW�KRPH�DQG�GLVFKDUJHG��:KHQ�,�JRW�KRPH��-RH�DQG�3DW�UHSHDWHGO\�VDLG��³'ULYH�IDVW��'DGG\��OLNH�0RPP\�GRHV�´��,�GURYH�SUHWW\�VORZO\�LQ�-DSDQ��RQ�WKH�OHIW�VLGH�RI�WKH�URDG��

,QVWHDG�RI�¿QLVKLQJ�XS�P\�WUDLQLQJ�LQ�0LQQHDSROLV��ZH�GH-FLGHG�WR�PRYH�WR�/RV�$QJHOHV�ZKHUH�P\�IDPLO\�OLYHG��7KH�8&/$�0HGLFDO� 6FKRRO� ZDV� EHLQJ� EXLOW� DQG� WKHLU� IDFXOW\�ZDV�KRXVHG�DW� WKH�9$�+RVSLWDO� LQ� WKH�:HVWHUQ�SDUW�RI�/RV�$QJHOHV�� D� ���PLQXWH� GULYH� IURP�ZKHUH� WKH� 8&/$�0HGL-FDO�&HQWHU�ZDV�WR�EH�EXLOW��,�VWDUWHG�DW�WKH�9$�LQ�'HFHPEHU������DQG�KDYH�EHHQ�KHUH�HYHU�VLQFH��,�WUDLQHG�ZLWK�:LOOLDP��%LOO��+HZLWW��D�SULQFH�RI�D�PDQ�DQG�DQ�H[SHUW�FOLQLFDO�LQIHF-WLRXV�GLVHDVHV�SHUVRQ��+H�ZDV�YHU\�DUWLFXODWH��,�ORYHG�WR�KHDU�his formal presentations and lectures. I learned a good deal about life and how to be a gentleman, as well as infectious GLVHDVHV��IURP�KLP��+H�ZDV�D�JRRG�WHQQLV�SOD\HU�DQG�ZH�KDG�PDQ\�IXQ�PDWFKHV��$IWHU���\HDU�RI�WUDLQLQJ�LQ�LQWHUQDO�PHGL-cine/infectious diseases, I was offered a job as Instructor of 0HGLFLQH�DW�8&/$��7KH�VDODU\�ZDV�ORZ�VR�WKH\�SHUPLWWHG�PH�WR�KDYH�D�KDOI�WLPH�MRE�DW�WKH�9$�+RVSLWDO��WKHQ�NQRZQ�DV�WKH�:DGVZRUWK�9$��QRZ�9$�+RVSLWDO�:HVW�/RV�$QJHOHV���,�ZRUNHG�LQ�WKH�(PHUJHQF\�5RRP�IURP����QRRQ�6DWXUGD\�WR���DP�6XQGD\�HYHU\�ZHHNHQG��D����KRXU�VKLIW�DQG�WKHUHIRUH�KDOI�WLPH���6RPH�ZHHNHQGV�,�ZRXOGQ¶W�JHW�PXFK�VOHHS��EXW�,�ZRXOG�FDWFK�XS�RQ�6XQGD\��,W�ZDV�D�JUHDW�H[SHULHQFH��VHHLQJ�the patient before anyone else and often they were quite ill. ,�KDG�D�FUDFNHUMDFN�QXUVH�QDPHG�-RKQQ\�ZKR�ZRXOG�VFUHHQ�SDWLHQWV�IRU�PH�ZKHQ�WKLQJV�JRW�EXV\��6KH�KDG�WUHPHQGRXV�clinical judgment and I very quickly learned that if she whis-pered “Drop that patient and come here quickly” that I better GR� WKDW�� 6XUJHRQV�� UDGLRORJLVWV�� DQG� RWKHU� VSHFLDOLVWV� WRRN�calls from home, but were always available on short notice.

$IWHU���\HDUV��,�VZLWFKHG�RYHU�WR�WKH�9$�IXOO�WLPH�DV�&KLHI�RI�WKH�,QIHFWLRXV�'LVHDVHV�6HFWLRQ�DQG�WKH�3XOPRQDU\�'LVHDVH�6HFWLRQ��$IWHU�VRPH���\HDUV�RU�VR��D�IXOO�WLPH�&KLHI�ZDV�VH-

OHFWHG�IRU�WKH�3XOPRQDU\�'LVHDVH�6HFWLRQ�DQG�,�VWD\HG�ZLWK�WKH�,QIHFWLRXV�'LVHDVHV�6HFWLRQ��9DULRXV�SHRSOH�DURXQG�WKH�FRXQWU\�ZHUH�QDPLQJ�WKHLU�XQLWV�,QIHFWLRXV�'LVHDVH�6HFWLRQ�RU�'LYLVLRQ�� HWF�� )LQDOO\��0D[� )LQODQG�� LQIRUPDOO\� NQRZQ�as the “Father of Infectious Diseases”, at the Boston City +RVSLWDO��(G�.DVV�DQG�RWKHUV�GHFLGHG�LW�ZDV�WLPH�WR�RUJDQL]H�DQ�RI¿FLDO�QDWLRQDO�VRFLHW\��WKH�,QIHFWLRXV�'LVHDVHV�6RFLHW\�RI�$PHULFD��$Q�RUJDQL]DWLRQDO�PHHWLQJ�ZDV�VHW�XS�LQ������DQG�%LOO�+HZLWW�DQG�,�ZHUH� LQYLWHG� WR� MRLQ� LQ� WKH�RUJDQL]D-WLRQDO�DFWLYLWLHV��7KH�6RFLHW\�FDPH�LQWR�EHLQJ�LQ�������)RU-PDO�WUDLQLQJ�SURJUDPV�FDPH�DORQJ�ODWHU�DQG�VSHFL¿F�FULWHULD�IRU� FHUWL¿FDWLRQ� RI� WUDLQLQJ� SURJUDPV� DQG� RI� )HOORZV�ZDV�later still.

1RW�ORQJ�DIWHU�,�EHFDPH�&KLHI�RI�,QIHFWLRXV�'LVHDVHV�DW�WKH�9$��ZH�KDG�D�SDWLHQW�YHU\�UHPLQLVFHQW�RI�WKH�RQH�,�KDG�HQ-FRXQWHUHG� LQ�0LQQHDSROLV�� ,W�ZDV� D� FDVH� RI� SXWULG� SOHXUDO�HPS\HPD�ZLWK� QR� JURZWK� RQ� �DHURELF�� FXOWXUHV� DQG� TXHV-WLRQDEOH�SOHRPRUSKLF�EDFWHULD�RQ�*UDP�VWDLQ��,�GLVFXVVHG�WKH�FDVH�ZLWK�'U�9HUD�6XWWHU��KHDG�RI�WKH�&OLQLFDO�0LFURELRORJ\�/DE��DW�WKH�9$�DQG�WROG�KHU�ZKDW�P\�IHOORZ�WUDLQHH�LQ�0LQ-neapolis said about it possibly being anaerobic.

9HUD�VDLG�VKH�ZDV�VXUH� WKDW�VKH�KDG�DQ�ROG�%UHZHU�DQDHUR-ELF� MDU� VRPHZKHUH� LQ� WKH�KRVSLWDO� EDVHPHQW��6KH� IRXQG� LW��FOHDQHG�LW�XS��DQG�ZH�¿QDOO\�¿JXUHG�RXW�KRZ�WR�XVH�LW��ZLWK�RUGLQDU\� OLQH�JDV�� ,Q�PDQ\�DUHDV�� OLQH�JDV� �QDWXUDO� JDV�� LV�WR[LF�WR�DQDHUREHV��EXW�OXFNLO\�LW�ZDV�QRW�LQ�/�$��:H�KDG�D�funny-looking setup, but we were able to grow several an-DHUREHV�IURP�WKH�HPS\HPD�ÀXLG�RI�WKLV�SDWLHQW��7KDW�VWDUWHG�a concerted effort to look for anaerobes in all kinds of speci-mens and we ultimately learned a good bit about anaerobic bacteriology and clinical aspects of anaerobic infections. :KHQ�RUDO�QHRP\FLQ�ZDV�¿UVW�LQWURGXFHG��ZH�VWXGLHG�LW�EH-cause of my previous interest in preoperative bowel “preps” ZKLOH�ZRUNLQJ�ZLWK�'U�3RWK�LQ�*DOYHVWRQ��:H�VHW�XS�YDULRXV�FXOWXUH�PHGLD� LQ�SODWHV� DQG�ZH�DOVR�XVHG�D� VHULHV�RI�ÀXLG�thioglycolate broths, with serial ten-fold dilutions of stool and various concentrations of neomycin. It was a major dis-DSSRLQWPHQW� WR� ¿QG� QR� JURZWK� RQ� DQ\� RI� RXU� SODWHV��7KH�EURWKV�ZHUH� WXUELG��EXW�*UDP�VWDLQ� VKRZHG� IXQQ\�ORRNLQJ�GHEULV�DQG�QRWKLQJ�JUHZ�RQ�VXEFXOWXUHV�RQWR�SODWHV��,W��¿QDO-O\���GDZQHG�RQ�PH�WKDW�WKHVH�EURWKV�ZHUH�SUREDEO\�JURZLQJ�DQDHUREHV�DQG�WKLV�ZDV�TXLFNO\�YHUL¿HG�E\�VXEFXOWXUH�RQWR�plates incubated in the Brewer jar.

There were not many people interested in anaerobes in the 8�6��DW� WKDW� WLPH�DQG�QRW�PXFK� OLWHUDWXUH� WKDW�ZDV�KHOSIXO��'DYLG�7��6PLWK�RI�'XNH�FHUWDLQO\�NQHZ�DERXW�WKHP�DQG�ZDV�GRLQJ�YDULRXV�VWXGLHV�LQ�DQLPDOV��+H�GLHG�EHIRUH�,�WKRXJKW�WR� WU\� WR� FRQWDFW�KLP� �QRZ��RI� FRXUVH�� HYHU\RQH� IHHOV� IUHH�to e-mail with any questions about anaerobes or anaerobic

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173The Bulletin of BISMiS

Sydney M. Finegold

infections, but it just didn’t seem proper to write or phone LQ�WKRVH�GD\V���:LOOLDP�$OWHPHLHU��D�GLVWLQJXLVKHG�VXUJHRQ��wrote about anaerobes in surgical infections and was inter-ested in the so-called Bacteroides melaninogenicus �ODWHU�H[SDQGHG� WR� VHYHUDO� JHQHUD� DQG�PXOWLSOH� VSHFLHV��� (GZLQ�3XODVNL�ZDV�DQRWKHU�VXUJHRQ�LQWHUHVWHG�LQ�DQDHUREHV��7KHUH�ZHUH� GHQWLVWV�� QRWDEO\�6LJPXQG�6RFUDQVN\�� DW� WKH�)RUV\WK�'HQWDO�,Q¿UPDU\�LQ�%RVWRQ��LQYROYHG�ZLWK�WKHVH�RUJDQLVPV��/RXLV� 'H6SDLQ� 6PLWK� DQG� ODWHU� 7KHRGRU� 5RVHEXU\� ZURWH�texts on the nonsporeforming anaerobes and the indigenous PLFURÀRUD��LQFOXGLQJ�DQDHUREHV��,�PHW�'U�/��'6�6PLWK�DQG�had a very enjoyable conversation with him. The French, DQG� WR�D� OHVVHU�H[WHQW��*HUPDQV�KDG�DUWLFOHV�RQ�DQDHUREHV�LQ� WKH�����V�DQG� WKH�%ULWLVK�D� OLWWOH� ODWHU�� ,�ZDV�DEVROXWHO\�amazed on how much was known back then about both an-aerobic bacteriology and also anaerobic infections. In my HDUO\�GD\V�DW� WKH�9$�+RVSLWDO� �WKHQ�NQRZQ�DV�:DGVZRUWK�9$���,�ZDV�FDXJKW�XS�LQ�UXQQLQJ�WKH�,QIHFWLRXV�'LVHDVH�DQG�3XOPRQDU\�'LVHDVH�6HFWLRQV�DQG�VWHHULQJ�D�+RVSLWDO�,QIHF-tion Committee.

,�¿QDOO\�UHDOL]HG�WKDW�,�ZDV�RYHUORRNLQJ�D�JROG�PLQH�RI�LQ-formation by not studying anaerobic infections and bowel ÀRUD�LQWHQVLYHO\��DQG�PHQGHG�P\�ZD\V��$QG�,�JRW�EUDVK�DQG�made efforts to meet more people who had been working with anaerobes, many in various meetings, and some that I made a point to visit during travels. I was warmly welcomed E\�+HQUL�%HHUHQV�RI�/LOOH��)UDQFH��ZKR�KDG�ZULWWHQ�D�QLFH�monograph on anaerobic bacteria with some clinical infor-PDWLRQ��,�ZDV�SULYLOHJHG�WR�PHHW�$QGUH�3UpYRW��WKH�PDVWHU�

IURP�3DULV��ZKR�ZURWH�FRXQWOHVV�DUWLFOHV��PRQRJUDSKV��DQG�ERRNV��+H�ZDV�LQ�LOO�KHDOWK�WKHQ�DQG�GLG�QRW�ZLVK�WR�VSHDN�(QJOLVK�DOWKRXJK�KH�NQHZ�LW�TXLWH�ZHOO��VR�,�VWUXJJOHG�ZLWK�P\�UXGLPHQWDU\�)UHQFK��+H�ZDV�YHU\�SOHDVDQW��,W�LV�LQWHUHVW-ing to note that this leader in anaerobic bacteriology never LVRODWHG�DQ\�RI� WKH�SLJPHQWHG�*UDP�VWDLQ�QHJDWLYH�DQDHUR-bic bacilli because he did not use blood or hemoglobin in KLV�PHGLD��,�PHW�7UHYRU�:LOOLV�RI�WKH�8.�ZKRVH�ERRN��Clos-tridia of Wound Infection� LV�D�FODVVLF��2WKHUV�IURP�WKH�8.�who I have met in more recent years include Brian Duerden, +DURXQ�6KDK�� DQG�6DKHHU�*KDUELD�� DOO� OHDGHUV� LQ� WKH�¿HOG�RI�DQDHUREHV��SOXV�PDQ\�RWKHUV�WRR�QXPHURXV�WR�PHQWLRQ���,YDQ� +DOO�� ZKR� GHVFULEHG�&ORVWULGLXP� GLI¿FLOH� and many other clostridia, contacted me regarding his wife who had advanced cancer and disturbing foul-smelling discharges IURP�GHFXELWXV�XOFHUV��+H�IHOW�VKH�KDG�VHFRQGDU\�LQIHFWLRQ�with anaerobes but was unable to isolate any clostridia. I suggested that she might have infection with nonsporeform-ing anaerobes and that the odor might be controlled by the use of metronidazole. I had the opportunity to meet him not ORQJ� DIWHU� WKDW� DQG� HQMR\HG�KLV� FRPSDQ\� D� JUHDW� GHDO��+H�was elderly at that time, but he was quite tall and had perfect posture, a most imposing man.

2YHU� WKH�FRXUVH�RI�P\�H[SHULHQFH�DW�:DGVZRUWK�� ,�SDUWLFL-SDWHG�LQ�WUDLQLQJ�RI�VRPH����FOLQLFDO�LQIHFWLRXV�GLVHDVH�)HO-lows, microbiologists, and visiting scientists. Included was one obstetrics/gynecology faculty member, a general sur-geon, a head and neck surgeon, and a pediatrician.

Sydney Finegold (third from the right on the back row) surrounded by his laboratory crew in the 1970s.

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174

A little kid from Far Rockaway grows up

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The bulk of my research dealt with anaerobic bacteria and DQDHURELF�LQIHFWLRQV�DQG�WKH�PDNHXS�RI�WKH�ERZHO�ÀRUD�DQG�its role in disease. The following summarizes some of the projects we have undertaken in my laboratory.

(DUO\�RQ��ZKHQ�-RKQ�%DUWOHWW�ZDV�D�)HOORZ�LQ�P\�JURXS��ZH�did a lot of work on the role of anaerobes in various pleuro-SXOPRQDU\�LQIHFWLRQV�±�DVSLUDWLRQ�SQHXPRQLD��OXQJ�DEVFHVV��and pleural empyema and clearly established the importance of a variety of anaerobes in these entities. The empyema patients were no problem in terms of specimen collection �MXVW� WKRUDFHQWHVLV��� EXW� IRU� WKH� RWKHUV� -RKQ� %DUWOHWW�� ZKR�was very adept at percutaneous transtracheal aspiration and was willing to come see patients at any hour, accumulated a great deal of good clinical and microbiologic data on aspira-tion pneumonia and lung abscess, as well as empyema.

