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CHAPTER TWO

The Future of TaxonomyAmanda Lousie Jones1Department of Biology, Food and Nutritional Sciences, School of Life Sciences, Northumbria University,Newcastle upon Tyne, United Kingdom1Corresponding author: e-mail address: [email protected]

Contents

1.

AdvISShttp

Introduction

ances in Applied Microbiology, Volume 80 # 2012 Elsevier Inc.N 0065-2164 All rights reserved.://dx.doi.org/10.1016/B978-0-12-394381-1.00002-7

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2. The Past 25 3. The Present 26 4. The Future 29 Acknowledgment 33 References 33
Abstract

Microbial systematics has always been a misunderstood scientific discipline. It is readilyassumed that systematists use antiquated techniques to examine themolecular, morpho-logical, physiological, and biochemical properties of microorganisms. It is also believedthat the circumscription of novel taxa is not essential let alone a requirement and it isdue to this that systematics has become a dying art. It is rarely appreciated that system-atics is a discipline that is essential to all sciences and that without the use of current tech-niques, descriptions of novel species or higher taxa cannot be correctly published. SinceWoese and colleagues first publicized the use of the small subunit ribosomal RNA as amolecular tool, phylogenetic analysis of 16S rRNA gene sequences has become an essen-tial step in the polyphasic approach of microbial systematics. However, this moleculartechnique has limitations which have become apparent, and therefore it is evident thatfull genome comparisons are soon going to be a requirement for the full circumscriptionof novel taxa. The next generation of sequencing technology has enabled more informa-tion to be incorporated into the full systematic picture and that is immense as it is only thestart of the genomic era. It is hoped that high-throughput sequencing will complimentpolyphasic data rather than throwing a different light on it and thus soon become anessential minimal standard for taxonomic descriptions.

1. INTRODUCTION

Systematics is a fundamental discipline to the field of microbiology. It has

an impact in all aspects of microbiological sciences, frommedical microbiology,

environmental microbial studies to the investigations in the biotechnological

23

24 Amanda Lousie Jones

field. This immense impact is due to the ability of systematics to achieve three

goals introduced by Cowan (1965), namely, classification, identification, and

nomenclature. Classification is the ordering of microorganisms into taxonomic

groups; this tends to be based on their numerous differences and similarities,

with reliance upon the differences for most of the analytical techniques (Zhi,

Zhao, Li, & Zhao, 2012). Identification can be established by comparison with

key characteristics of previously described taxa and can result in unknown

microorganisms being identified as members of known species or subsequently

requiring classification as a novel taxa (Zhi et al., 2012). Nomenclature is the

third goal of systematics (Sutcliffe, Trujillo, & Goodfellow, 2012) and this is

also an essential part of systematics and is directed by the International Code

of Nomenclature of Bacteria (Sneath, 1992) to ensure microorganisms are

given internationally recognized names, as well as denoting the taxonomic

hierarchy, such as species, genus, family, and order (Zhi et al., 2012).

A fourth goal of systematics has been recently suggested by Staley (2010),

which is that comprehending microbial diversity is also a benefit. The use of

16S rRNA gene sequence analysis has enabled microbial taxonomists to

understandmicrobial communities, particularly by “deep” sequencing, which

has resulted in a greater understanding of the microbial diversity within these

environments, in particular highlighting the number of taxa present in micro-

bial communities and what has not been cultured at present. The process of

microbial descriptionhas improved,with greater than9000prokaryotic species

described so far, andover 50% in the last decade.However, it is still thought that

the currently described species only account for less than 1% of the microbial

diversity present (Sutcliffe et al., 2012). It is thought that current methods are

dated and new approaches such as genomics are required. Iverson et al. (2012)

have recently documented the development of novel computer software that

enables full genomesobtained fromametagenomic analysis of amicrobial com-

munity. Using next-generation sequencing, the software analyzed the data

obtained, thus enabling the production of individual genomes of all microbes

present (Iverson et al., 2012). This technology would enable the genomes of

previously unculturedmicroorganisms to be obtained and provides the oppor-

tunity for cultivation strategies for these organisms to be devised.

