the microbial diversity of inland waters

6
The microbial diversity of inland waters Martin W Hahn The conservation and sustainable use of freshwater resources is of global importance. Microorganisms are not only the most abundant organisms in natural freshwater systems, but are also key players in ecological processes controlling water quality. Detailed knowledge of the diversity and function of microorganisms dwelling in freshwater habitats is an essential prerequisite for the sustainable management of freshwater resources. Freshwater systems are inhabited by microbial communities that are indigenous to this habitat type and usually do not occur in marine systems, saline inland waters and terrestrial habitats. Despite recent advances in the characterization of the diversity of freshwater microorganisms, knowledge essential for a holistic understanding of their ecological roles is still lacking. Addresses Institute for Limnology, Austrian Academy of Sciences, Mondseestrasse 9, 5310 Mondsee, Austria Corresponding author: Hahn, Martin W ([email protected]) Current Opinion in Biotechnology 2006, 17:256–261 This review comes from a themed issue on Environmental biotechnology Edited by David A Stahl and Michael Wagner Available online 15th May 2006 0958-1669/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. DOI 10.1016/j.copbio.2006.05.006 Introduction Inland waters, including lakes, ponds, rivers, streams, wetlands and groundwater (water beneath the earth’s surface), consist of either freshwater or saline water. Fresh- water is water with a salt content (salinity) of less than 1gL 1 , while saline waters are characterized by salinities >1gL 1 . The saline inland waters are mainly represented by saline ground water systems and saline lakes. The latter include inland seas such as the Caspian Sea and the Dead Sea. Inland waters contain only 0.5% of the total global water and only 20% of the total amount of freshwater (the other 80% are contained in glaciers and polar ice), but comprise almost 100% of the freshwater resources utilized by the human population. Freshwater is an essential ele- ment of daily life, as well as an essential resource for many industrial and agricultural processes. Clean and predict- able supplies of freshwater drive the economic and eco- logical systems on which we depend, making the sustainable development of freshwater resources among the most pressing of global challenges today. Microorganisms, including bacteria, archaea, protists (protozoa and algae) and fungi, numerically and bio- chemically dominate all inland water habitats. Some of these microorganisms are key players in biogeochemical processes (e.g. the metabolization of dissolved organic carbon or nitrogen cycling) that are crucial processes for entire ecosystems. Furthermore, microorganisms are major players in processes controlling the water quality of inland waters, and they are crucially involved in the fate of pollution released to the environment. Owing to the rapidly increasing importance of the sustainable management of freshwater resources, detailed knowledge on the diversity, specific functions and ecology of micro- organisms inhabiting freshwater ecosystems is urgently needed. Obtaining such information was not possible for most aquatic microbes until the 1990s, because the majority of microorganisms lack morphological traits sui- table for discriminating species and a large proportion of microorganisms are difficult to cultivate. The advent of molecular techniques opened up new avenues of research on the diversity and function of microorganisms in inland waters. This review summarizes recent advances in this important field of research, and especially highlights the advances in research on bacteria inhabiting inland waters. Important results obtained for other microorganisms dwelling in inland water habitats could not be included because of space constraints. The discovery of ‘typical freshwater bacteria’ Bacteria usually represent >90% of microorganisms in non-extreme aquatic habitats. In the 1980s, it was believed that bacterial species inhabiting freshwater sys- tems do not differ taxonomically from bacteria inhabiting the surrounding terrestrial environments [1]. Only Gram- positive bacteria (i.e. Actinobacteria and Firmicutes) were considered to be absent from the water column (pelagic zone) of freshwater habitats. These assumptions were based on cultivation experiments that resulted, on the one hand, in the isolation of the same opportunistic taxa (e.g. Pseudomonas spp.) from soil and freshwater samples and, on the other hand, in the isolation of only a few Gram-positive bacteria (Actinobacteria and Firmicutes) from freshwater sites. The publication of the first inves- tigations on the bacterial diversity of freshwater lakes conducted by cultivation-independent methods radically changed this view [2–5]. An inventory of the bacterial taxa was carried out using direct nucleic acid isolation, fol- lowed by the amplification and sequencing of bacterial 16S rRNA genes. Comparing sequences retrieved from freshwater habitats with sequences deposited in public databases enabled the identification of bacterial taxa present in the investigated habitats, or at least the Current Opinion in Biotechnology 2006, 17:256–261 www.sciencedirect.com

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Page 1: The microbial diversity of inland waters

The microbial diversity of inland watersMartin W Hahn

The conservation and sustainable use of freshwater resources

is of global importance. Microorganisms are not only the most

abundant organisms in natural freshwater systems, but are also

key players in ecological processes controlling water quality.