2XU� JURXS��ZLWK� FROODERUDWRUV�� KDV� SXEOLVKHG� D� ODERUDWRU\�manual for clinical anaerobic bacteriology, now in its sixth HGLWLRQ��2XU�VWXGLHV��WRJHWKHU�ZLWK�'U�5REHUW�%HQQLRQ��KDYH�included extensive analysis of the bacteriology of appendi-citis. In the case of gangrenous and perforated appendicitis, ZH� IRXQG� DQ� DYHUDJH�RI� ���RUJDQLVPV� ��� DQDHURELF� DQG���DHURELF��SHU�VSHFLPHQ�±�PDQ\�PRUH�WKDQ�SUHYLRXV�LQYHVWLJD-tors had noted. We also studied the antimicrobial suscepti-bility of the isolates and the clinical outcome, evaluated the response to various antibacterial regimens and compared the microbiology of acute and complicated appendicitis. In these studies, we demonstrated the superiority of culture of WKH�DSSHQGL[�WLVVXH�RYHU�FXOWXUH�RI�SHULWRQHDO�ÀXLG�

During the studies on appendicitis, we encountered a novel VSHFLHV� RI� DQDHURELF� *UDP�VWDLQ�QHJDWLYH� EDFLOOXV� ZKLFK�we named Bilophila wadsworthia. This organism was the third most common anaerobe we encountered in gangrenous and perforated appendicitis despite being a relatively minor FRPSRQHQW�RI�WKH�LQGLJHQRXV�ERZHO�ÀRUD��VXJJHVWLQJ�WKDW�LW�

KDV�VLJQL¿FDQW�YLUXOHQFH��:H�DQG�RWKHUV�KDYH�VXEVHTXHQWO\�encountered this organism frequently in a wide variety of FOLQLFDOO\�VLJQL¿FDQW�LQIHFWLRQV��PDQ\�RI�ZKLFK�ZHUH�TXLWH�VHULRXV� �H�J�� EDFWHUHPLD�� HPS\HPD�� SXUXOHQW� DUWKULWLV���2I�LQWHUHVW��LQ�WKH�DSSHQGLFLWLV�VWXG\��RXU�UHVHDUFK�ODERUDWRU\��LQ�������ZDV�XQDEOH�WR�LGHQWLI\�IXOO\�FHUWDLQ�DQDHURELF�*UDP�VWDLQ�QHJDWLYH�DQG�*UDP�VWDLQ�SRVLWLYH�URGV�RFFXUULQJ�LQ�DO-most one-third of patients, using only phenotypic tests.

We have also collaborated with Dr Bennion, Dr David Talan, and others on a study of the bacteriology of skin and soft tis-VXH�LQIHFWLRQV�LQ�LQWUDYHQRXV�GUXJ�XVHUV�����VSHFLPHQV��DQG�RWKHUV�ZLWK�QR�VXFK�KLVWRU\�����VSHFLPHQV�������RI�WKHVH�LQ-fections were closed lesions that were sampled by aspiration with a syringe and needle. Staphylococcus aureus and the

“Streptococcus milleri group” were prominent aerobes in ERWK� JURXSV� RI� SDWLHQWV�� FRDJXODVH�QHJDWLYH� VWDSK\ORFRFFL�and Streptococcus pyogenes were also prominent in the non-,9'8�JURXS��7KH�DQDHURELF�ÀRUD�GLIIHUHG�LQ�WKH�WZR�JURXSV�DV�ZHOO��7KH�,9'8�JURXS�PRVW�FRPPRQO\�KDG�Fusobacte-rium nucleatum, pigmented Prevotella species, Peptostrep-tococcus micros, Actinomyces odontolyticus, and Veillonella VSHFLHV��ZKHUHDV�WKH�QRQ�,9'8�JURXS�KDG�SULPDULO\�Pepto-streptococcus species, Bacteroides�VSHFLHV��DQG�*UDP�VWDLQ�positive anaerobic bacilli. In the overall patient population, ���� RI� VXEMHFWV� KDG� RQH� RU� PRUH� `-lactamase-producing organism.

:H�KDYH�VWXGLHG�WKH�ÀRUD�RI����ZRXQG�LQIHFWLRQV�IROORZLQJ�KHDG�DQG�QHFN�FDQFHU�VXUJHU\��3UHRSHUDWLYH�DHURELF�FXOWXUHV�of the oropharynx and skin were of no value in predicting OLNHO\�LQIHFWLQJ�RUJDQLVPV�SRVWRSHUDWLYHO\��3RVWRSHUDWLYHO\��_-hemolytic streptococci of various types, Staphylococcus

Sydney Finegold at the VA Middleton Award ceremony in Washington, D.C., in 1984. Front row: Joyce (son Mike's wife), Sid and Mary; back row: sons Joe and Mike, daughter Pat and her husband, Michael.

Sid (second from left) with cousin Sylvia, Mary, his Dad, and brother Harold. Photo taken in 1975.

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175

Sydney M. Finegold

The Bulletin of BISMiS

aureus and Staphylococcus epidermidis were the principal LVRODWHV�DPRQJ�WKH�DHUREHV��3ULQFLSDO�DPRQJ�WKH�ODUJH�JURXS�of anaerobes recovered were several species of Peptostrep-tococcus��PRVW�RI�ZKLFK�KDYH�VXEVHTXHQWO\�EHHQ�SODFHG�LQ�other genera), Fusobacterium nucleatum, and several spe-cies of Bacteroides �DOVR�PRVWO\� UHFODVVL¿HG�DV�Prevotella or Porphyromonas subsequently), including Bacteroides melaninogenicus and Bacteroides oralis��2QH�RI�WKH�Pepto-streptococcus species was renamed Finegoldia magna by a %ULWLVK�JURXS�DQG�WKHUHLQ�OLHV�D�WDOH��0\�FRXVLQ��DQG�FORVH�IULHQG���0LOWRQ� )LQHJROG�� LV� D� KLJKO\� UHFRJQL]HG� SHGLDWULF�SDWKRORJLVW�DW�7H[DV�&KLOGUHQ¶V�+RVSLWDO�DQG�%D\ORU�8QLYHU-VLW\�6FKRRO�RI�0HGLFLQH�LQ�+RXVWRQ�ZKHUH�KH�ZDV�IRUPHUO\�&KDLUPDQ�RI�WKH�'HSDUWPHQW��2Q�RQH�RFFDVLRQ�ZKHQ�,�ZDV�JLYLQJ� D� OHFWXUH� DW� KLV�PHGLFDO� VFKRRO�� WKH�'HDQ� �ZKR� UH-DOO\�OLNHV�0LOWRQ�DQG�LV�D�FORVH�IULHQG�RI�KLV��LQ�LQWURGXFLQJ�me mentioned that I had this bacterium Finegoldia magna QDPHG�DIWHU�PH�DQG�ORRNHG�RYHU�DW�0LOWRQ�DQG�VDLG��³+RZ�FRPH�\RX�DUH�RQO\�µ)LQHJROGLD�PLQLPD¶´"�0LOWRQ�DQG�,�ZHUH�both embarrassed by this, but it was all in good fun.

$� SDSHU� IURP� RXU� ODERUDWRU\� FRYHUHG� D� PXOWLFHQWHU� VWXG\�of the bacteriology of chronic bacterial maxillary sinusitis LQ�����HYDOXDEOH�DGXOWV��7KHUH�ZHUH����DHURELF�DQG����DQ-aerobic pathogens recovered. The prevalent anaerobes were Prevotella spp., anaerobic streptococci, and Fusobacterium spp. Recurrences of disease following antimicrobial therapy were twice as frequent with anaerobes as with aerobes when

FRXQWV� RI� DQDHUREHV�ZHUH� ����PO� RU� JUHDWHU��$�SDWKRJHQLF�role for Granulicatella in chronic sinusitis was documented IRU�WKH�¿UVW�WLPH�

$�QRYHO�VSHFLHV�WKDW�ZH�KDYH�GHVFULEHG�LV�Sutterella wadsworth-ensis which was “split out” of the Bacteroides� �QRZ�Cam-pylobacter) gracilis�³JURXS �́�LW�ZDV�VXVSHFWHG�WR�EH�D�QRYHO�species because of its unique resistance to metronidazole.

We studied what we are calling the Clostridium clostridi-oforme “group”. In the course of studies we are carrying RXW� LQ� UHODWLRQ� WR� WKH�SRVVLEOH� UROH�RI� LQWHVWLQDO�PLFURÀRUD�LQ�DXWLVP��ZH�HQFRXQWHUHG�DQ�RUJDQLVP�WKDW�ZH�LGHQWL¿HG�DV�Clostridium clostridioforme� LQ�DXWLVWLF�VXEMHFWV¶�IHFDO�ÀRUD�WKDW�ZDV�QRW�SUHVHQW� LQ�FRQWURO�FKLOGUHQ¶V� IHFDO�ÀRUD��ODWHU��molecular studies proved that it was also present in the con-WUROV��EXW�LQ�VLJQL¿FDQWO\�VPDOOHU�QXPEHUV���&DUHIXO�VWXGLHV�on this organism demonstrated certain phenotypic differenc-es from Clostridium clostridioforme� DQG� ��6� U'1$� VWXG-LHV�VXJJHVWHG�D�SRVVLEOH�QRYHO�VSHFLHV� WKDW�ZDV�FRQ¿UPHG�E\�'1$±'1$�UHDVVRFLDWLRQ�VWXGLHV��:H�KDYH�QDPHG� WKLV�organism Clostridium bolteae��ZH�KDYH�DOVR�HQFRXQWHUHG�LW�in bacteremia and in intra-abdominal abscess secondary to SHUIRUDWHG� DSSHQGLFLWLV�� 5HFHQWO\�� D� IRUPHU� 3RVW�'RFWRUDO�)HOORZ�LQ�WKH�8&/$�9$�&OLQLFDO�0LFURELRORJ\�)HOORZVKLS�3URJUDP�FDOOHG�P\�DWWHQWLRQ�WR�D�IDWDO�FDVH�RI�VHSVLV�GXH�WR�Clostridium clostridioforme��ZH� DVNHG� WR� VWXG\� WKH� RUJDQ-LVP� UHFRYHUHG�� DQG� ��6� U'1$� VWXGLHV� SURYHG� LW� WR� EH�� LQ-

The Finegold laboratory crew ca. 1990. Seated, left to right: Chengxu Liu, Yuli Song, and Maureen McTeague; stand-ing, left to right: Paula Summanen Carlson, Sydney Finegold, Tom Tomzynski, Hana Wexler, and Denise Molitoris.

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176

A little kid from Far Rockaway grows up

The Bulletin of BISMiS

VWHDG��D�UHODWHG�RUJDQLVP�UHFHQWO\�GHVFULEHG�IURP�WKH�8.�DV�Clostridium hathewayi��6R��KHUH�DUH� WZR�GLIIHUHQW�YLUXOHQW�organisms that can readily be confused with Clostridium clostridioforme WKDW� ZHUH� FRQ¿UPHG� DV� GLIIHUHQW� E\� ��6�U'1$�VWXGLHV��7KH�Clostridium clostridioforme “group” is a XQLTXH�JURXS��WKH�PHPEHUV�RI�ZKLFK�DOO�VKRZ�*UDP�VWDLQ�negative relatively thin rods with tapered ends and colonies ZKLFK� VKRZ� D� FU\VWDOOLQH� LQWHUQDO� VWUXFWXUH� �Clostridium clostridioforme�ZDV�FODVVL¿HG�DV�DQ�DQDHURELF�*UDP�VWDLQ�negative rod related to Fusobacterium in the older litera-WXUH���$OO� WKUHH�PDMRU� VSHFLHV� LQ� WKLV�JURXS�DUH� VLJQL¿FDQW�pathogens, having been recovered from a number of serious infections, including bacteremia. The source of all these or-ganisms appears to be the lower bowel.

In the past few years, we have learned or developed vari-RXV� PROHFXODU� PHWKRGV�� VXFK� DV� ��6� U'1$� VHTXHQFLQJ��PXOWLSOH[� 3&5�� VSDFHU�UHJLRQ� �65��3&5� SDWWHUQ� DQDO\VLV��5HS�3&5��'**(�� DQG� UHDO�WLPH�3&5�� IRU� UDSLG� DQG� DFFX-UDWH� LGHQWL¿FDWLRQ� RI� FOLQLFDOO\� LPSRUWDQW� DQDHURELF� EDFWH-ULD�� ,Q�RQH�RI�RXU� UHFHQW� VWXGLHV�RQ�*UDP�SRVLWLYH� DQDHUR-ELF� FRFFL� �*3$&��� ZH� HYDOXDWHG� WKH� XWLOLW\� RI� ��6� U'1$�sequencing as a means of identifying clinically important *3$&�E\�VHTXHQFLQJ����W\SH�VWUDLQV�RI�HVWDEOLVKHG�*3$&�VSHFLHV� DQG� ���� FOLQLFDO� LVRODWHV� ZKLFK� KDG� EHHQ� VWXGLHG�RQO\�E\�SKHQRW\SLF�WHVWV��%DVHG�RQ�WKH�VHTXHQFHV�RI�WKH����W\SH�VWUDLQV�REWDLQHG�LQ�WKLV�VWXG\����������������RI�FOLQL-FDO�LVRODWHV�ZHUH�DFFXUDWHO\�LGHQWL¿HG�WR�VSHFLHV�OHYHO��ZLWK�WKH�RWKHU����FOLQLFDO�VWUDLQV�UHYHDOLQJ�QLQH�XQLTXH�VHTXHQFHV�that may represent eight novel species. This is in contrast WR�SKHQRW\SLF�LGHQWL¿FDWLRQ��E\�ZKLFK�RQO\�����RI�LVRODWHV�ZHUH�FRUUHFWO\�LGHQWL¿HG�WR�VSHFLHV�OHYHO��:H�KDYH�GRQH���6�U'1$�VHTXHQFH�DQDO\VLV�RQ�PRUH� WKDQ������FOLQLFDOO\� LP-SRUWDQW�DQDHURELF�EDFWHULD� �HLWKHU� IURP�RXU�FOLQLFDO� LVRODWH�

collection or our type strain collection), and compared the sequence data with those in public databases. We have con-tributed our clean sequence data to public databases, and ZH�DUH�HVWDEOLVKLQJ�D���6�U51$�JHQH�VHTXHQFH�GDWDEDVH�IRU�anaerobic bacteria for our own studies. Furthermore, based RQ�WKH�VHTXHQFH�LQIRUPDWLRQ��WZR�PXOWLSOH[�3&5�VFKHPHV�ZHUH�GHYHORSHG�IRU�UDSLG�DQG�DFFXUDWH�LGHQWL¿FDWLRQ�RI�WHQ�Bacteroides fragilis� JURXS� VSHFLHV� DQG� ��� *3$&� VSHFLHV�originally in the genus Peptostreptococcus, respectively. In one study, we reported a rapid and reliable two-step multi-SOH[�3&5�DVVD\�WR�LGHQWLI\�WKH�WKHQ�WHQ�Bacteroides fragilis group species. The primers were designed from nucleotide VHTXHQFHV�RI�WKH���6�U51$��WKH���6±��6�U51$�LQWHUJHQLF�VSDFHU� UHJLRQ�� DQG�SDUW�RI� WKH���6� U51$�JHQH��7KH�HVWDE-OLVKHG� WZR�VWHS�PXOWLSOH[� 3&5� LGHQWL¿FDWLRQ� VFKHPH�ZDV�DSSOLHG� WR� WKH� LGHQWL¿FDWLRQ�RI�����FOLQLFDO� LVRODWHV�RI� WKH�Bacteroides fragilis� JURXS� WKDW� ZHUH� SUHYLRXVO\� LGHQWL¿HG�to species level by phenotypic tests. The new scheme was PRUH� DFFXUDWH� WKDQ� SKHQRW\SLF� LGHQWL¿FDWLRQ�� ZKLFK� ZDV�DFFXUDWH� RQO\� ������RI� WKH� WLPH�� ,Q� DQRWKHU� VWXG\��ZH� UH-SRUWHG�D�WZR�VWHS�PXOWLSOH[�3&5�DVVD\�WR�LGHQWLI\����*3$&�species originally in the genus Peptostreptococcus. The LGHQWL¿FDWLRQ�REWDLQHG�IURP�PXOWLSOH[�3&5�DVVD\V�VKRZHG������DJUHHPHQW�ZLWK���6�U'1$�VHTXHQFLQJ�LGHQWL¿FDWLRQ��EXW�RQO\���������������DJUHHG�ZLWK�LGHQWL¿FDWLRQ�REWDLQHG�E\�SKHQRW\SLF�WHVWV��7KHVH�PXOWLSOH[�3&5�VFKHPHV�WKDW�ZH�have established are simple, rapid, and reliable methods for WKH� LGHQWL¿FDWLRQ� RI� WKHVH� WZR� JURXSV� RI� DQDHUREHV��7KH\�will permit more accurate assessment of the role of various Bacteroides fragilis�JURXS�DQG�*3$&�PHPEHUV�LQ�LQIHFWLRQ�and of the degree of antimicrobial resistance in each of the group members.

2XU�JURXS�KDV�KDG�D� ORQJ�VWDQGLQJ� LQWHUHVW� LQ�ERZHO�ÀRUD��

UCLA Clinical Laboratory group ca. 2005. From left to right: Sydney Finegold, Jim Miller, Liz Wagar, Matt Goetz, Dave Bruckner, Maurice White, and Marie-Claire Rowlinson.