These techniques are the future of microbial taxonomy and ecology, and

there are misconceptions that microbial taxonomists do not exploit these

modern techniques and instead prefer to utilize well-established methodol-

ogy. However, this concept is not truewith thework of Peter Sneath bringing

the advent of numerical taxonomy in 1957, an early adoption of computa-

tional techniques to be exploited by systematists (Sneath & Sokal, 1973)

25The Future of Taxonomy

and then Rita Colwell established the use of polyphasic taxonomy to improve

taxonomic descriptions (Colwell, 1970). Finally, the addition of the phyloge-

netic analysis of the 16S rRNA gene sequence by Carl Woese and colleagues

enabled a better understanding of the microbial world (Woese & Fox, 1977).

To better appreciate the future applications that will be available to systema-

tists, we need to look at the previous studies and the resources available, these

then need to be compared with the current techniques, the protocols used,

and the standards required, to aid the understanding of the applications that

are required and give a better indication of the microbial taxonomic needs

for the not too distant future.

2. THE PAST

Since Ferdinand Cohn, in the 1870s, the ability to classify microor-

ganisms was based on microbial physiology, pathogenicity, products they

produce, and their morphological appearance. This later improved with

the Society of American Bacteriologists’ Committee on Bacterial Classifica-

tion and Nomenclature using additional criteria such as growth conditions

to aid genus descriptions (Logan, 1994). In 1923, Bergey’s manual of determi-

native bacteriology was published in a bid to provide an identification scheme

based on phenetic traits, biochemical profiles, morphological traits, and nu-

tritional requirements. This became the first out of eight editions that were

subsequently published (Logan, 1994). However, after the eighth edition in

1974, it was found that the system created was not appropriate, leading to

unrealistic groupings of microorganisms (Logan, 1994). This led to the

decision for proposals of new bacterial names to be validly published or their

descriptive publication to be approved in the International Journal of Systematic

Bacteriology, now known as the International Journal of Systematic and

Evolutionary Microbiology. This journal is the “cornerstone” of microbial

systematics and adheres to the strict guidelines of the Bacteriological Code

(www.ijs.sgmjournals.org).

During this time of change and uncertainty, Peter Sneath brought to

light the use of computers for taxonomic analyses. The numerical taxonomic

techniques that were originally proposed and later established were referred

to as Adansonian taxonomy, following the principles of Adanson, of study-

ing phenetic differences and traits. Numerical taxonomy involved grouping

microorganisms, referred to as operational taxonomic units (Sneath & Sokal,

1973), by numerical methods into taxonomic units based upon the organ-

isms’ characteristics. The important characteristic of this technique was that


each character is of equal importance and therefore in the analysis has equal

weighting (Priest & Austin, 1993). Once the computer analysis has been per-

formed, certain traits could then be deemed of higher importance and used

as differential characteristics. The types of traits that are taken into consid-

eration are morphological data, growth requirements, biochemical analysis,

antibiotic inhibitory analyses, and carbon source utilization data.

In 1970, it was proposed by Rita Colwell that polyphasic taxonomy was

the next progressive step for improving bacterial classification (Colwell,

1970). This approach enabled traits of phenotypic and genotypic nature

to be analyzed, and therefore classifications to be based on a consensus of

high-quality data. The characteristics that were analyzed were phenetic traits

such as those used in numerical taxonomy, chemical analysis of the cell wall

(chemotaxonomy), and genotypic data such as DNAGþC content (mol%).

The extensive incorporation of the polyphasic approach into taxonomy has

led to an improved classification system, resulting in improved identifica-

tions, which is evident in the recent edition of Bergey’s manual of systematic

bacteriology (de Vos et al., 2009) and is now seen to be the “gold standard

approach” for taxonomic descriptions.