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Sydney M. Finegold

177The Bulletin of BISMiS

2XU�VWXGLHV�KDYH�EHHQ�SXEOLVKHG�LQ�YDULRXV�SHHU�UHYLHZHG�journals at different times and then summarized in depth in a FKDSWHU�SXEOLVKHG�LQ�������LQ�Encyclopedia of Microbiology, (OVHYLHU��SS�����±������:H�KDYH�DOVR�SXEOLVKHG�D�VXPPDU\�of our own data and a literature review on clostridia in the KXPDQ�JXW�ÀRUD��&KDSWHU���RI�Clostridia in Gastrointestinal Disease��HGLWHG�E\�6�3��%RUULHOOR��������DQG�ZURWH�WKH�VHF-tion on Clostridium� LQ� WKH��VW�HGLWLRQ�RI�Bergey’s Manual of Systematic Bacteriology. We wrote the Bacteroides, Alis-tipes, and Porphyromonas� VHFWLRQV� IRU� WKH� �QG� HGLWLRQ� RI�Bergey’s Manual of Systematic Bacteriology, and the “Clos-tridium´� DQG� ³$QDHURELF� *UDP�SRVLWLYH� &RFFL´� VHFWLRQV�IRU�WKH��WK�HGLWLRQ�RI�WKH�Manual of Clinical Microbiology DQG�WKH�³$QDHURELF�*UDP�SRVLWLYH�&RFFL´�IRU�WKH���WK�HGL-tion. We have developed an excellent selective medium for clostridia and have been involved in a number of studies of�&ORVWULGLXP�GLI¿FLOH-induced antimicrobial-agent related pseudomembranous colitis, including the toxins of this or-ganism, and bacterial interference between this bacterium DQG�QRUPDO�IHFDO�ÀRUD��2WKHU�VWXGLHV�LQFOXGH�WKH�LPSRUWDQFH�of anaerobic bacteria in blind loop syndrome and in d-lactic acidosis.

2XU�JURXS�KDG�WKH�RSSRUWXQLW\�WR�VWXG\�WZR�DGXOW�SDWLHQWV�with d-lactic acidosis. The conditions predisposing to this entity were extensive small bowel resection following mes-enteric infarction in one patient, and jejunoileal bypass in the second. In addition to acidosis, patients with this prob-OHP�PDQLIHVW� VLJQL¿FDQW� SV\FKLDWULF� DQG� QHXURORJLF� DEQRU-PDOLWLHV��6WRRO�FXOWXUHV�RQ�WKHVH�WZR�SDWLHQWV�VKRZHG�KLJK�FRXQWV� DQG� D� PDUNHG� SUHGRPLQDQFH� RI� *UDP�VWDLQ�SRVL-WLYH�� QRQVSRUHIRUPLQJ� EDFWHULD�� SULQFLSDOO\� EL¿GREDFWHULD��lactobacilli,and Eubacterium. In sharp contrast with the normal situation, neither patient had Bacteroides present in FRXQWV�DERYH����/g of stool. d�/DFWDWH�ZDV�SURGXFHG�IURP�

DSSURSULDWH�PHGLD� LQ� VLJQL¿FDQW� DPRXQWV� E\�PDQ\� RI� WKH�bacteria isolated from the patients, but not from any bacte-ria recovered from normal control patients. The patients had a good clinical response and a normalization of their stool ÀRUD�RQ�RUDO�YDQFRP\FLQ�WKHUDS\�

We have done extensive studies on the gut bacteriology of patients with jejunoileal bypass used for the treatment of PRUELG�REHVLW\��(LJKW�SDWLHQWV�KDG�VWXGLHV�DW�WKH�WLPH�RI�WKH�surgery, but before the bypass procedure was done, by aspi-UDWLRQ�RI�ERZHO�FRQWHQWV��1R�DQWLELRWLFV�ZHUH�XVHG�LQ�SUHS-DUDWLRQ�RI� WKH�SDWLHQWV� IRU�VXUJHU\�� ,Q�¿YH�SDWLHQWV�� MHMXQDO�specimens were sterile and the other three had low counts RI� D� SUHGRPLQDQWO\� DHURELF� ÀRUD�� ,OHDO� FRQWHQWV� \LHOGHG�variable but usually higher counts than in the jejunum and there were similar numbers of aerobes and anaerobes. In four patients whose bypass had been established and who required a subsequent surgery for complications of the by-pass procedure, it was possible to obtain specimens again for comparison. Contents of the functioning small bowel LQ�WKUHH�RI�WKH�SDWLHQWV�VKRZHG�FRXQWV�RI����±���/ml and the ÀRUD�UHVHPEOHG�WKDW�RI�IHFHV��)RXU�VSHFLPHQV�IURP�WKH�H[-cluded loops were colonized with fecal organisms and the FRXQWV� UDQJHG� IURP� ������ WR� �����/ml. Thus, in jejunoileal bypass both the functioning small bowel and the excluded ORRS�EHFRPH�FRORQL]HG�ZLWK�FRORQLF�ÀRUD��7KH�HQWHURSDWK\�and systemic complications, including hepatosteatosis, im-proved on metronidazole, an antimicrobial active virtually only against anaerobic bacteria.

,Q�������%ROWH�SXEOLVKHG�DQ�LQWULJXLQJ�K\SRWKHVLV�WKDW�Clos-tridium tetani �RU� RWKHU� EDFWHULD� LQ� WKH� JXW��PLJKW� SOD\� D�UROH�LQ�ODWH�RQVHW�DXWLVP��2Q�WKH�EDVLV�RI�WKLV�K\SRWKHVLV��DQ�open-label trial of oral vancomycin was contemplated. Dr 5LFKDUG�6DQGOHU��D�SHGLDWULF�JDVWURHQWHURORJLVW� LQ�&KLFDJR��

Sid with one of his special Fellow trainees, John Bartlett, who is currently Professor at Johns Hopkins (2008).

Sid with one of his former Fellows, Ellie Goldstein.

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A little kid from Far Rockaway grows up

178 The Bulletin of BISMiS

ZDV�ZRUNLQJ�ZLWK�(OOHQ�%ROWH�DW�WKDW�WLPH��KH�FDOOHG�PH�WR�see if I would work with them on this proposed study to pro-vide suggestions re. antimicrobials and to do bacteriologic studies on the stools of the patients before and after treat-PHQW��,Q�WKLV�VWXG\��SDWLHQWV�UDQJHG�IURP����WR����PRQWKV�LQ�DJH��%\�WKH�&KLOGKRRG�$XWLVP�5DWLQJ�6FDOH��VL[�FKLOGUHQ�met the criteria for severe autism, two for moderate autism, DQG�WKUHH�IRU�PLOG�DXWLVP��9DQFRP\FLQ�ZDV�JLYHQ�RUDOO\�IRU���ZHHNV��7KHUH�ZDV� JRRG� HYLGHQFH� RI� D� FOLQLFDO� UHVSRQVH�LQ� �� RI� ��� HYDOXDEOH� FKLOGUHQ�ZLWK� ODWH�RQVHW� DXWLVP��7KH�response involved improved behavior, communication, and social skills. Behavior and communication analog rating scales were not done in blinded fashion, but paired video-WDSHV�����PLQXWHV�LQ�D�SOD\URRP�HQYLURQPHQW��PDGH�EHIRUH�and during therapy were evaluated in blinded fashion by a clinical child psychologist who had no personal contact with WKH� FKLOGUHQ�� 3DWLHQWV� UHODSVHG� WR� WKHLU� SUH�WUHDWPHQW� VWDWH�within a few weeks of discontinuation of the vancomycin.

The second study that we completed on autistic children was entirely microbiologic in nature. There were two parts to this VWXG\������IHFDO�VWXGLHV��XVLQJ�SUH�WUHDWPHQW�VSHFLPHQV�IURP�the above study plus normal controls) with cultures designed SULPDULO\�WR�UHFRYHU�FORVWULGLD��DQG�����VWXGLHV�RI�WKH�XSSHU�gastrointestinal contents. In both parts of the study, both au-WLVWLF�FKLOGUHQ�DQG�FRQWURO�FKLOGUHQ��DJH��DQG�VH[�PDWFKHG��FRQWULEXWHG�VSHFLPHQV��,Q�WKH�FDVH�RI�WKH�IHFDO�ÀRUD�VWXGLHV��the decision was made to focus on clostridia because of the HQRUPRXV�DPRXQW�RI�ZRUN�LQYROYHG�LQ�GRLQJ�WRWDO�ÀRUD�VWXG-LHV� E\� FRQYHQWLRQDO�PLFURELRORJLF�PHWKRGV�� ,GHQWL¿FDWLRQ�of isolates was done both by conventional phenotypic tests DQG�E\���6�U51$�JHQH�VHTXHQFLQJ��:H�IRXQG����VSHFLHV�RI�Clostridium�LQ�WKH�VWRROV�RI����DXWLVWLF�FKLOGUHQ�DQG����LQ�WKH�stools of the eight control children studied. The geometric PHDQ�FRXQW�RI�FORVWULGLD�ZDV��� ORJ�KLJKHU� LQ� WKH�VWRROV�RI�DXWLVWLF�FKLOGUHQ�WKDQ�LQ�WKH�FRQWUROV��$OWRJHWKHU��WKHUH�ZHUH����GLIIHUHQW�VSHFLHV�RI�FORVWULGLD�HQFRXQWHUHG�

,Q� WKH� XSSHU� *,� SDUW� RI� WKH� VWXG\�� VSHFLPHQV� IURP� VHYHQ�children with autism and four control children were studied. The cultures were set up to identify any bacterium or yeast WKDW�ZDV�SUHVHQW��7KH�JDVWULF�S+�ZDV�HOHYDWHG�LQ�WZR�RI�IRXU�FKLOGUHQ�ZLWK�DXWLVP� IRU�ZKRP�JDVWULF�S+�ZDV�PHDVXUHG��WKHVH�FKLOGUHQ�KDG�QRW�EHHQ�RQ�+� blockers or proton pump inhibitors. The two children with hypochlorhydria had the PRVW� SURIXVH� PLFURELDO� ÀRUD� SUHVHQW�� 7KH� PRVW� VWULNLQJ�microbiologic result was that nonsporeforming anaero-bic and microaerophilic bacteria were totally absent from specimens from the control children. In contrast, of the four children with autism whose specimens yielded growth, such RUJDQLVPV�ZHUH�SUHVHQW��WZR�FKLOGUHQ¶V�VSHFLPHQV�KDG��±��GLIIHUHQW�VSHFLHV��$PRQJ�WKH�WKUHH�VXEMHFWV�ZLWK�DXWLVP�ZKR�

had few or no organisms recovered from their specimens, one had never had diarrhea or constipation and a second had had multiple courses of antimicrobials for recurrent sinus-itis, but none in the month prior to the sampling.

The above fecal specimens were tested subsequently using UHDO�WLPH�3&5� �57�3&5���ZH� IRXQG� WKDW� FHOO� FRXQW� GLIIHU-ences of Clostridium bolteae and Clostridium clusters I and ;,��EXW�QRW�FOXVWHU�;,9�DE��ZHUH�VWDWLVWLFDOO\�VLJQL¿FDQW�EH-tween autistic and age- and sex-matched control children �KLJKHU�EDFWHULDO�FRXQWV�LQ�DXWLVWLF�FKLOGUHQ��

:H� PDGH� D� ELJ� VWHS� IRUZDUG� ZKHQ� ZH� MRLQHG� ZLWK� 6FRW�'RZG� RI� /XEERFN�� 7H[DV�� WR� HPSOR\� S\URVHTXHQFLQJ�� D�rapid-throughput method that permits examining many more samples in a given time than with cultural methods. /LNH�RWKHU�PROHFXODU�PHWKRGV� VXFK�DV� UHDO�WLPH�3&5�� WKH�RUJDQLVP�FDQ�EH�LGHQWL¿HG�E\�PDWFKLQJ�WKH�'1$�ZLWK�UHDG-ily available databases, but it cannot be recovered for other studies such as virulence for animals and antimicrobial sus-FHSWLELOLW\�WHVWLQJ��+RZHYHU��LW�LGHQWL¿HV�PDQ\�RI�WKH�RUJDQ-LVPV� WKDW� DUH� XQFXOWLYDEOH�� JLYHV� D� IDLUO\� URXJK�TXDQWL¿FD-tion, and with the proper analysis provides a much broader picture than is feasible with cultural techniques. We were DEOH�WR�GHWHUPLQH�WKDW�WKH�IHFDO�ÀRUD�RI�DXWLVWLF�VXEMHFWV�ZDV�abnormal when compared to normal controls.

Comparing the principal phyla detected by pyrosequencing, ZH�QRWH� WKDW� WKH�QRUPDO�FRQWUROV�KDG�����Firmicutes and ����Bacteroidetes�ZKHUHDV�WKH�FRUUHVSRQGLQJ�¿JXUHV�ZHUH�UHYHUVHG�IRU�WKH�DXWLVWLF�VXEMHFWV�±�����IRU�WKH�Firmicutes DQG�����IRU�WKH�Bacteroidetes. This is a striking example of DQ�DEQRUPDO�IHFDO�ÀRUD��6LEOLQJV�ZHUH�LQ�EHWZHHQ��VXJJHVW-ing that they may have acquired some abnormality of their ÀRUD�IURP�WKHLU�DVVRFLDWLRQ�ZLWK�WKHLU�DXWLVWLF�VLEOLQJ��7KLV��if documented, would have profound epidemiological sig-QL¿FDQFH�)LQDOO\��IURP�WKLV�S\URVHTXHQFLQJ�VWXG\��ZH�ZHUH�able to suspect that Desulfovibrio and Bacteroides vulgatus might play a key role in regressive autism because they were VWDWLVWLFDOO\�VLJQL¿FDQWO\�PRUH�SUHYDOHQW�LQ�DXWLVWLF�VXEMHFWV�than in controls. We proceeded to do selective culture and UHDO�WLPH�3&5�IRU�WKHVH�WZR�W\SHV�RI�RUJDQLVPV�RQ�DOO�RI�WKH�stools studied previously by pyrosequencing. Bacteroides vulgatus� WXUQHG�RXW�QRW� WR�VKRZ�DQ\�VLJQL¿FDQW�GLIIHUHQFH�between the stool samples from both groups, but the genus Desulfovibrio DQG� LWV�¿YH� VSHFLHV� IRXQG� LQ� WKH�KXPDQ�JXW�VKRZHG� VWDWLVWLFDOO\� VLJQL¿FDQW�GLIIHUHQFHV�� LQGLFDWLQJ� WKDW�Desulfovibrio may be a key bug in regressive autism.

$�UHFHQW�SDSHU�RI�RXUV��DFFHSWHG�IRU�SXEOLFDWLRQ�DV�SDUW�RI�D�symposium, provides information on susceptibility of De-sulfovibrio species to various antimicrobials. These data are

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179

Sydney M. Finegold

The Bulletin of BISMiS

of interest in terms of potential therapy of regressive autism and also in terms of the pathogenesis of the disease and pos-sibilities for prevention. The data must be interpreted with respect to levels of the various drugs obtained in the bowel. 3HQLFLOOLQV�DQG�FHSKDORVSRULQV��DV�ZHOO�DV�WULPHWKRSULP�VXO-IDPHWKR[D]ROH��DQG�ÀXRURTXLQRORQHV�ZKLFK�VKRXOG�QRW�EH�used in young children anyway beause of potential toxicity) may well predispose to regressive autism in consideration of the resistance of Desulfovibrio to them and their impact RQ� WKH� ERZHO� ÀRUD� ZKLFK� ZRXOG� SHUPLW� WKLV� RUJDQLVP� WR�grow to larger numbers as the competition is reduced. The data also indicate other drugs that might be used to treat ear infections, for example, with less risk of major bowel ÀRUD� FKDQJHV� RI� WKH� W\SH� GLVFXVVHG�� LQFOXGHG� ZRXOG� EH�GUXJV�VXFK�DV�WKH�PDFUROLGHV�DQG�WHWUDF\FOLQHV��$]WUHRQDP��a monobactam antibiotic that has been used for decades and was supplanted by newer drugs is now being used again in VHOHFWHG� VLWXDWLRQV� ZKHUH� *UDP�VWDLQ�QHJDWLYH� EDFLOOL� DUH�resistant to many or most other drugs. This drug is not sup-posed to be active against anaerobes but it is moderately ac-tive against Desulfovibrio. It is susceptible to destruction by `�ODFWDPDVHV��ZKLFK�Desulfovibrio produces itself) but oth-erwise has a number of good features for this setting such as not being absorbed to any extent when given orally, and it is well tolerated. Combining it with sulbactam, a `-lactamase inhibitor, provides synergistic activity while eliminating the threat posed by the common `-lactamases.

2WKHU� QRWDEOH� HYHQWV� GXULQJ� P\� WHUP� DW� WKH� :DGVZRUWK�9$� �QRZ�9$�0HGLFDO� &HQWHU�:/$� DQG� RWKHU� QDPHV��� LQ-

FOXGH� WKH� ELUWK� RI�P\� WKLUG� FKLOG��0LNH�� LQ� ������+H�ZDV�GXH�DURXQG�1HZ�<HDU¶V�'D\��EXW�0DU\�ZRUNHG�KDUG�LQ�RXU�garden hoping we could get another income tax deduction. $V�LW�WXUQHG�RXW��KH�ZDV�ERUQ�DW������D�P��RQ���-DQXDU\��+H�ZDV�WKH�¿UVW�EDE\�ERUQ�LQ�WKH�QHZ�\HDU�IRU�RXU�HQWLUH�0HGL-FDO�&HQWHU�DQG�ZH�ZRQ�D�IUHH�SOD\SHQ�DV�D�UHVXOW��0LNH��OLNH�-RH�DQG�3DW��KDV�EHHQ�D�UHDO�EOHVVLQJ��+H�LV�GRZQ�WR�HDUWK��really funny and punny, and lives nearby so that we play WHQQLV�GRXEOHV��DV�SDUWQHUV��DOPRVW�HYHU\�6XQGD\��,�DOVR�JHW�WR� VHH� KLP� D� ORW� RWKHUZLVH� EHFDXVH� KH¶V� VR� FORVH��+H� LV� D�WHDFKHU�DQG� WHQQLV�FRDFK�DW�9HQLFH�+LJK�6FKRRO��ZKLFK� LV�D�VKRUW�ZDON�IURP�P\�KRPH�LQ�0DULQD�'HO�5H\��$V�WHQQLV�JHWV�PRUH�GLI¿FXOW�IRU�PH��0LNH�UHDOO\�KHOSV�RXW�EHFDXVH�KH�FRYHUV�WKH�FRXUW�VR�ZHOO��$ERXW�WKH�WKLUG�VHW��,�JHW�ORRVHQHG�XS�DQG�EHFRPH�PRUH�HIIHFWLYH��0LNH�ZRUNV�IRU�PH�GXULQJ�school vacation periods, entering data into my database, get-WLQJ�KDUG�WR�¿QG�DUWLFOHV�IURP�WKH�8&/$�OLEUDU\��DQG�HYHQ�GRLQJ�HUUDQGV��ZKLFK�VDYHV�PH�D�ORW�RI�WLPH��+H�KDV�D�KHDUW�WKH�VL]H�RI�KLV�KHDG��QRW�OLWHUDOO\����KH�LV�DOZD\V�GRLQJ�WKLQJV�IRU� SHRSOH��$OWKRXJK� KH� DQG� KLV�ZLIH�� -R\FH� �ZKR� DOVR� LV�YHU\�QLFH�WR�PH��KDYH�QR�FKLOGUHQ��0LNH�LV�OLNH�D�IDWKHU�WR�many of his students, some of whose parents are divorced or who have to work two or three jobs to get by and don’t KDYH�DV�PXFK�WLPH�IRU�WKHLU�FKLOGUHQ�DV�RWKHU�SDUHQWV��+H�LV�DYDLODEOH� DQ\� WLPH� IRU� DQ\ERG\�ZKR�QHHGV�KHOS��2QH�GD\�KH� UHFHLYHG�D�FDOO�DURXQG���D�P�� IURP�RQH�RI�KLV� VWXGHQWV�who lived in a bad part of town because she felt she needed KHOS�WR�GHDO�ZLWK�KHU�SDUHQWV��+H�ZHQW�RYHU�DQG�VWUDLJKWHQHG�everything out.

0\�ZLIH�GHYHORSHG�SDQFUHDWLF�FDQFHU�DQG�PDQDJHG�WR�VXU-YLYH�IRU����PRQWKV�EHFDXVH�VKH�ZDV�VXFK�D�¿JKWHU��6KH�ZDV�playing tennis while wearing her chemotherapy infusion SXPS�� 6KH� GLHG� LQ� ������ %HFDXVH� ,� HQMR\HG�PDUULHG� OLIH�ZLWK�0DU\�VR�PXFK��,�UXVKHG�LQWR�DQRWKHU�PDUULDJH�UHODWLYH-

Marilyn Lerner (5’0”) with (from left) Sydney’s son Mike, son Joe, and grandson Chris (ranging in height from 6’4½” to 6’7”).

Marilyn and Sid in 2007.

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180

A little kid from Far Rockaway grows up

The Bulletin of BISMiS

ly soon after she died and it turned out to be a bad mistake. :H�VHSDUDWHG�DIWHU�VRPH���\HDUV�DQG�,�KDYH�MXVW�GLYRUFHG�KHU��)RUWXQDWHO\��,�PHW�D�ORYHO\�DQG�ZRQGHUIXO�ZRPDQ��0DULO\Q�/HUQHU��QRW�ORQJ�DIWHU�WKH�VHSDUDWLRQ��:H�KDYH�D�ORW�RI�IXQ�together, playing tennis, going to movies and the theater and PXVLFDO�SHUIRUPDQFHV�DV�ZHOO� DV�8&/$�EDVNHWEDOO�JDPHV��DQG�WUDYHOLQJ��6KH�LV�D�QXUVH��LV�YHU\�EULJKW�DQG�KDV�EURDG�LQWHUHVWV��6KH�YROXQWHHUV�IRU� WKH�9HQLFH�KRPHOHVV�SHRSOH¶V�clinic, plays the violin, and is involved in golf and roller VNDWLQJ��6KH�LV�DQ�H[FHOOHQW�GDQFHU��EXW�ZH�GRQ¶W�PHVK�ZHOO�ZLWK� WKDW��+HU�KXVEDQG�� D�SV\FKLDWULVW�� GLHG� MXVW� DERXW� WKH�VDPH�WLPH�WKDW�0DU\�GLG��1HLWKHU�RI�XV�ZDQWV�WR�UHPDUU\��VR�we just enjoy life together.

,�³UHWLUHG´�LQ�������,�FXW�ZD\�EDFN�RQ�P\�FOLQLFDO�ZRUN�EXW�FRQWLQXHG� LW� IRU� �±��PRUH� \HDUV� EHIRUH� UHVWULFWLQJ�P\VHOI�to research, with occasional lectures. I have enjoyed this a great deal, especially since research was the principal leg of the “academic three-legged stool” that suffered when one gets very busy with clinical work and teaching. I still do

miss the clinical side, however.

The research is fun and exciting, but what makes it very spe-cial is the bright young people who have worked with me and taught me so much. Three people deserve special praise DV�WKH\�KDYH�ZRUNHG�IRU�PH�RQ�DQG�RII�IRU�DSSUR[LPDWHO\����\HDUV� ±� 3DXOD� 6XPPDQHQ�&DUOVRQ�� -XOLH�'RZQHV�� DQG�'H-QLVH�0ROLWRULV��2WKHUV�ZKR�GHVHUYH�VSHFLDO�FUHGLW� IRU� WKHLU�FRQWULEXWLRQV�WR�WKH�ODERUDWRU\�LQFOXGH�9HUD�6XWWHU��+DQQDK�:H[OHU��+DQQHOH�-RXVLPLHV�6RPHU��<XOL�6RQJ��&KHQJ[X�/LX��(OOHQ�-R�%DURQ��DQG�PDQ\�,QIHFWLRXV�'LVHDVH�)HOORZV��QRWD-EO\�-RKQ�%DUWOHWW��(OOLH�-�&��*ROGVWHLQ��/DQFH�*HRUJH��*RG-IUH\�+DUGLQJ��DQG�,W]KDN�%URRN���,�DP�DOVR�LQGHEWHG�WR�WKH�many outstanding collaborators I have been blessed to work with over the years, many too many to mention. They have added immeasurably to the work of the laboratory and they have enriched my life. It is remarkable that in academia one FDQ�KDYH�D�SHUVRQDO�¿UVW�IDPLO\�VXFK�DV�,�KDYH�DQG�KDYH�KDG�and, in addition, a second family of mentors, students, and colleagues.

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181© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 181–188

Introduction

1HZ� GUXJV� HVSHFLDOO\� DQWLELRWLFV� DUH� XUJHQWO\� QHHGHG� WR�WKZDUW�SDWKRJHQV� �7DOERW�HW�DO���������DQG� OLIH�WKUHDWHQLQJ�GLVHDVHV��6DODV�HW�DO����������%DFWHULDO�PDULQH�QDWXUDO�SURG-ucts are important sources of novel natural products for drug GLVFRYHU\� �%OXQW�HW�DO���������������)DXONQHU��������+DHI-QHU���������0DULQH�EDFWHULD�KDYH�D�FRPPRQ�PHFKDQLVP�WR�incorporate bromine or other halogens into organic com-pounds that can potentially lead to enhanced bioactivities. +LVWRULFDOO\�� WKH� LVRODWLRQ�RI�QHZ�PHWDEROLWHV�IURP�PDULQH�RUJDQLVPV�EHJDQ�LQ�����V��,Q�������WKH�¿UVW�PDULQH�EDFWHUL-al metabolite reported was the highly brominated antibiotic ������WULEURPR����Ov�K\GUR[\��v��v-dibromophenyl) pyrrole. This compound was isolated from an Alteromonas species obtained from the surface of the Caribbean seagrass Thalas-sia� E\�%XUNKROGHU� DQG� FR�ZRUNHUV� �6DODV� HW� DO��� ������� ,Q�

�����WKH�VDPH�JURXS�LVRODWHG�DQ�DQWLELRWLF�SURGXFLQJ�Pseu-domonas� IURP�D� WLGHSRRO� LQ�/D�-ROOD��&DOLIRUQLD�� ,VRODWLRQ�DQG�SXUL¿FDWLRQ�RI�WKH�PHWDEROLWHV�\LHOGHG���EURPR�LQGROH�FDUER[DOGHK\GH��LWV�GHEURPR�DQDORJ��DQG�D�PL[WXUH�RI���Q�SHQW\O�� DQG� ��Q�KHSW\OTXLQROLQRO�� 7KH�PRVW� LQWHUHVWLQJ� RI�WKHVH� ZDV� ��Q�SHQW\OTXLQROLQRO�� ZKLFK� KDG� SRWHQW� DFWLY-ity against Staphylococcus aureus. The unique metabolite ��EURPR�LQGROH�FDUER[DOGHK\GH� ODFNHG�DQWLPLFURELDO�SURS-HUWLHV��)HQLFDO���������7KH�LVRODWLRQ�RI�WKHVH�KLJKO\�EURPL-nated compounds illustrates a unique property that distin-JXLVKHV�PDULQH�IURP�WHUUHVWULDO�EDFWHULD��6LQFH�WKHQ��D�EURDG�spectrum of biological activities has been detected, for in-stance, antibiotic, antifungal, toxic, cytotoxic, neurotoxic, antimitotic, antiviral, antineoplastic, and cardiovascular �&9��DFWLYLWLHV�

In more recent years, new targets have been added for gen-HUDO� VFUHHQLQJ�� LQFOXGLQJ��$,'6�� LPPXQRVXSSUHVVLYH�� DQWL�LQÀDPPDWLRQ��$O]KHLPHU¶V� GLVHDVH�� DJHLQJ� SURFHVVHV�� DQG�VRPH�WURSLFDO�GLVHDVHV��.HOHFRP���������$OWKRXJK�UHVHDUFK�on metabolites from marine micro-organisms is growing rapidly, a key problem for the scientists in pharmaceutical industries and academic sectors is to effectively discover active marine microbes and obtain their natural products.

Microbial systematics is pivotal to meeting some of the major challenges facing humankind, as exem-SOLÀHG�E\�WKH�QHHG�IRU�QRYHO�QDWXUDO�SURGXFW�PHGLFLQHV��$�V\VWHPDWLFV�JXLGHG�ELRSURVSHFWLQJ�LQYHVWL-gation of bioactive compounds from unique, untapped, ecological niches, including the construction RI�KLJK�TXDOLW\� OLEUDULHV� RI�PDULQH�PLFUREHV� DQG� WKHLU� FUXGH�H[WUDFWV�� KDV�EHFRPH�DQ�HIÀFLHQW� DS-SURDFK�WR�GULYH�GUXJ�GLVFRYHU\��7KH�FULWHULD�IRU�VWUDLQ�VHOHFWLRQ�LQFOXGH��WKH�XQLTXHQHVV�DQG�ULFKQHVV�of biodiversity of the ecolological niches from which the strains are isolated (Hayakawa et al., 2004), symbiosis with medicinal plants (i.e. endophytes), morphological and taxonomical distinctiveness, DQG�D�ELDV� WRZDUGV�WKH�VWXG\�RI�DFWLQRP\FHWHV� IRU� WKHLU�SURYHQ�WUDFN�UHFRUG�DV�SUROLÀF�VRXUFHV�RI�natural products. We optimize natural product production for the selected strains, prepare extracts and subject them to high-throughput (HTP) screening (both cell-based and target-based), followed up by LC-MS dereplication, and prioritize the strains for fermentation scale-up, isolate and determine the structures of the novel natural products, and produce and assemble the library for screening. Our ecology- and taxonomy-based approach to strain selection for novel natural product discovery con-trasts with traditional natural product discovery programs, most of which rely heavily on the designs of the HTP assays to screen often randomly collected micro-organisms.

Contact details1CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, People’s Republic of China.2Graduate School of Chinese Academy of Sciences, Beijing, 100049, P.R. China.

Corresponding author: Li-Xin Zhang – [email protected]

Na Yang,1,2 Biao Ren,1,2 Jian Wang1 and Li-Xin Zhang1

Isolation of novel natural products from un- or underex-plored marine actinomycetes

BISMiS 2011 Paper

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182

Isolation of novel natural products from un- or underexplored marine actinomycetes

The Bulletin of BISMiS

Fortunately, advances in microbial systematics and analyti-cal techniques in constructing high-quality natural product libraries and high-throughput screening methods have facil-itated the development of novel natural products discovery. $PRQJ�PDULQH�PLFUREHV��WKH�DFWLQRP\FHWHV�JURXS�LV�D�ULFK�source of drug candidates as new secondary metabolites can be discovered by screening dereplicated, novel actinomy-FHWHV� �*RRGIHOORZ� DQG� )LHGOHU�� ������ RU� E\� UH�VFUHHQLQJ�NQRZQ� DFWLQRP\FHWHV� GLUHFWHG� E\� JHQRPLFV� �+HUWZHFN� HW�DO���������WKURXJK�V\VWHPDWLFV�WHFKQRORJ\��7KLV�PLQL�UHYLHZ�is based upon actinobacterial systematics which is used to direct novel natural products discovery by two separate URXWHV�� LVRODWLQJ�XQ�H[SORUHG�PDULQH�DFWLQRP\FHWHV�DQG�UH�screening under-explored marine actinomycetes.

Systematics leads to new natural products investigations

Discovery of novel actinomycetes from marine sources

$FWLQRP\FHWHV� DUH� ZLGHO\� GLVWULEXWHG� LQ� GLIIHUHQW� PDULQH�ecosystems and have evolved great genomic and metabolic diversity. There is a tremendous potential for the isolation of novel secondary metabolites from marine actinomycetes. The probability of discovering new secondary metabolites from novel actinomycetes is much higher than from “old” or common actinomycetes. Thus, isolating novel actinomycete strains is one of the best approaches to discovering novel natural products. Therefore, maximizing the types of sam-ples and developing isolation and culturing strategies will HQKDQFH�FRQWULEXWLRQV� �=KDQJ�HW� DO��� �������7KH�SUHGLFWHG�values of actinobacterial diversity shows that as many as �����WD[D�H[LVW�LQ�PDULQH�KDELWDWV��DQG�DSSUR[LPDWHO\�����of these taxa represent novel species and genera-based on ��6� U51$� JHQH� FORQH� OLEUDU\� GDWD�� 5HFHQW� GDWD� IURP� FXO-ture-dependent studies have revealed that the genera Diet-zia, Rhodococcus, Streptomyces, Salinispora, Marinophilus, Solwaraspora, Salinibacterium, Aeromicrobium, William-sia, and Verrucosispora�H[LVW�LQ�PDULQH�HQYLURQPHQWV��/DP��������� 6SHFL¿FDOO\� WKH� JHQHUD�Salinispora and Verrucosis-pora�SURPLVH�WR�EH�WKH�PRVW�H[FLWLQJ�¿QGLQJ�EHFDXVH�WKH\�produced the novel bioactive series of compounds, the sa-OLQLVSRUDP\FLQV�DQG�DE\VVRPLFLQV��UHVSHFWLYHO\��)HQLFDO�HW�DO���������6XVVPXWK�HW�DO���������

Investigations for the isolation of novel actinomycetes from marine environments continue, including enrichment tech-QLTXHV�� QHZ� VHOHFWLRQ� PHWKRGV� DQG� PHGLD� �-HQVHQ� HW� DO���������0DJDUYH\�HW�DO����������7DEOHV���DQG�����)RU�LQVWDQFH��it is important to provide suitable growth conditions with SURSHU�QXWULHQWV��FDUERQ��QLWURJHQ��WUDFH�PHWDOV��RU�WKH�FRU-UHFW� WHPSHUDWXUH�� DHUDWLRQ�� DQG� WLPH� RI� FXOWLYDWLRQ��PHGLD�

supplemented with signaling molecules, such as pyruvate, F\FOLF�DGHQRVLQH�PRQRSKRVSKDWH��DQG�KRPRVHULQH�ODFWRQHV��use of “harsh” conditions or pre-treatments to increase the QXPEHU�DQG�GLYHUVLW\�RI�UDUH�DFWLQRP\FHWHV��LQ�DGGLWLRQ��GLI-ferent antibiotics are used to reduce the growth of unwanted IXQJL�DQG�*UDP�VWDLQ�QHJDWLYH�EDFWHULD�

Genomics combined with systematics

$OWKRXJK�JUHDW�SURJUHVV�KDV�EHHQ�PDGH��VWUDWHJLHV�WRZDUGV�the isolation of new marine-derived actinomycetes are still ODFNLQJ� �/DP���������7KH� DGYDQFH�RI�JHQRPH� VHTXHQFLQJ�has revived an interest in rescreening actiomycetes for bio-active compounds. The massive surge in genome-sequenc-ing projects has revealed the great biosynthetic potential and metabolic diversity of micro-organisms. To date, whole-ge-QRPH� VHTXHQFHV�RI�RYHU�����DFWLQRP\FHWHV� DUH�SXEOLVKHG�RQ�WKH�ZHEVLWH��KWWS���ZZZ�JHQRPHVRQOLQH�RUJ����7KH�³SK\-ORJHQRPLFV´�DSSURDFK��¿UVW�SURSRVHG�E\�-RQDWKDQ�$��(LVHQ�DQG�3KLOLS�&��+DQDZDOW��FRPELQHV�JHQRPH�VHTXHQFH�LQIRU-mation and phylogenetic studies into a composite analysis �(LVHQ� DQG� +DQDZDOW�� ������� 7KH� *HQRPLF� (QF\FORSHGLD�of Bacteria and Archaea� �*(%$�� SURMHFW� FKRVH� W\SLFDO�micro-organisms for sequencing to reveal the evolutionary UHODWLRQVKLSV��7KH�SURMHFW�SURGXFHG�PDQ\�EHQH¿WV�LQFOXGLQJ�the reconstruction of phylogenetic history, the discovery of new protein families and biological properties, and the pre-diction of functions for known genes from other organisms �(LVHQ�HW�DO����������7KH�SK\ORJHQRPLFV�DQG�*(%$�SURMHFW�indicate a new era in actinobacterial systematics and im-prove the prospects of natural product discovery.