The start of the molecular era saw the use of the small subunit ribosomal

RNA (16S rRNA), with Carl Woese and colleagues demonstrating the

application of phylogenetic analysis to determine that Archaea form their

own kingdom, which enabled a better understanding of the microbial world

(Woese & Fox, 1977). At the beginning of the use of this molecular marker,

only small sections of the gene were able to be amplified and analyzed and Sabvalues calculated (Woese, 1987). In addition to the sequencing data, DNA:

DNA hybridization of genomic DNA was becoming more prevalent since

it was first reported by Johnson and Ordal (1968). Wayne et al. (1987)

subsequently illustrated how a cut-off point of 97% of the 16S rRNA gene

sequence similarity is indicative of a novel species, which was found to be

comparable to a 70% threshold using the DNA:DNAhybridization technique

(Wayne et al., 1987). This has subsequently led to DNA:DNA hybridization

as being considered as the “gold standard” in microbial classification.

3. THE PRESENT

Since the advent of PCR-based 16S rRNA gene sequence analysis,

microbial taxonomy has not changed dramatically; however, the different

aspects of taxonomy have been clarified for better understanding by scien-

tists. It has been suggested that there are different stages of taxonomy, and


these should be referred to as alpha, beta, and gamma. The alpha taxonomic

stage is the classification of species, the naming, and the identification (Zhi

et al., 2012). The beta taxonomy is the assignment of species to a natural clas-

sification, based on their phylogeny but also chemotaxonomy, phenotypic,

and additional genotypic information. Natural classifications are based on

the phenetic approach, which is based on the whole organisms’ attributes,

phenotype, and genotype, with natural phylogenetic classifications based on

evolution (Priest & Austin, 1993). The final stage known as gamma taxonomy

is based on intraspecific categories, such as subspecies and ecotypes, although

most of these investigations are carried out by ecologists (Zhi et al., 2012).

The current approach to the description of a novel taxon would be to

initially perform a phylogenetic analysis of the isolate with an almost com-

plete 16S rRNA gene sequence in comparison with each type strain from

the genus, the isolate was most similar to from the nBLAST search

(Altschul, Gish, Miller, Myers, & Lipman, 1990), in addition to representa-

tive type species residing within the same order. This analysis enables the

visualization of the phylogenetic positioning of the isolate in question within

the order, but a further analysis of the nucleotide differences and percentage

similarity between the strains analyzed gives a better indication of the novelty

of the organism. If the isolate is deemed presumptively novel, additional phy-

logenetic algorithms should be performed to ensure parity in the analysis pres-

ented.The algorithms that tend to be chosen are least-squares likelihood (Fitch

& Margoliash, 1967), neighbor-joining (Saitou & Nei, 1987), maximum-

likelihood (Felsenstein, 1981), and maximum-parsimony (Kluge & Farris,

1969) methods along with evolutionary distance matrices prepared after Jukes

and Cantor (1969). In addition, the unrooted tree topologies are further eval-

uated with the use of a bootstrap analysis (Felsenstein, 1985) based on 1000

resamplings. In addition to the phylogenetic analysis, the DNAGþC content

(mol%) should be ascertained, along with DNA:DNA hybridization

depending on the percentage of 16S rRNA gene similarity of the isolate

and its closest neighbor.

The delineation of a novel species is currently a tricky situation, with sys-

tematists differing in the choice of tree algorithms and with the multiple ver-

sions of 16S rRNA operon, which can have differences from 2% to 5%

(Kampfer, 2012). Moreover, the 16S rRNA gene has become limited in

its use for taxonomic characterization of many taxa. For example, members

of the genus Tsukamurella are not able to be defined with the phylogenetic

analysis of 16S rRNA gene sequence and therefore more reliance is placed

onDNA:DNAhybridization (Goodfellow&Kumar, 2012). Unfortunately,


the previously stated 70% cut-off for DNA:DNA hybridization data, equat-

ing to�97% 16S rRNA gene sequence similarity, can also be debatable with

a more realistic value of >70%, that is readily seen particularly within the

genus Rhodococcus, with evidence that the cut-off point for members of

the genus Rhodococcus needs to be set at 80% (Goodfellow, Chun,

Stackebrandt, & Kroppenstedt, 2002). Additional limitations of the 16S

rRNA gene sequence are also seen with the lack of resolution of higher taxa;

however, there are other limitations in the classification of higher taxa with

the lack of phenotypic data and even further molecular data.