The development of phylogenomics brings several novel research methods to infer the evolutionary history of Acti-nobacteria on the basis of their genome analysis. The two primary standard phylogenomic reconstruction methods are sequence-based methods and methods that are based on ZKROH�JHQRPH�IHDWXUHV�ZLWK�UDUH�JHQRPLF�FKDQJHV��5*&V���3KLOLSSH�HW�DO����������&RPSRVLWLRQ�YHFWRU��&9��LV�RQH�RI�the acknowledged methods which has been used in archaeal WD[RQRP\��+DR�HW�DO����������1RYHO�WD[D�VXFK�DV�VXERUGHUV�Actinopolysporineae and Kineosporiineae, families Actinop-olysporaceae, Kineosporiaceae, and Beutenbergiaceae, and genus Quadrisphaera�ZHUH�SURSRVHG�E\�WKH�5*&V�PHWKRG��/L�HW�DO����������8VLQJ�ZKROH�JHQRPH�DQDO\VLV�WR�RYHUFRPH�the limitation of poorly resolved phylogenies is becoming a promising method. Different universally conserved protein-encoding genes mined from the genome were applied to UHVROYH� WKLV�SUREOHP��%UHLWOLQJ�HW�DO����������7KHRUHWLFDOO\��species having a close relationship implies that they have the same gene order and may produce the same kind of me-tabolites. Thus, it is very important to determine the most accurate evolutionary position of actinomycetes.

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183The Bulletin of BISMiS

Na Yang, Biao Ren, Jian Wang and Li-Xin Zhang

Table 2. Commonly used isolation media

Selective medium Selective agent Target taxa Reference

Arginine-vitamins agar None Microbispora, Streptosporan-gium spp.

Nonomura and Ohara (1969)

Colloidal chitin agar None Actinomycetes Hsu and Lockwood (1975)Humic acid-salts-vitamin agar None Dactylosporangium, Micro-

bispora, Micromonospora, Streptosporangium, Thermo-monospora spp.

Hayakawa and Nonomura (1987)

Humic acid-gellan gum None Microbispora Suzuki et al. (1998)Marine agar None Kocuria marina Kim et al. (2004)

Salinibacterium amurskyense Han et al. (2003)Serinicoccus marinus Chun et al. (2004)

Starch-casein-mineral salts agar

Cycloheximide nystatin Streptomyces spp. Kuester and Williams (1964)

Diagnostic sensitivity test agar

Demethylchlortetracy-cline

Nocardia asteroides Orchard and Goodfellow (1974)

Demethylchlortetracy-cline, chlortetracycline

Orchard et al. (1977)

MethacyclineInorganic mineral salts agar Cycloheximide nystatin Rhodococcus spp. Rowbotham and Cross (1977)Glucose yeast extract Rifampicin Actinomadura spp., Strepto-

myces albusAthalye et al. (1985)

Thermomonospora chromog-ena

5DIÀQRVH�KLVWLGLQH�DJDU Cycloheximide, nystatin Streptomyces chromofuscus Vickers et al. (1984)Starch-casein-seawater agar Actidione Streptomyces spp. Goodfellow and Haynes (1984)Starch-casein agar plus 0.5%NaCl

Cycloheximide, nalidixic acid, nystatin

Actinoplanes spp. Takizawa et al. (1993)

Glucose yeast extract agar Cycloheximide Gordonia and Tsukamurella spp.

Goodfellow et al. (1991)

SM3 agar Novobiocin, nalidixic acid Amycolatopsis spp. Tan (2002)M1-M5 Cycloheximide, rifampicin Salinispora spp. Fenical et al. (2002)Starch casein agar Cycloheximide, nystatin Streptacidiphilus spp. Kim et al. (2003)Humic acid-vitamin agar Cycloheximide Streptomyces violaceusniger Hayakawa et al. (2004)

Table 1. Commonly used pretreatment methods

Pretreatment method Reference

Filter method Hirsch and Christensen (1983)

Dispersion and differential centrifugation (DDC) Hopkins et al. (1991)

Radiation method Zotchev et al. (2007)

Stamping method Fenical et al. (2002)

Dilution and heat-shock method Fenical et al. (2002)

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184

Isolation of novel natural products from un- or underexplored marine actinomycetes

The Bulletin of BISMiS

Research on actinobacterial whole-genome sequences is an effective method to study actinobacterial physiological dif-ferentiation, regulation of metabolic networks, prediction of natural products, taxonomy and evolutionary relations, etc. $�UHFHQW�VWXG\�FRQWDLQV�VHYHUDO�DVSHFWV�RI�DFWLQREDFWHULDO�JH-nomics and natural product isolation. These include whole-genome sequence mining, genome scanning, metagenomics, DQG�KHWHURORJRXV�H[SUHVVLRQ��6KHQ�DQG�9DQ�/DQHQ��������

High-quality actinobacterial natural product libraries

The inherent superiority of marine actinobacterial isolates and the development of high-throughput screening tech-QRORJ\� PDNH� D� 0DULQH� 0LFUREH� 1DWXUDO� 3URGXFW� /LEUDU\��0013/��DWWUDFWLYH�IRU�GUXJ�GLVFRYHU\��%XJQL�HW�DO���������*DQMX� HW� DO��� ������ .RHKQ�� ������� 7R�PDNH� WKH�0013/�more convenient for new screening patterns and to shorten the bioactive marine natural products discovery pipeline, we KDYH�FKDUDFWHUL]HG�DQ�0013/�SDUDGLJP�JXLGHG�E\�PLFUR-ELDO�V\VWHPDWLFV��=KDQJ�HW�DO����������)LJXUH����

Biodiversity- and taxonomy-guided library construction

Chemical diversity is coupled to the novel biodiversity of PDULQH�DFWLQRP\FHWHV��.RHKQ�DQG�&DUWHU��������6LQJK�DQG�3HODH]���������$�PDMRU�JRDO�IRU�FRQVWUXFWLQJ�D�0013/�LV�WR�increase the diversity of the natural products while decreas-ing their redundancy. Techniques including selective isola-WLRQ��SKHQRW\SH�DQDO\VLV�DQG�TXLFN�LGHQWL¿FDWLRQ�EDVHG�RQ�taxonomy are most commonly used in discovering marine DFWLQRP\FHWHV��$PDQQ�DQG�/XGZLJ��������$QGHUVRQ�HW�DO���������+HQWVFKHO�HW�DO���������.HOOHU�DQG�=HQJOHU��������/DUV-HQ�HW�DO���������0XOOHU�HW�DO����������%\�XVLQJ�WKHVH�VWUDWHJLHV��ZH�KDYH� LVRODWHG�PRUH� WKDQ��������PDULQH�DFWLQREDFWHULDO�VWUDLQV��ZKLFK�FRYHUHG�PRVW�JHQHUD�RI�DFWLQRP\FHWHV��$IWHU�WKH�DQDO\VLV�RI�WKH�JHQHWLF�GLYHUVLW\�RI�3.6�DQG�1536�ELR-synthetic systems in these strains, the systematic alteration RI�HDV\�DFFHVVLEOH�IHUPHQWDWLRQ�SDUDPHWHUV��PHGLD�FRPSRVL-WLRQ��S+�YDOXH��WHPSHUDWXUH��DGGLWLRQ�RI�HQ]\PH�LQKLELWRUV��oxygen supply, culture vessel) were employed to stimulate the novel compounds produced from these gene clusters EDVHG�RQ�RXU�KLJK�WKURXJKSXW�ELRDVVD\V��=HHFN�HW�DO����������0DQ\�RI�WKH�H[WUDFWV�IURP�RXU�LVRODWHV�VKRZHG�SRWHQWLDO�ELR-DFWLYLWLHV��$VKIRUWK�HW�DO����������7KHVH�GDWD�GHPRQVWUDWHG�WKH� GRJPD� �QRYHO� LVRODWHVAnovel gene clustersAnovel compounds) and the value of taxonomy-guided strain selec-tion and biosynthesis gene cluster analysis.

Dereplication of actinomycetes and their products

$QRWKHU�LPSRUWDQW�SDUW�RI�DQ�0013/�LV�GHFUHDVLQJ�UHGXQ-

GDQF\�±�LQ�RUGHU�WR�UHGXFH�VFUHHQLQJ�FRVWV�DQG�LQFUHDVH�WKH�success rate, dereplication approaches are urgently needed.

The redundancy of actinomycetes strains is the major issue for high-quality natural products library construction. The selection of media and pre-treatment methods are important for isolation of actinomycetes from marine sources. But further dereplication of genetically identical actinomycete strains is still necessary before natural products library con-struction as they may contain the potential for producing the same metabolites.

The dereplication of strains can be fully achieved by acti-nobacterial taxonomy. These methods are widely used in QRYHO�VWUDLQ�LGHQWL¿FDWLRQ��'HUHSOLFDWLRQ�RI�VWUDLQV�EHFRPHV�PXFK�HDVLHU�ZLWK�WKH�WD[RQRP\�PHWKRGV�±�SKHQRW\SLF�SUR-¿OLQJ��FKHPLFDO�DQDO\VLV��DQG�JHQRW\SLF�SUR¿OLQJ��0RUSKRO-ogy discrimination such as spore formation, aerial mycelia, strain colonies and diffusible pigment by the naked eye or microscopy is the most rapid way to dereplicate strains. &RORQ\�FRORU�JURXSV�UHÀHFW�WKH�WD[RQRPLF�GLYHUVLW\�RI�FXO-tivable actinomycetes in marine environment on oatmeal agar directly. Chemical analyses are also commonly used in analyzing whole-cell sugar, polar lipids or diaminopimelic

Figure 1. Building a Marine Microbe Natural Product Library in the laboratory.

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185The Bulletin of BISMiS

Na Yang, Biao Ren, Jian Wang and Li-Xin Zhang

DFLG��'$3��W\SH��0DOGRQDGR�HW�DO���������WR�DVVLJQ�VWUDLQV�to different groups. Integrated with the genotypic data such DV�5HVWULFWLRQ�)UDJPHQW�/HQJWK�3RO\PRUSKLVP��5)/3��DQG�'HQDWXULQJ� *UDGLHQW� *HO� (OHFWURSKRUHVLV� �'**(�� RI� WKH���6���6�JHQHV��WKH�GHUHSOLFDWLRQ�ZRUN�FDQ�EH�IXOO\�DFKLHYHG��7KH�ODWHVW�PHWKRG�LV� WR�XVH�WKH�SRO\NHWLGH�V\QWKDVH��3.6��gene probe to detect strains. The results indicate that strains WKDW�KDG�VLPLODU�EDQG�SDWWHUQV�KDUERUHG�VLPLODU�3.6�JHQHV��)RU�H[DPSOH��$\XVR�6DFLGR�DQG�*HQLOORXG��������GHVLJQHG�QHZ�3&5�SULPHUV�WDUJHWHG�WR�VSHFL¿FDOO\�DPSOLI\�1536�DQG�3.6�,� JHQH� VHTXHQFHV� IURP�DFWLQRP\FHWHV��7KH� VHTXHQFH�DQDO\VLV�RI�DPSOL¿HG�SURGXFWV�FORQHG�IURP�WZR�PRGHO�V\V-tems and used to validate these molecular tools has shown WKH�H[WUHPH�ULFKQHVV�RI�1536�RU�3.6�,�OLNH�VHTXHQFHV� LQ�WKH�DFWLQRP\FHWH�JHQRPH��:KHQ� WKHVH�3&5�SULPHUV�ZHUH�WHVWHG�RQ�D�ODUJH�FROOHFWLRQ�RI�����UHIHUHQFH�VWUDLQV�HQFRP-passing all major families and genera of the actinomycetes, it was observed that the wide distribution of these genes in the well-known productive Streptomyces species is also ex-tended to other minor lineages where in some cases very few ELRDFWLYH�FRPSRXQGV�KDYH�EHHQ�LGHQWL¿HG�WR�GDWH��8VLQJ�WKH�3.6�JHQHV�IRU�GLUHFW�GHUHSOLFDWLRQ�ZRUN�LV�PRUH�FRQYHQLHQW�for bioactive compound screening. Dereplication is the ba-sic procedure to be used for differentiating phenotypically ambiguous strains in order to facilitate the follow-up screen-ing strategies and thereby minimize costs and time in sorting large collections of isolates.

Following the actinomycetes dereplication, the chemical dereplication procedure also plays an important role in 0013/��)RU�H[DPSOH��%UDQGDR�HW�DO��GHYHORSHG�D�S\URO\VLV�PDVV�VSHFWURPHWU\��3\06��PHWKRG��%UDQGDR�HW�DO����������7KLV�WHFKQLTXH�LV�D�ZKROH�FHOO�¿QJHUSULQWLQJ�WHFKQLTXH�WKDW�enables the rapid and reproducible sorting of micro-organ-isms, which uses small samples and has the advantage of EHLQJ�IXOO\�DXWRPDWHG��0RUHRYHU��3\06�DQDO\VLV�UHYHDOHG�VLJQL¿FDQW� YDULDWLRQ� ZLWKLQ� S\URJURXSV� WKDW� FRQWDLQHG�VWUDLQV�ZLWK�WKH�VDPH�JHQRW\SLF��356��FKDUDFWHULVWLFV��WKXV�emphasizing its discriminatory capacity at the interspecies level. For the sake of the accelerated dereplication of natural SURGXFWV��0XQUR�HW�DO����������DGYDQFHV�LQ�PRGHUQ�VSHFWUR-scopic methods have allowed the development of tandem DQDO\WLFDO� WHFKQLTXHV�� VXFK� DV�06�06�06� �.RQLVKL� HW� DO����������*&�(,�06��7LPPHUPDQQ�HW�DO����������+3/&�63(�105��-DURV]HZVNL�HW�DO����������/&�06�06��:ROIHQGHU�HW�DO����������DQG�/&�105��%RE]LQ�HW�DO���������+HQNHO�HW�DO����������$OO�RI�WKHVH�WHFKQLTXHV�LQFUHDVH�WKH�FKHPLFDO�GLYHU-VLW\�RI�0013/�

Prediction of the relation between tax-onomy and secondary metabolite produc-tion

6WUHSWRP\FLQ�ZDV�WKH�¿UVW�FODVV�RI�DQWLELRWLFV�GHULYHG�IURP�WKH� DFWLQRP\FHWHV�� 6LQFH� WKHQ�� ODUJH� JURXSV� RI� DQWLELRWLFV�have been isolated from actinomycetes, and Streptomyces became the main source of antibiotic-producing strains. But when the redundancy problem of repeatedly isolating the same compounds from Streptomyces became more and more serious, isolating novel rare actinomycetes became the JRDO�RI�GUXJ�GLVFRYHU\�UHVHDUFKHUV��8QIRUWXQDWHO\��QR�GH¿-nite rule of “which genus of actinomycetes produces which groups of compounds” has been discovered or published to date. We may occasionally predict the metabolites based on SUHYLRXVO\�UHSRUWHG�GDWD��<LQJ�+XDQJ�HW�DO���������VFUHHQHG������DFWLQRP\FHWHV�XVLQJ�GHJHQHUDWH�SULPHUV�GHVLJQHG�DF-cording to the conserved regions of polyether epoxidases and discovered a group of strains that have the potential of producing polyether ionophores. The genera having the ability to produce polyether ionophores are Streptomyces, Actinomadura, Dactylosporangium, and Micromonospora �+XDQJ�HW�DO����������7KH�¿QDO�UHVXOWV�RI�WKHVH�H[SHULPHQWV�UHYHDOHG� ��� SRVLWLYH� LVRODWHV� WKDW� EHORQJHG� WR� ¿YH� JHQHUD�that were able to produce polyether ionophores as predicted. In addition, two new analogs were found.

Prospects and conclusions

7KH�PDULQH�HQYLURQPHQW�LV�D�SUROL¿F�UHVRXUFH�IRU�WKH�LVROD-WLRQ�RI�OHVV�H[SORLWHG�PLFURRUJDQLVPV��0DULQH�PLFURELRORJ\�with a distinct focus on bioactive compounds is developing strongly in several countries. Furthermore, it has been reit-erated that natural product research and discovery in marine DFWLQREDFWHULD� VKRZV�H[FHSWLRQDO�SURPLVH��+HQFH�� WKHUH� LV�an increasing need to discover more novel marine actino-bacteria and their novel biosynthesis gene clusters. Further-more, constructing a library of marine actinobacteria guided by microbial systematics is also amenable to the discovery of biological compounds.

Dedication

:H�ZRXOG�OLNH�WR�GHGLFDWH�WKLV�SDSHU�WR�WKH�PRUH�WKDQ�����SDUWLFLSDQWV�IURP����FRXQWULHV�DW�WKH�,QDXJXUDO�&RQIHUHQFH�RI�%HUJH\¶V�,QWHUQDWLRQDO�6RFLHW\�IRU�0LFURELDO�6\VWHPDWLFV�in Beijing.

Acknowledgements

3DUW�RI� WKLV�ZRUN�ZDV�SHUIRUPHG�XQGHU�D�UHVHDUFK�FROODER-UDWLRQ�EHWZHHQ�*OREDO�$OOLDQFH�IRU�7%�'UXJ�'HYHORSPHQW��7%� $OOLDQFH�� DQG� ,QVWLWXWH� RI� 0LFURELRORJ\� RI� &KLQHVH�

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186

Isolation of novel natural products from un- or underexplored marine actinomycetes

The Bulletin of BISMiS

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$WKDO\H��0���0��*RRGIHOORZ��-��/DFH\�DQG�5�3��:KLWH��������1XPHULFDO� FODVVL¿FDWLRQ� RI�Actinomadura and Nocardi-opsis��,QW��-��6\VW��%DFWHULRO��35:���±���

$\XVR�6DFLGR��$��DQG�2��*HQLOORXG��������1HZ�3&5�SULPHUV�IRU�WKH�VFUHHQLQJ�RI�1536�DQG�3.6�,�V\VWHPV�LQ�DFWLQR-P\FHWHV��GHWHFWLRQ�DQG�GLVWULEXWLRQ�RI�WKHVH�ELRV\QWKHWLF�JHQH�VHTXHQFHV�LQ�PDMRU�WD[RQRPLF�JURXSV��0LFURE��(FRO��49:���±���

%OXQW�� -�:���%�5��&RSS��0�+��0XQUR�� 3�7��1RUWKFRWH� DQG�0�5��3ULQVHS��������0DULQH�QDWXUDO�SURGXFWV��1DW��3URG��Rep. 20:��±���

%OXQW�� -�:���%�5��&RSS��0�+��0XQUR�� 3�7��1RUWKFRWH� DQG�0�5��3ULQVHS��������0DULQH�QDWXUDO�SURGXFWV��1DW��3URG��Rep. 21:��±���

%RE]LQ��6�&���6��<DQJ�DQG�7�3��.DVWHQ��������/&�105��D�QHZ�WRRO�WR�H[SHGLWH�WKH�GHUHSOLFDWLRQ�DQG�LGHQWL¿FDWLRQ�RI� QDWXUDO� SURGXFWV�� -�� ,QG�� 0LFURELRO�� %LRWHFKQRO�� 25: ���±����

%UDQGDR��3�)���0��7RULPXUD��5��.XUDQH�DQG�$�7��%XOO��������'HUHSOLFDWLRQ�IRU�ELRWHFKQRORJ\�VFUHHQLQJ��3\06�DQDO\-VLV�DQG�3&5�5)/3�66&3��356��SUR¿OLQJ�RI���6�U51$�JHQHV�RI�PDULQH�DQG�WHUUHVWULDO�DFWLQRP\FHWHV��$SSO��0L-crobiol. Biotechnol. 58:���±���

%UHLWOLQJ��5���0�7��$ODP��0�(��0HUOR�DQG�(��7DNDQR��������*HQRPH�EDVHG� SK\ORJHQHWLF� DQDO\VLV� RI� Streptomyces DQG�LWV�UHODWLYHV��0RO��3K\ORJHQHW��(YRO��54:����±����

%XJQL�� 7�6��� %�� 5LFKDUGV�� /�� %KRLWH�� '�� &LPERUD�� 0�.��+DUSHU�DQG�&�0�� ,UHODQG��������0DULQH�QDWXUDO�SURGXFW�libraries for high-throughput screening and rapid drug GLVFRYHU\��-��1DW��3URG��71:�����±�����

&KXQ��-���+��<L��3��6FKXPDQQ�DQG�.��6RKQ��������Serinicoc-cus marinus gen. nov., sp nov., a novel actinomycete with l-ornithine and l�VHULQH�LQ�WKH�SHSWLGRJO\FDQ��,QW��-��6\VW��

(YRO��0LFURELRO��54:�����±�����(LVHQ��-�$��DQG�3�&��+DQDZDOW��������$�SK\ORJHQRPLF�VWXG\�RI�'1$�UHSDLU�JHQHV��SURWHLQV��DQG�SURFHVVHV��0XW��5HV��'1$�5HSDLU�435:����±����

(LVHQ�� -�$��� '�<�� :X�� 3�� +XJHQKROW]�� .�� 0DYURPDWLV�� 5��3XNDOO��(��'DOLQ��1�1�� ,YDQRYD��9��.XQLQ��/��*RRGZLQ��0��:X��%�-��7LQGDOO��6�'��+RRSHU��$��3DWL��$��/\NLGLV��6��6SULQJ��,�-��$QGHUVRQ��3��'¶KDHVHOHHU��$��=HPOD��0��6LQJ-HU��$��/DSLGXV��0��1RODQ��$��&RSHODQG��&��+DQ��)��&KHQ��-�)��&KHQJ��6��/XFDV��&��.HUIHOG��(��/DQJ��6��*URQRZ��3��&KDLQ�� '�� %UXFH�� (�0�� 5XELQ�� 1�&�� .\USLGHV� DQG� +�3��.OHQN�� ������$� SK\ORJHQ\�GULYHQ� JHQRPLF� HQF\FORSDH-dia of Bacteria and Archaea��1DWXUH�462:�����±�����

)DXONQHU�� '�-�� ������ 0DULQH� SKDUPDFRORJ\�� $QWRQLH� YDQ�/HHXZHQKRHN�77:����±����

)HQLFDO��:��������&KHPLFDO�VWXGLHV�RI�PDULQH�EDFWHULD�±�GH-veloping a new resource. Chem. Rev. 93:�����±�����

)HQLFDO��:���7�-��0LQFHU�� 3�5�� -HQVHQ� DQG�&�$��.DXIIPDQ�������� :LGHVSUHDG� DQG� SHUVLVWHQW� SRSXODWLRQV� RI� D� PD-jor new marine actinomycete taxon in ocean sediments. $SSO��(QYLURQ��0LFURELRO��68:�����±�����

)HQLFDO��:��� 3�*��:LOOLDPV�� *�2�� %XFKDQDQ�� 5�+�� )HOLQJ��&�$�� .DXIIPDQ� DQG� 3�5�� -HQVHQ�� ������ 1HZ� F\WRWR[LF�salinosporamides from the marine actinomycete Salinis-pora tropica��-��2UJDQ��&KHP��70:�����±�����

*DQMX��/���.�3��0LVKUD��0��6DLUDP��3�.��%DQHUMHH�DQG�5�&��6DZKQH\��������$�UHYLHZ�RI�KLJK�WKURXJKSXW�WHFKQRORJ\�IRU�WKH�VFUHHQLQJ�RI�QDWXUDO�SURGXFWV��%LRPHG��3KDUPDFR-ther. 62:���±���

*RRGIHOORZ��0���-��=DNU]HZVND�&]HUZLQVND��(�*��7KRPDV��0��0RUGDUVNL��$�&��:DUG� DQG�$�/�� -DPHV�� ������ 3RO\-phasic taxonomic study of the genera Gordona and Tsu-kamurella including the description of Tsukamurella wratislaviensis�VS��QRY��=HQWUDOEO��%DNWHULRO��,QW��-��0HG��0LFURELRO��9LURO��3DUDVLWRO��,QIHFW��'LV��275:����±����

*RRGIHOORZ��0��DQG�+�3��)LHGOHU��������$�JXLGH�WR�VXFFHVV-IXO�ELRSURVSHFWLQJ��LQIRUPHG�E\�DFWLQREDFWHULDO�V\VWHPDW-LFV��$QWRQLH�YDQ�/HHXZHQKRHN�98:����±����

*RRGIHOORZ��0��DQG�-�$��+D\QHV��������$FWLQRP\FHWHV� LQ�marine sediments. In Biological, Biochemical and Bio-PHGLFDO�$VSHFWV� RI�$FWLQRP\FHWHV� �HGLWHG� E\�2UWL]�2U-WL]��%RMDOLO�DQG�<DNROHII���$FDGHPLF�3UHVV��2UODQGR��SS�����±����

+DHIQHU��%��������'UXJV�IURP�WKH�GHHS��PDULQH�QDWXUDO�SURG-ucts as drug candidates. Drug Disc. Today 8:����±����

+DQ��6�.���2�,��1HGDVKNRYVND\D��9�9��0LNKDLORY��6�%��.LP�DQG�.�6�� %DH�� ������ Salinibacterium amurskyense gen. nov., sp. nov., a novel genus of the family Microbacte-riaceae�IURP�WKH�PDULQH�HQYLURQPHQW��,QW��-��6\VW��(YRO��0LFURELRO��53:�����±�����

+DR��%�/���-�'��6XQ�DQG�=��;X��������:KROH�JHQRPH�EDVHG�Archaea�SK\ORJHQ\�DQG�WD[RQRP\��D�FRPSRVLWLRQ�YHFWRU�

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187The Bulletin of BISMiS

Na Yang, Biao Ren, Jian Wang and Li-Xin Zhang

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+D\DNDZD��0���<��<RVKLGD�DQG�<�� ,LPXUD��������6HOHFWLYH�isolation of bioactive soil actinomycetes belonging to the Streptomyces violaceusniger�SKHQRW\SLF�FOXVWHU��-��$SSO��0LFURELRO��96:����±����

+HQNHO�� 7��� -�� %LW]HU�� %�� .RSFNH��0�� 6WDGOHU�� 9�� +HLOZLJ��<�0��-X�DQG�6��6HLS��������$FFHOHUDWHG�GHUHSOLFDWLRQ�RI�natural products, supported by reference libraries. Chi-mia 61:����±����

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+LUVFK��&�)��DQG�'�/��&KULVWHQVHQ��������1RYHO�PHWKRG�IRU�VHOHFWLYH� LVRODWLRQ�RI�DFWLQRP\FHWHV��$SSO��(QYLURQ��0L-crobiol. 46:����±����

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+VX��6�&��DQG�-�/��/RFNZRRG��������3RZGHUHG�FKLWLQ�DJDU�as a selective medium for enumeration of actinomycetes LQ�ZDWHU�DQG�VRLO��$SSO��0LFURELRO��29:����±����

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188

Isolation of novel natural products from un- or underexplored marine actinomycetes

The Bulletin of BISMiS

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189© BISMiS 2011

The Bulletin of BISMiS (2011), Volume 2, part 2, pp. 189–196

Introduction

7KH��QG�HGLWLRQ�RI�Bergey’s Manual of Systematic Bacteriol-ogy follows “a phylogenetic framework based on analysis of the nucleotide sequence of the small ribosomal subunit 51$�� UDWKHU� WKDQ� D� SKHQRW\SLF� VWUXFWXUH´� �*DUULW\¶V� 3UHI-ace). The successful and impressive “congruence” of pro-NDU\RWLF�SK\ORJHQ\�DQG�WD[RQRP\�RQ�WKH�EDVLV�RI���6�U51$�gene sequence analysis raises the problem of independent MXVWL¿FDWLRQ�RI�WKH�ODWWHU��7KH�&97UHH�DSSURDFK�WR�LQIHU�SUR-NDU\RWLF�SK\ORJHQ\�� LQWURGXFHG�D� IHZ�\HDUV� DJR� �4L�HW� DO�������D�� ����E��+DR� HW� DO��� ������� GLVWLQJXLVKHV� LWVHOI� IURP�WKH���6�U51$�DQDO\VLV�ERWK�LQ�LQSXW�GDWD��ZKROH�JHQRPHV��DQG�LQ�PHWKRGRORJ\��DOLJQPHQW�IUHH���,W�LV�UHPDUNDEOH�WKDW�WKH�&97UHH� UHVXOWV� VXSSRUW� WKH���6� U51$�SK\ORJHQ\�DQG�%HUJH\¶V�6\VWHPDWLFV�LQ�D�PDMRULW\�RI�EUDQFKHV�IURP�SK\OD�GRZQ�WR�JHQHUD�DQG�VSHFLHV��0RUHRYHU��DW�WKH�VSHFLHV�OHYHO�DQG� EHORZ� ZKHUH� ��6� U51$� DQDO\VLV� ODFNV� VKDUS� UHVROX-WLRQ��&97UHH�SURYLGHV�D�GH¿QLWH�DQG�UHDVRQDEOH�EUDQFKLQJ�scheme.

$V�WKH�FRVW�RI�VHTXHQFLQJ�D�SURNDU\RWH�JHQRPH�NHHSV�GURS-ping and automatic annotation of bacterial genomes has reached a more or less ripe stage as compared to that for Eu-karya��ZH�H[SHFW�WKDW�&97UHH�ZLOO�EHFRPH�D�FRQYHQLHQW�WRRO�in microbial systematics to obtain a rapid approximation of

WKH�FODVVL¿FDWLRQ�RI�D�QHZO\�VHTXHQFHG�RUJDQLVP�DQG�IRU�D�more effective design of phenotyping experiments.

Feasibility of using whole genomes

6LQFH�WKH�¿UVW�WZR�EDFWHULDO�JHQRPHV�ZHUH�SXEOLVKHG�LQ�������)OHLVFKPDQQ�HW�DO���������)UDVHU�HW�DO��������� WKH�QXPEHU�of sequenced prokaryotic genomes has kept rapidly grow-LQJ��$W�WKH�PRPHQW�RI�ZULWLQJ�WKHVH�OLQHV��PRUH�WKDQ������well-annotated genomes have been released and there are PRUH�WKDQ������RQ�JRLQJ�VHTXHQFLQJ�SURMHFWV��$OWKRXJK�WKH�selection of species to be sequenced in most cases is based on practical needs other than for phylogenetic or taxonomic FRQVLGHUDWLRQV� �WKH�*(%$�SURMHFW�EHLQJ�DQ�H[FHSWLRQ��VHH�:X�HW�DO����������WKH�VHTXHQFHG�JHQRPHV�QRZ�FRYHU�D�ZLGH�WD[RQRPLF�UDQJH��$V�RI���-XO\������WKH�SURNDU\RWLF�JHQRPHV�UHOHDVHG�DW�WKH�1&%,�)73�VLWH�FDPH�IURP��������SK\OD���������� FODVVHV�� ���� ����� RUGHUV�� ���� ����� IDPLOLHV�� ���� �����JHQHUD�������VSHFLHV�DQG������VWUDLQV��QXPEHUV�LQ�SDUHQWKH-ses indicate uncertain taxa including those labeled as Incer-tae sedis or Candidatus). The coverage is much wider than WKH�FROOHFWLRQ�RI�DERXW�������6�U51$�JHQH�VHTXHQFHV�ZKHQ�&DUO�:RHVH�DQG�FRZRUNHUV�SURSRVHG�D�SK\ORJHQHWLF�GH¿QL-WLRQ�RI�WKH�PDMRU�HXEDFWHULDO�WD[D��:RHVH�HW�DO���������

$Q� HVVHQWLDO� DGYDQWDJH� RI� XVLQJ� ZKROH� JHQRPHV� FRQVLVWV�LQ� FLUFXPYHQWLQJ� WKH� ODWHUDO� JHQH� WUDQVIHU� �/*7�� SUREOHP�DV� ERWK�/*7� DQG� OLQHDJH�GHSHQGHQW� JHQH� ORVV� DUH�PHUHO\�PHFKDQLVPV�RI�JHQRPH�HYROXWLRQ��2QH�DYRLGV�DV�ZHOO� WKH�WHGLRXV� WDVN�RI�¿QGLQJ�RUWKRORJRXV�JHQHV�EHFDXVH�DQ\RQH�

Contact detailsT-Life Research Center, Fudan University, Shanghai 200433, China.