The next stage in the descriptive process is to examine the novel isolate

along with its nearest neighbors, which would have been determined from

the phylogenetic analysis, by phenotypic characterization. The types of anal-

ysis that would be performed are the morphological appearance of the isolate

after growth on specific nutritious media for a specified time and tempera-

ture. Micro-morphological characteristics will also be examined such as

spore forming and motility, and it is also essential to establish the morpho-

logical life cycle of the isolate. The nutritional requirements of the novel

isolate are the next criteria to establish. These analyses tend to take the form

of utilization of carbohydrates and organic acids (Shirling & Gottlieb, 1966);

in addition, the degradation of a number of compounds is analyzed

(Goodfellow & Pirouz, 1982; Gordon, Barnett, Handerha, & Pang, 1974)

along with antimicrobial susceptibility testing (Groth et al., 2004) and

enzyme activities, which tends to be ascertained by the use of API ZYM

test kits (bioMerieux). Finally, the isolate would be subjected to tolerance

testing for temperature, pH, and NaCl concentrations. The data from all

of the phenotypic assessment, which can amount to over 100 tests, will

be incorporated into the taxonomic description; however, a minimum of

20 characteristics will need to be documented to establish differences

between the related taxa tested.

The final stage for a novel species description is to ascertain the isolates’

cell wall chemotype (Lechevalier & Lechevalier, 1970). This is determined

by examining the diagnostic isomers of diaminopimelic acid (A2pm; Staneck

& Roberts, 1974) and whole-organism sugars (Hasegawa, Takizawa, &

Tanida, 1983). Additional key chemotaxonomic markers should also be

established, including fatty acid methyl ester analysis (Komagata & Suzuki,

1987), determination of the predominant isoprenoid quinones (Collins,

1994), muramic acid type (Uchida, Kudo, Suzuki, & Nakase, 1999), the

presence and length of mycolic acids (Minnikin, Alshamaony, &

Goodfellow, 1975), and the polar lipid profile (Minnikin et al., 1984). Until


recently, whole cell protein analysis was performed by Curie point mass

spectrometry (Ferguson, Ward, Sanglier, & Goodfellow, 1997; Sanglier,

Whitehead, Saddler, Ferguson, & Goodfellow, 1992). Pyrolysis mass

spectrometry data were examined using combined principal component

and canonical variate analyses (Windig, Haverkamp, & Kistemaker,

1983), thus enabling the clustering of pyrogroups, groups that tended to

differentiate between the environments isolates are cultivated from. This

technique has since become redundant with differing mass spectrometry

techniques taking its place.

It needs to be kept in mind that the examination and the subsequent

description of novel taxa should conform to the minimal standards for

the taxon, and the strains which the novel taxa are most related too.

The aim of the minimal standards is to provide a guidance on the descrip-

tion of novel taxa and to direct the appropriate testing required to establish

the taxonomic positioning of the isolate in question (Whitman, 2012).

However, the number of available minimal standards covers only a tiny

fraction of known microbial diversity. A number of members within

the taxonomic community think that the polyphasic approach and the cur-

rent battery tests required are costly in time and money. Moreover, in

many cases, the taxonomic utility of these tests is undermined by the cur-

rent situation whereby 70% or more novel taxa are described based on sin-

gle strains (Sutcliffe et al., 2012). With the start of the genomic era, it can

be decided which tests should be used to create a new “gold standard”

along with novel and upcoming genomic techniques.

4. THE FUTURE

Genomics is the future of systematics; however, its full potential has

yet to be fully realized and exploited. Since the start of the genomic era, sci-

entists have started to use genomes to assess the phylogenetic relationships

between organisms, with a variety of techniques used including the order

of the genes being examined, analysis of the shared genes, and finally, the

construction of super trees (Beiko, Harlow, & Ragan, 2005; Belda,

Moya, & Silva, 2005; Ciccarelli et al., 2006; Ding et al., 2008; Gao &

Gupta, 2012; Lathe, Snel, & Bork, 2000; Snel, Bork, & Huynen, 1999).

The results from these differing analyses do not match the current

phylogenetic relationships established by phylogenetic analysis of the 16S

rRNA gene sequence, as the genomes are dynamic as well as much more

diverse than the phenotypes, genotypes, and chemotypes illustrated


(Gao & Gupta, 2012; Gogarten, Doolittle, & Lawrence, 2002; Gogarten

& Townsend, 2005; Lawrence & Hendrickson, 2005; Snel, Huynen, &

Dutilh, 2005).

It is thought that bacterial genomes can have between 0% and 20% genes

obtained by horizontal gene transfer (HGT), which can be seen in some in-

stances as a process of evolution such as the transfer of antibiotic resistance

which does not occur in conserved regions of the genome. Definite HGT is

usually when genes are found only in a particular genome which is

phylogenetically diverse from other genomes containing the specific genes.

However, with genomes containing homologues, it is harder to unravel

where the HGT started and if it happened, although HGT is not readily seen

in genes involved in transcription and translation. HGT has already thrown

questions on using single genes for phylogenetic trees, such as 16S rRNA

gene, and therefore, it is thought that core genes in plural should be used

for better differentiation (Gao & Gupta, 2012).

It is seen that genomes of related taxa can be very different. Current phy-

logenetic analysis of genomes illustrates that strains within species can be

very different and may indicate that the taxonomic positioning is too rigid

and strains are too wide a term and further differentiation is required. This

issue with phylogenetic analysis of genes may lead to modification of the

methods required for species description (Gao & Gupta, 2012). One

suggested method is the use of conserved inserts and deletions (indels) in

gene/proteins sequences which are classed as rare genetic elements, which

could be used for the phylogeny of microorganisms. This is due to indels

being flanked by conserved regions and therefore possess a reliability insur-

ance, also the rarity and highly specific nature of these types of changes make

their characteristics good candidates, as well as the difference in evolutionary

rates should not affect the indel or the interpretation of it. In addition,

genetic elements could be incorporated at any time during evolution and

therefore the identifications of indels at different phylogenetic depths

become possible (Gao & Gupta, 2012).

Another analysis that can be derived from genomic information is

conserved signature proteins or lineage-specific proteins. This is usually a

number of specific proteins which are unique to certain strains, species,

or higher taxa (Gao & Gupta, 2012). Alternatively, systematists can analyze

single-nucleotide polymorphisms which can be exploited as tools for

genome relatedness studies as well at chromosomal and gene levels (Zhi

et al., 2012). Staley (2009) suggested a phylogenomic species concept which

involves more information from the genomic data via a multilocus sequence


analysis, an in-depth approach involving the use of housekeeping genes as they

evolve slowly and at a constant rate, which should give a good understanding

of true phylogenetic relationships. This technique is thought to be a possible

replacement of DNA:DNA hybridization; however, whole genome compar-

isons using average nucleotide identity (ANI; Konstantinidis & Tiedje, 2005),

which compares the shared genes between two genomes, have shown to give

the best correlation with DNA:DNA hybridization, with 95–96% ANI cor-

relating with the 70% cut-off for DNA:DNA hybridization data (Goris et al.,

2007; Konstantinidis & Tiedje, 2005). However, prokaryotic species concepts

should be based on more than one characteristic, such a phenotypic or

genotypic, and also be based on more than one type of analysis, that is,

the phylophenetic species is based on DNA:DNA hybridization, 16S

rRNA gene sequence analysis, and phenotypic descriptions to establish a

taxonomic species (Zhi et al., 2012).