[email protected]

CVTrees support the Bergey’s Systematics and provide high resolution at species levels and below

Bailin Hao

CV stands for Composition Vector. CVTree is an alignment-free method for inferring phylogenetic trees from prokaryote whole genomes by using CVs after a subtraction procedure. CVTree is the name of a public domain Web Server that implements the method. The results obtained by this method or by WKH�:HE�6HUYHU�DUH�DOVR�VRPHWLPHV�FDOOHG�&97UHHV��7KH�EUDQFKLQJV�LQ�&97UHHV�DUH�YHULÀHG�E\�GLUHFW�comparison with the Bergey’s Systematics and agree well with the latter at all taxonomic ranks from phylum down to species with a few exceptions, which in most cases correspond to long-debated prob-lems and may hint on possible taxonomic revisions. Moreover, CVTrees provide higher strain resolu-tion at species level and below. In this mini-review the CVTree method will be described and some of its results will be shown.

BISMiS 2011 Paper

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190 The Bulletin of BISMiS

CVTrees support the Bergey’s Systematics

who believes in Charles Darwin must admit that all ge-nomes are orthologs.

Necessity of being alignment-free

3URNDU\RWLF�JHQRPHV�DUH�H[WUHPHO\�GLYHUVH�LQ�WKHLU�VL]H�DQG�JHQH� FRQWHQW��$� VPDOO� JHQRPH�RI Mycoplasma genitalium KDV�RQO\�OHVV�WKDQ�KDOI�D�PLOOLRQ�EDVHSDLUV�DQG�OHVV�WKDQ�����genes, not to mention the tiny genomes of a few endosym-biont bacteria, e.g. Candidatus +RGJNLQLD� FLFDGLFROD��7KH�largest genome sequenced so far, that of Sorangium cellu-losum��KDV�PRUH�WKDQ����PLOOLRQ�EDVHSDLUV�DQG��������JHQHV��,W� LV� YHU\� GLI¿FXOW�� LI� QRW� LPSRVVLEOH�� WR� ³DOLJQ´� VXFK� JH-nomes or to identify orthologous genes shared by all species.

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%HLQJ� DOLJQPHQW�IUHH� UHQGHUV� WKH� &97UHH� PHWKRG� SDUDP-eter-free, because alignment of amino acid sequences in-volves many parameters via scoring matrices, gap penalties, HWF��7KRXJK�WKH�SHSWLGH�OHQJWK�.�ORRNV�OLNH�D�SDUDPHWHU��LW�LV�DFWXDOO\�QRW��:H�QHYHU�DGMXVW�.�DQG�WKH�VDPH�.�LV�XVHG�IRU�DOO�JHQRPHV��.¶V�UROH�LV�PRUH�OLNH�WKH�NQRE�LQ�DQ�RSWLFDO�PL-FURVFRSH�WKDW�FRQWUROV�WKH�UHVROXWLRQ��/RQJHU�.V�SXW�HPSKD-VLV�RQ�VSHFLHV�VSHFL¿FLW\��EXW�VKRUWHU�.V�WDNH�LQWR�DFFRXQW�common features shared by many species. In fact, we con-VWUXFW�&97UHHV�IRU�DOO�. ��WR���DQG�ZDWFK�WKH�³FRQYHUJHQFH´�

RI�WKH�EUDQFKLQJV�ZLWK�.�LQFUHDVLQJ��)RU�D�TXLFN�RYHUYLHZ�of the whole phylogeny based on many available genomes LW�LV�VXI¿FLHQW�WR�UXQ�D�VLQJOH�MRE�IRU�. ��RU���DQG�WKHUH�LV�QR�QHHG�WR�XVH�.�JUHDWHU�WKDQ����:H�RPLW�WKH�WHFKQLFDO�UHDVRQV�supporting the above statement.

$OWKRXJK�WKH�EDVLF�LGHD�RI�&97UHH�LV�TXLWH�VLPSOH��LWV�LPSOH-mentation is complicated by the necessity of dealing with YHU\� ORQJ�&9V�DQG�KXJH�GLVVLPLODULW\�PDWULFHV��7KHUHIRUH��for practitioners in microbiology we designed a public-do-main software which has been published twice in the Web 6HUYHU� LVVXHV�RI�1XFOHLF�$FLGV�5HVHDUFK��4L�HW�DO�������E��;X�HW�DO����������:H�LQYLWH�LQWHUHVWHG�FROOHDJXHV�WR�SOD\�ZLWK�&97UHH�LQ�WKHLU�,QWHUQHW�EURZVHU�DW�KWWS���WOLIH�IXGDQ�HGX�FQ�FYWUHH��ZKHUH�DQ�RQOLQH�KHOS�¿OH�DQG�LWV�SULQWDEOH�YHUVLRQ�LV�available.

We note in passing that all examples to be given below are GUDZQ�IURP�WKH�VDPH�VHW�RI�&97UHHV�IRU�. ��WR���EDVHG�RQ�D�GDWDVHW�RI������SURNDU\RWLF�JHQRPHV��DIWHU�H[FOXGLQJ�WLQ\�genomes of a few endosymbiont bacteria.

Direct comparison with taxonomy

3K\ORJHQ\�DQG�WD[RQRP\�DUH�QRW�V\QRQ\PV��EXW��LGHDOO\��D�faithful phylogeny and a reasonable taxonomy should agree with each other in basic topologies. Traditionally, phylo-JHQHWLF� WUHHV�DUH�YHUL¿HG�E\� VWDWLVWLFDO� UHVDPSOLQJ� VXFK�DV�bootstrap or jackknife. This kind of test tells at most the stability and self-consistency of the trees, by far not the ob-jective correctness of the results. We advocate the viewpoint that a phylogenetic tree should be checked by direct com-parison with taxonomy which is not based on the same kind RI�SK\ORJHQ\��:H�QRWH�WKDW�&97UHHV�DUH�VXSSRUWHG�E\�ERWK�MDFNNQLIH�DQG�ERRWVWUDS� WHVWV�DV�ZHOO� �=XR�HW�DO���������� ,W�is remarkable that this was impossible even a decade ago, as whether prokaryote proteins contain phylogenetic signal ZDV� TXHVWLRQHG� WKHQ� �7HLFKPDQQ� HW� DO��� ������ DQG�ZKROH�genome based phylogeny was unable to “resolve the major EUDQFKLQJV�RI�WKH�%DFWHULD´��+X\QHQ�HW�DO���������

,Q�FRPSDULQJ�&97UHHV�ZLWK�SURNDU\RWH�WD[RQRP\�RXU�JXLG-ing principle is monophyleticity of the branches and a use-ful notion is a “collapsed tree”. Whenever all genomes in the dataset from a certain taxon appear in one and the same branch and no genomes from other taxa occur in that branch, we have full agreement of the phylogeny and taxonomy at that level. Then the branch may be collapsed to a single leaf labeled by the name of the taxon. For example, there are ���³Cyanobacteria” genomes in our dataset and they always IRUP�D�PRQRSK\OHWLF�EUDQFK��ZH�FDQ�FROODSVH�WKH�EUDQFK�WR�a single leaf labeled for all the Cyanobacteria^��`�

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Convergence at different taxonomic ranks

7R�JLYH�DQ�LGHD�RQ�WKH�FRPSDULVRQ�RI�&97UHH�UHVXOWV�ZLWK�taxonomy we illustrate this at different taxonomic levels. )RU�H[DPSOH��DW�WKH�SK\OXP�OHYHO�ZH�KDYH�

Acidobacteria^�`� .�.�.�.�.�

$TXL¿FDH^�`� .���.�.�.�

Chlamydiae^��`� .�.�.�.�.�

Chlorobi^��`� .�.�.�.�.�

Crenarchaeota^��`� ��������.�

Cyanobacteria^��`� ��.�.�.�.�

Deferribacteres^�`� .�.�.�.�.�

Deinococcus-Thermus^��`� .���.�.�.�

Dictyoglomi^�`� .�.�.�.�.�

Elusimicrobia^�`� ����.�.�.�

Fusobacteria^�`� ��.�.�.�.�

Planctomycetes^�`� .�.�.�.�.�

Synergistetes^�`� .�.�.�.�.�

Thaumarchaeota^�`� .�.�.�.�.�

Thermodesulfobacteria^�`� .�.�.�.�.�

Thermotogae^��`� .���.�.�.�

Verrucomicrobia^�`� ����.�.�.�

+HUH� DQG� EHORZ� .�.�.�.�.�� PHDQV� WKH� FRUUHVSRQG-LQJ�SK\OXP� IRUPV�D�PRQRSK\OHWLF�EUDQFK� LQ� DOO�¿YH� WUHHV�FRQVWUXFWHG�IRU�. ��WR����WKRXJK�WKH�WRSRORJ\�PD\�QRW�EH�H[DFWO\�WKH�VDPH��$�PLVVLQJ�.�YDOXH�OLNH�.�².�.�.��LQ-dicates that the phylum does not appear as a monophyletic EUDQFK�DW�. ��

The non-convergence of “Crenarchaeota´�DW�.���LV�FDXVHG�by 7KHUPR¿OXP joining “Candidatus .RDUFKDHXP´�RXWVLGH�but close to the monophyletic cluster.

3K\OD� DEVHQW� LQ� WKH� DERYH� OLVW� GR� QRW� IRUP�PRQRSK\OHWLF�EUDQFKHV�LQ�&97UHHV��)RU�H[DPSOH��WKH�SK\OXP�Proteobac-teria�LV�UHSUHVHQWHG�E\�����VHTXHQFHG�JHQRPHV�IRU�WKH�WLPH�EHLQJ�� WKH�PRVW�DPRQJ�DOO�SK\OD��7KUHH�RI� LWV�¿YH�FODVVHV��WKH�Alphaproteobacteria, Betaproteobacteria, and Epsilon-proteobacteria��GR�IRUP�PRQRSK\OHWLF�EUDQFKHV�LQ�&97UHHV�

DV�VHHQ�LQ�WKH�SDUWLDO�OLVW�RI�FRQYHUJHQW�FODVVHV�VKRZQ�EHORZ�

Acidobacteria^�`� ����.�.�.�

Alphaproteobacteria^���`� ��.�.�.�.�

$TXL¿FDH^�`� .���.�.�.�

Archaeoglobi^�`� .�.�.�.�.�

Bacteroidia^��`� ����.�.�.�

Betaproteobacteria^��`� ����.�.�.�

Chlamydiae^��`� .�.�.�.�.�

Chlorobia^��`� .�.�.�.�.�

&KORURÀH[L^�`� .�.�.�.�.�

Deferribacteres^�`� .�.�.�.�.�

Dehalococcoidetes^�`� .�.�.�.�.�

Deinococci^��`� .���.�.�.�

Dictyoglomia^�`� .�.�.�.�.�

Elusimicrobia^�`� ����.�.�.�

Epsilonproteobacteria^��`� .�.�.�.�.�

Fusobacteria^�`� ��.�.�.�.�

Methanobacteria^�`� .�.�.�.�.�

Methanococci^��`� .�.�.�.�.�

The fact that Betaproteobacteria is intermixed with the Gammaproteobacteria�� REVHUYHG� ¿UVW� LQ� ��6� U51$� JHQH�VHTXHQFH� DQDO\VLV� �:RHVH� HW� DO��� ������ KDSSHQV� DOVR� LQ�&97UHHV��,I�ZH�WDNH�%HWD�*DPPD�DV�D�VLQJOH�JURXS�DV�VXJ-gested by Woese, then the only class which does not form D�PRQRSK\OHWLF�FOXVWHU�LQ�&97UHHV�LV�Deltaproteobacteria. This has been observed in some conserved marker gene VWXGLHV��/XGZLJ���������,Q�SDUWLFXODU��WKH�³FODVV´�VSOLWV�LQWR�several clusters with Bdellovibrio, a deltaproteobacterium forming a sister group with Leptospira from the phylum Spirochaetes��DQ� LQH[SOLFDEOH�¿QGLQJ� WKDW�QHHGV� WR�EH�FRQ-¿UPHG�E\�IXUWKHU�WD[RQRPLF�VWXGLHV�

In the above list there is also a highly convergent order “De-halococcoidetes´^�`� WKDW� KDV� QRW� EHHQ� OLVWHG� LQ� Bergey’s Manual for the time being. It is this order that caused the otherwise convergent phylum “&KORURÀH[L” to drop out from the list of convergent phyla. The order “Dehalococ-coidetes” is located not far from “&KORURÀH[L”, as shown be-ORZ��ZKHUH��&!�DQG��*!�LQGLFDWH�&ODVV�DQG�*HQXV��

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192 The Bulletin of BISMiS

CVTrees support the Bergey’s Systematics

The branching scheme shown above may be used to test the SUHGLFWLYH� SRZHU� RI� &97UHH�� 7KH� FODVV� Thermomicrobia ZDV�RULJLQDOO\� GH¿QHG� DV� D� SK\OXP�DQG� D� FODVV�ZLWK� RQO\�one species, Thermomicrobium roseum��LQ�YROXPH���RI�Ber-gey’s Manual of Systematic Bacteriology�� /DWHU� RQ� LW�ZDV�proposed to transfer another species from the phylum Acti-nobacteria to this class and to transfer the entire class to the phylum “&KORURÀH[L´��+XJHQKROW]�HW�DO���������

Thermobaculum was not listed in the Bergey’s Manual�2XW-OLQHV�DQG� LW�ZDV�DVVLJQHG�D� VWDWXV�RI�XQGH¿QHG�SK\OXP� LQ�1&%,� WD[RQRP\�� +RZHYHU�� D� UHFHQW� FRPSDULVRQ� RI� JHQH�order in full genome data places it in the phylum “Chloro-ÀH[L´��.XQLVDZD���������7KHUHIRUH��DOO����JHQRPHV�VKRZQ�above, which form a monophyletic branch, may correspond WR�D�UHGH¿QHG�SK\OXP�³&KORURÀH[L´��:H�DQWLFLSDWH�WKLV�UH-vision in future editions of Bergey’s Manual. The fact that

“&KORURÀH[L” did not appear in the list of convergent phyla ZDV�FDXVHG�E\�ODJJLQJ�WD[RQRPLF�LQIRUPDWLRQ�DW�1&%,��RQ�ZKLFK�WKH�&97UHH�FROODSVLQJ�SURFHGXUH�GHSHQGV�

$V�D�GHWDLOHG�WD[RQ�E\�WD[RQ�FRPSDULVRQ�RI�&97UHH�SK\ORJ-eny with prokaryote taxonomy will be published elsewhere at a later time we omit similar but much longer lists of order, family, genus, and species convergence and touch on an ad-YDQFHG�IHDWXUH�RI�&97UHH�WKDW�JRHV�EH\RQG�WKH�UHDFK�RI���6�U51$�DQDO\VLV��QDPHO\��LWV�KLJK�UHVROYLQJ�SRZHU�IRU�VWUDLQV�

Limitations of 16S rRNA analysis

³$OWKRXJK� ��6� SK\ORJHQ\� LV� DUJXDEO\� H[FHOOHQW� IRU� FODV-VL¿FDWLRQ�RI�Bacteria and Archaea from the domain level down to the family or genus, it lacks resolution below that OHYHO´��6WDOH\��������)R[�HW�DO����������³7KH�VLQJOH�FDWHJR-U\� IRU�ZKLFK�668�VHTXHQFH�GLYHUJHQFHV� FDQQRW�SURYLGH�D�VKDUS�UHVROXWLRQ�LV�VSHFLHV´��<DU]D�HW�DO����������)RUWXQDWHO\��ZKROH�JHQRPH�EDVHG�&97UHHV�DUH�DEOH�WR�SURYLGH�KLJK�UHVR-OXWLRQ�DW� WKH� VSHFLHV�DQG� LQIUDVXEVSHFL¿F� OHYHOV�ZKLFK�DUH�urgently needed in ecological, environmental, clinical, and pharmaceutical studies.

/HW� XV� ¿UVW� ORRN� DW� VRPH� H[FHUSWV� IURP� WKH� JHQXV� FRQYHU-JHQFH�OLVW�

Edwardsiella^�`� .�.�.�.�.�

Eggerthella^�`� .�.�.�.�.�

Ehrlichia^�`� .�.�.�.�.�

Erwinia^�`� ����.�.�.�

Escherichia^��`� .���������

Exiguobacterium^�`� .�.�.�.�.�

Flavobacterium^�`� .�.�.�.�.�

Francisella^��`� .�.�.�.�.�

Frankia^�`� ��.�.�.�.�

… … … … … …

Salinibacter^�`� .�.�.�.�.�

Salinispora^�`� .�.�.�.�.�

Salmonella^��`� .�.�.�.�.�

Serratia^�`� .�.�.�.�.�

Shewanella^��`� .�.�.�.�.�

Shigella^�`� .�.�������

Sinorhizobium^�`� .�.�.�.�.�

�ZKHUH�³«�«�«´�GHQRWHV�RPLWWHG�OLQHV�LQ�D�ORQJ�OLVW��

What caused the “bad” convergence of the genera Esche-richia^��`�DQG�Shigella^�`"�%\�JRLQJ�WR�WKH�VSHFLHV�OHYHO��we see

Escherichia coli^��`� .�.�.�.�.�

Shigella boydii^�`� .�.�.�.�.�

6KLJHOOD�ÀH[QHUL^�`� ��.�.�.�.�

DOO�IRUP�ZHOO�GH¿QHG�VSHFLHV��+RZHYHU��LQ�WZR�SDSHUV��SXE-OLVKHG����\HDUV�DSDUW��3XSR�HW�DO���������=KRX�HW�DO����������the Shigella strains were shown by different methods to mixed with E. coli strains, thus violating the monophyletic-LW\�RI�WKH�ODWWHU��7KH�&97UHH�UHVXOWV�PD\�KHOS�WR�VKHG�OLJKW�on whether to put Shigella within the species Escherichia coli or just in the genus Escherichia as sister species to Escherichia coli.