Previous chemotaxonomic, phenotypic, and genotypic data classed in this

instance as phenotypes can be correlatedwithmolecular phenotypes, with ref-

erence to genomic data. However, a full understanding of metabolic and bio-

synthetic processes will be needed when using genomic data for taxonomic

comparisons. An example of this is the analysis of isoprenyl diphosphate

synthase, an enzyme which is involved in the determination of the men-

aquinone chain length in actinomycetes, yet it will be uncertain when the

change length is terminated (Zhi et al., 2012). However, the menaquinone

biosynthetic pathway has shown differing genes involved and therefore has

been shown as a useful aid in speciation. Care needs to be taken when looking

at genomic information as the presence of a specific gene is not necessarily

indicative that gene expression will occur. It also needs to be considered that,

when using genomic data, it will have to be fully analyzed as the core genome

may indicate essential function, although still can be dispensable which may

not aid classification of species but may aid higher taxa to be classified; how-

ever, the peripheral genome which relates to survival in niches environments,

such as biochemical pathways which are essential for bacterial growth, will

enable more accurate classification of taxa (Zhi et al., 2012).

The recommendation of Zhi et al. (2012) is that the phylogenomic back-

bone of microbial systematics should be merged with biochemical traits,

physiological traits, morphological traits, and the biology of the organism.

This will enable a full understanding of the evolution and taxonomic

relationships between taxa in regard to both their taxonomic positioning

and relationships between microbes residing in the same environmental

niche. Also, until an agreed approach to establish the phylogenetic


positioning of taxa by using genomic data, DNA GþC content (mol%) and

DNA:DNA hybridization, via ANI or multilocus sequence typing, can be

achieved by using the genomic data alone. Therefore, it is becoming apparent

that draft genomes are soon going to be requiredwith each species description,

especially as the cost of analyzing genomes is coming down especially with

next-generation sequencing (Sutcliffe et al., 2012). Genomic analyses would

enable ecological and physiological insights along with the taxonomy of mi-

croorganisms through their diverse metabolic systems. Since “deep” sequenc-

ing of microbial communities can be achieved, culturable and nonculturable,

niche adaptation can be assessed, including defining the human microbiome,

the pathogenic potential, and disease states in the human body.

For a species description in the future, more than one isolate should be

analyzed although this is in an ideal situation and a rare occurrence, with a

genome of the type strain, along with a selection of phenotypic characters

to be analyzed which could take the form of phenotypic microarray panels.

Phenotypicmicroarray is a rapidmethod to ascertain phenotypic characteristics

and if the same protocol was used then possibly a database could be created and

utilized so that only a handful of panelswould need to be performed per species

description. In addition, the phenotypicmicroarray can also give a comparison

with the genomic informationonmetabolicpathways (Bochner, 2009).Anad-

ditional analysis that could be incorporated in the future descriptive studies is

mass spectral analysis by MALDI–TOF–mass spectrometry. This analysis has

been readily incorporated in clinicalmicrobiological laboratories. Standardized

protocols of a selected few chemotaxonomic markers would also enable the

storage of data online and therefore preventing the numerous tests being

repeated. The absence of online databases indicates that taxonomy is currently

behind the times,with the lack of databases hindering the developmentof rapid

and cost-effective methods.

It is evident that a new era of systematics is rapidly approaching and

hopefully it will be a high-throughput era, enabling the descriptions of

numerous taxa but in a cost- and time-effective format. It will hopefully en-

able systematists to concentrate onmicroorganisms of importance in the bio-

technological and clinical fields. However, this will only be of benefit if the

sources of information are frequently updated and widely available, and

therefore, it would be appropriate for the next and subsequent editions of

Bergey’s manual of systematic microbiology to become an online version, with

access to databases and genomic information, and therefore usable by all

microbiologists. An example of a information resource that can be combined

with additional resources is the Genomic Encyclopaedia of Bacteria and


Archaea (Wu et al., 2009). Microbial taxonomy is an art form, and possibly a

dying one, as emphasized in reports from the UK House of Lords Science

and Technology Committee (2007–2008) and the Review Team at the

Natural History Museum (Boxshall & Self, 2010). Therefore, building a sus-

tainable future for taxonomy is paramount to the survival of systematists and

a fundamental discipline.

ACKNOWLEDGMENTThe author is grateful to I.C. Sutcliffe for a critical reading of the manuscript and comments.

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