$QRWKHU� H[DPSOH� FRPHV� IURP� WKH�Yersinia pestis and Yer-sinia pseudotuberculosis� SUREOHP�� $OWKRXJK� '1$±'1$�hybridization method could not distinguish them as two ge-QRPHVSHFLHV��D�SURSRVDO� WR�FKDQJH� WKH�FODVVL¿FDWLRQ�³ZDV�UHMHFWHG� E\� WKH� -XGLFLDO� &RPPLVVLRQ� EHFDXVH� RI� SRVVLEOH�danger to public health if there was confusion regarding Yersinia pestis�� WKH�SODJXH�EDFLOOXV´� �%UHQQHU�HW�DO����������

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+RZHYHU�� LQ�&97UHHV� WKHUH� LV� QR� FRQIXVLRQ� DW� DOO��$W� WKH�SUHVHQW�WLPH�WKHUH�DUH����JHQRPHV�EHORQJLQJ�WR�WKH�JHQXV�Yersinia, distributed in three species. They all form mono-SK\OHWLF�FOXVWHUV�

Yersinia^��`� .�.�.�.�.�

Yersinia pestis^�`� .�.�.�.�.�

Yersinia peudotuberculosis^�`� .�.�.�.�.�

Yersinia enterocolitica^�`� ����.�.�.�

7KHUHIRUH�� WKH� JHQXV� DQG� WKH� VSHFLHV� DUH� DOO�ZHOO� GH¿QHG��Yersinia pestis and Yersinia peudotuberculosis are distin-JXLVKDEOH� VSHFLHV��7KHUH� LV� QR� QHHG� IRU� WKH� -XGLFLDO�&RP-mission to be concerned.

2Q���2FWREHU�������GXULQJ�D�VKRUW�YLVLW�WR�%LHOHIHOG��WKH�DX-WKRU�XVHG�&97UHH�WR�REWDLQ�D�TXLFN�FRQ¿UPDWLRQ�RI�$OIUHG�3KXHOHU¶V�FRQMHFWXUH�WKDW�Rhizobium lupini�+�����LV�DFWXDOO\�an Agrobacterium strain very closely related to the strain &����:LEEHUJ�HW�DO����������7KLV�ZDV�MXVW�DQRWKHU�HSLVRGH�RI�the Agrobacterium–Rhizobium�GHEDWH��<RXQJ�HW�DO���������)DUUDQG� HW� DO��� ������<RXQJ� HW� DO��� ������� ,Q� WKH� �����JH-QRPH�&97UHHV�����JHQRPHV�RI�Agrobacterium and Rhizobi-um species, taken together, do form a monophyletic cluster, but the monophyleticity of Agrobacterium is violated by a PRQRSK\OHWLF�JURXS�RI�¿YH�Rhizobium strains.

Possible new higher rank taxa

&97UHHV� PD\� DOVR� SURYLGH� FOXHV� DERXW� WKH� LQWHUUHODWLRQ-VKLSV�DPRQJ�KLJKHU�UDQN�WD[D��:H�GUDZ�D�IHZ�H[DPSOHV��$V�mentioned before, the class Deltaproteobacteria does not IRUP�D�PRQRSK\OHWLF�EUDQFK�LQ�&97UHHV��2QH�RI�LWV�RUGHUV� Myxococcales, represented by nine genomes at this time, es-capes from the class as a whole and becomes juxtaposed with some other phyla as shown in the following branching VFKHPH��FXW�RXW�IURP�D������JHQRPH�&9WUHH�FROODSVHG�WR�WKH�SK\OXP�OHYHO��ZKHUH��3� and �2��LQGLFDWH�3K\OXP�DQG�2UGHU���

Therefore, the Myxococcales may comprise a separate phylum.

$V�DQRWKHU�H[DPSOH��ZH�QRWH� WKDW� WKH�JHQXV�Coprothermo-bacter, listed under Firmicutes in Bergey’s Manual of Sys-

tematic Bacteriology���QG�HGLWLRQ��YRO�����HDUQV�LWVHOI�D�SRVL-WLRQ�DW�WKH�SK\OXP�UDQN�LQ�&97UHHV�DV�IROORZV�

7KLV�SODFHPHQW�ZDV� VXSSRUWHG�E\�D���6� U51$�VXUYH\��GH-noting Coprothermobacter as an “established” phylum �6FKORVV�HW�DO���������

Instead of continuing with this type of example to be veri-¿HG�E\�WD[RQRPLVWV�LQ�WKH�IXWXUH��ZH�UHIHU�WR�VRPH�&97UHH�SUHGLFWLRQV�WKDW�KDYH�EHHQ�FRQ¿UPHG�LQ�WKH�SDVW�IHZ�\HDUV�

5HWURVSHFWLYH�YHULÀFDWLRQ�RI�&97UHHV

,Q� WKH�&97UHH�DSSURDFK� WKHUH� LV�QR�SDUDPHWHU�DGMXVWPHQW�or sequence selection, the only “change” consists in trees JHWWLQJ�ODUJHU�DQG�ODUJHU�ZLWK�QHZ�JHQRPHV�UHOHDVHG��2YHU�the years we have noticed that, as a rule, taxonomic revi-VLRQV� OHDG� WR� EHWWHU� DJUHHPHQW�ZLWK�&97UHH��7KLV� FDQ� EH�FRQVLGHUHG�DV�UHWURVSHFWLYH�MXVWL¿FDWLRQ�RI�&97UHHV��$�IHZ�examples follow.

The genus Oceanobacillus was listed under Gammapro-teobacteria��*DUULW\�HW�DO���������DQG�ZH�KDG�WR�DGPLW�WKLV�³FURVV�SK\OXP�GLVFUHSDQF\´� LQ� RXU�PDQXVFULSW� �+DR� HW� DO���������DV�LW�DSSHDUHG�LQ�DOO�&97UHHV�LQ�WKH�Firmicutes branch. Fortunately enough, by the time of proof-reading, we no-WLFHG�WKDW�LQ�WKH�QH[W�UHOHDVH�RI�WKH�7D[RQRPLF�2XWOLQH��*DU-ULW\�HW�DO���������LW�ZDV�PRYHG�WR�Bacillaceae.

The two genomes from the genus Thiomicrospira did not FRPH� WRJHWKHU� LQ�&97UHHV� DW� DOO�.� YDOXHV��:KLOH�Thiomi-crospira crunogena remains within Gammaproteobacteria, 7KLRPLFURVSLUD�GHQLWUL¿FDQV joins Epsilonproteobacteria in DOO�&97UHHV� �6XQ�HW�DO����������7KLV�VSHFLHV�ZDV� UHQDPHG�6XOIXULPRQDV�GHQLWUL¿FDQV�DQG�PRYHG�WR�WKH�(SVLORQ�JURXS�LQ�72%$�5HO�������*DUULW\�HW�DO���������

,Q� DOO� &97UHHV� VLQFH� ������ WKH� FODVV�Mollicutes, a mono-phyletic cluster of its own, never joins other classes of Fir-micutes. We were encouraged to see that this class has been removed from the Firmicutes to become a separate phylum, Tenericutes, in Bergey’s Manual of Systematic Bacteriology, �QG�HGLWLRQ��YRO�����%\�WKH�ZD\��WKH�JHQXV�Erysipelothrix as-signed to a new class in the Firmicutes in the above volume may also belong to Tenericutes�DFFRUGLQJ�WR�&97UHHV�

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194 The Bulletin of BISMiS

CVTrees support the Bergey’s Systematics

3HUKDSV�WKLV�LV�D�VXLWDEOH�SODFH�WR�QRWH�WKDW�LQ�D�QXPEHU�RI�FDVHV� WKH�&97UHH� SK\ORJHQ\� DJUHHV�ZLWK� ��6� U51$�DQDO-\VLV� �H�J��<DU]D� HW� DO��� ������ EXW� ERWK� GLIIHU� IURP� WKH� FXU-UHQW�FODVVL¿FDWLRQ��%HVLGHV�WKH�%HWD�JURXS�PL[LQJ�ZLWK�WKH�*DPPD�JURXS�RI�WKH�Proteobacteria, a phenomenon already mentioned, we see that Ureaplasma becomes inserted into Mycoplasma, and Pedicoccus pentosaceus becomes insert-ed into Lactobacillus, violating the monophyleticity of the latter two genera.

Conclusion and discussion

&97UHH� LV� FOHDUO\� DQ� HIIRUW� ³HQ� URXWH� WR� D� JHQRPH�EDVHG�FODVVL¿FDWLRQ�RI�Archaea and Bacteria´��.OHQN�HW�DO����������Using whole genomes is both a merit and a demerit of the approach. It is a merit in light of the genomic era when thousands of prokaryotic genomes will be available in the not-too-distant future and a genome contains the maximal amount of phylogenetic information at the molecular level. It is a demerit inasmuch as the number of sequenced ge-QRPHV�FDQ�QHYHU�FDWFK�XS�ZLWK�WKDW�RI�WKH���6�U51$�JHQH�VHTXHQFHV��+RZHYHU��&97UHH�PD\�VHUYH�DV�D�FRPSOHPHQW�WR� ��6� U51$�DQG�RWKHU� SK\ORJHQLHV�� KHOSLQJ�SODFH�PLFUR-bial systematics on a sound basis. When genome sequences become commonplace in microbial laboratories, it costs QR�PRUH�WR�XVH�&97UHH��MXVW�VXEPLW�D�JHQRPH�WR�WKH�:HE�6HUYHU�DQG�VHH�ZKHUH�WKH�VHTXHQFH�SODFHV�WKH�WD[RQ��7KHQ��if necessary, one can design more delicate phenotyping ex-periments to pursue a more in-depth study of phylogeny and taxonomy.

5HJDUGLQJ� WKH� UHODWLRQ�RI�&97UHH� WR�RWKHU�ZKROH�JHQRPH�based methods, we have mentioned the gene order study in FRQQHFWLRQ�ZLWK� WKH�XQGH¿QHG� WD[RQ�Thermobaculum��$Q-RWKHU� WRSLF�ZRUWK�PHQWLRQLQJ� LV�'1$±'1$�K\EULGL]DWLRQ�SHUIRUPHG�E\�WKH�SURJUDP�-6SHFLHV��5LFKWHU�HW�DO���������RU�WKH�**'&�:HE�6HUYHU��$XFK�HW�DO����������:H�PHQWLRQ�WZR�FDVHV�RI�FRPSDULQJ�WKH�HOHFWURQLF�'1$±'1$�K\EULGL]DWLRQ�UHVXOWV�ZLWK�&97UHH�SUHGLFWLRQV��7KH�¿UVW�FRQFHUQV�D�QHZO\�released genome of Cellvibrio gilvus, assigned to Gamma-proteobacteria�DW�1&%,��LQ�&97UHHV�LW�MRLQV�WKH�JHQXV�Cel-lulomonas with the phylum Actinobacteria��**'&�VXSSRUWV�WKH�&97UHH�SODFHPHQW��7KH�VHFRQG�H[DPSOH�LV�Burkholderia -9��UHOHDVHG�LQ�$XJXVW������DW�1&%,��&97UHH�DQG�**'&�both indicate that it is actually another Stenotrophomonas maltophilia strain, not a Burkholderia at all. We note, how-HYHU��ERWK� -6SHFLHV�DQG�**'&�DUH�QRW� DOLJQPHQW�IUHH�� DV�they make use of blast results.

Acknowledgements

2XU�ZRUN�UHSRUWHG�LQ�WKLV�PLQL�UHYLHZ�KDV�EHHQ�VXSSRUWHG�E\�WKH�1DWLRQDO�%DVLF�5HVHDUFK�3URJUDP�RI�&KLQD������3URM-

HFW�1R������&%��������DQG�6KDQJKDL�/HDGLQJ�$FDGHPLF�'LVFLSOLQH�3URMHFW�1R��%�����:H�WKDQN�'U�=��;X�IRU�ZULWLQJ�WKH� WUHH�FROODSVLQJ� VFULSW��'U�*��=XR� IRU� GRLQJ� WKH�'1$±'1$� K\EULGL]DWLRQ� FRPSXWDWLRQ�� DQG�'U� =��4XDQ� IRU� WKH�Agrobacterium–Rhizobium debate papers.

References

$XFK��$�)��� +��3�� .OHQN� DQG� 0�� *RHNHU�� ������ 6WDQGDUG�operating procedure for calculating genome-to-genome GLVWDQFH�RQ�KLJKO\�VFRULQJ�VHJPHQW�SDLUV��6WDQGDUGV�*H-QRPH�6FL��������±����

%UHQQHU��'�-���-�7��6WDOH\�DQG�1�5��.ULHJ��������&ODVVL¿FD-tion of procaryotic organisms and the concept of bacterial speciation. In %HUJH\¶V� 0DQXDO� RI� 6\VWHPDWLF� %DFWHUL-RORJ\�� �QG� HGQ�� YRO�� ���7KH�Proteobacteria�� 3DUW�$�� ,Q-WURGXFWRU\�(VVD\V��HGLWHG�E\�%UHQQHU��.ULHJ��6WDOH\�DQG�*DUULW\���6SULQJHU��1HZ�<RUN��SS����±���

&KX��.�+��� -��4L��=��*��<X�DQG�9��$KQ��������2ULJLQ� DQG�phylogeny of chloroplasts revealed by a simple correla-WLRQ�DQDO\VLV�RI�FRPSOHWH�JHQRPHV��0RO��%LRO��(YRO��28: ��±���

)DUUDQG��6�.���3�%��YDQ�%HUNXP�DQG�3��2JHU��������Agrobac-terium� LV� D�GH¿QDEOH�JHQXV�RI� WKH� IDPLO\�Rhizobiaceae. ,QW��-��6\VW��(YRO��0LFURELRO��53:�����±�����

)HOVHQVWHLQ��-��������phylip��3K\ORJHQ\�,QIHUHQFH�3DFNDJH��YHU�� ������$YDLODEOH� IURP� KWWS���HYROXWLRQ�JHQHWLFV�ZDVK-ington.edu/

)OHLVFKPDQQ��5�'���0�'��$GDPV��2��:KLWH��5�$��&OD\WRQ��(�)�� .LUNQHVV�� $�5�� .HUODYDJH� HW� DO�� ������ :KROH�JH-nome random sequencing and assembly of Haemophilus LQÀXHQ]D�5G��6FLHQFH�269:����±����

)R[��*�(���-�'��:LVRW]NH\�DQG�3��-XUWVKXN��������+RZ�FORVH�LV�WRR�FORVH����6�U51$�VHTXHQFH�LGHQWLW\�PD\�QRW�EH�VXI-¿FLHQW�WR�JXDUDQWHH�VSHFLHV�LGHQWLW\��,QW��-��6\VW��%DFWHULRO��42:���±����

)UDVHU��&�0��� -�'��*RFD\QH��2��:KLWH��0�'��$GDPV��5�$��&OD\WRQ��5�'��)OHLVFKPDQQ��&�-��%XOW��$�5��.HUODYDJH��*��6XWWRQ��-�0��.HOOH\��-�/��)ULWFKPDQ��-�)��:HLGPDQ��.�9��6PDOO��0��6DQGXVN\�� -��)XKUPDQQ��'��1JX\HQ��7�5��8W-WHUEDFN��'�0��6DXGHN��&�$��3KLOOLSV��-�0��0HUULFN��-��)��7RPE��%�$��'RXJKHUW\��.�)��%RWW��3��&��+X��7�6��/XFLHU��6�1��3HWHUVRQ��+�2��6PLWK��&�$��+XWFKLVRQ�DQG�-�&��9HQ-WHU��������7KH�PLQLPDO�JHQH�FRPSOHPHQW�RI�Mycoplasma genitalium��6FLHQFH�270�����±����

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Page 113: eprints.uni-kiel.deeprints.uni-kiel.de/13540/1/BulletinofBISMIS_2-2.pdf · Contents of Volume 2, part 2 Review A century of systematics of the genus Bacteroides IURP D VLQJOH JHQXV

195

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+XJHQKROW]�� 3�� DQG� (�� 6WDFNHEUDQGW�� ������ 5HFODVVL¿FD-tion of Sphaerobacter thermophilus from the subclass Sphaerobacteridae in the phylum Actinobacteria to the class Thermomicrobia��HPHQGHG�GHVFULSWLRQ��LQ�WKH�SK\-lum &KORURÀH[L��HPHQGHG�GHVFULSWLRQ���,QW��-��6\VW��(YRO��0LFURELRO��54:�����±�����

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196 The Bulletin of BISMiS

CVTrees support the Bergey’s Systematics

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