Detailed knowledge of the diversity and function of

microorganisms dwelling in freshwater habitats is an essential

prerequisite for the sustainable management of freshwater

resources. Freshwater systems are inhabited by microbial

communities that are indigenous to this habitat type and usually

do not occur in marine systems, saline inland waters and

terrestrial habitats. Despite recent advances in the

characterization of the diversity of freshwater microorganisms,

knowledge essential for a holistic understanding of their

ecological roles is still lacking.

Addresses

Institute for Limnology, Austrian Academy of Sciences,

Mondseestrasse 9, 5310 Mondsee, Austria

Corresponding author: Hahn, Martin W ([email protected])

Current Opinion in Biotechnology 2006, 17:256–261

This review comes from a themed issue on

Environmental biotechnology

Edited by David A Stahl and Michael Wagner

Available online 15th May 2006

0958-1669/$ – see front matter

# 2006 Elsevier Ltd. All rights reserved.

DOI 10.1016/j.copbio.2006.05.006

IntroductionInland waters, including lakes, ponds, rivers, streams,

wetlands and groundwater (water beneath the earth’s

surface), consist of either freshwater or saline water. Fresh-

water is water with a salt content (salinity) of less than

1 g L�1, while saline waters are characterized by salinities

>1 g L�1. The saline inland waters are mainly represented

by saline ground water systems and saline lakes. The latter

include inland seas such as the Caspian Sea and the Dead

Sea. Inland waters contain only 0.5% of the total global

water and only 20% of the total amount of freshwater (the

other 80% are contained in glaciers and polar ice), but

comprise almost 100% of the freshwater resources utilized

by the human population. Freshwater is an essential ele-

ment of daily life, as well as an essential resource for many

industrial and agricultural processes. Clean and predict-

able supplies of freshwater drive the economic and eco-

logical systems on which we depend, making the

sustainable development of freshwater resources among

the most pressing of global challenges today.

Current Opinion in Biotechnology 2006, 17:256–261

Microorganisms, including bacteria, archaea, protists

(protozoa and algae) and fungi, numerically and bio-

chemically dominate all inland water habitats. Some of

these microorganisms are key players in biogeochemical

processes (e.g. the metabolization of dissolved organic

carbon or nitrogen cycling) that are crucial processes for

entire ecosystems. Furthermore, microorganisms are

major players in processes controlling the water quality

of inland waters, and they are crucially involved in the

fate of pollution released to the environment. Owing to

the rapidly increasing importance of the sustainable

management of freshwater resources, detailed knowledge

on the diversity, specific functions and ecology of micro-

organisms inhabiting freshwater ecosystems is urgently

needed. Obtaining such information was not possible for

most aquatic microbes until the 1990s, because the

majority of microorganisms lack morphological traits sui-

table for discriminating species and a large proportion of

microorganisms are difficult to cultivate. The advent of

molecular techniques opened up new avenues of research

on the diversity and function of microorganisms in inland

waters. This review summarizes recent advances in this

important field of research, and especially highlights the

advances in research on bacteria inhabiting inland waters.

Important results obtained for other microorganisms

dwelling in inland water habitats could not be included

because of space constraints.

The discovery of ‘typical freshwater bacteria’Bacteria usually represent >90% of microorganisms in

non-extreme aquatic habitats. In the 1980s, it was

believed that bacterial species inhabiting freshwater sys-

tems do not differ taxonomically from bacteria inhabiting

the surrounding terrestrial environments [1]. Only Gram-

positive bacteria (i.e. Actinobacteria and Firmicutes) were

considered to be absent from the water column (pelagic

zone) of freshwater habitats. These assumptions were

based on cultivation experiments that resulted, on the

one hand, in the isolation of the same opportunistic taxa

(e.g. Pseudomonas spp.) from soil and freshwater samples

and, on the other hand, in the isolation of only a few

Gram-positive bacteria (Actinobacteria and Firmicutes)from freshwater sites. The publication of the first inves-

tigations on the bacterial diversity of freshwater lakes

conducted by cultivation-independent methods radically

changed this view [2–5]. An inventory of the bacterial taxa

was carried out using direct nucleic acid isolation, fol-

lowed by the amplification and sequencing of bacterial

16S rRNA genes. Comparing sequences retrieved from

freshwater habitats with sequences deposited in public

databases enabled the identification of bacterial taxa

present in the investigated habitats, or at least the

www.sciencedirect.com

Page 2: The microbial diversity of inland waters

Microbial diversity of inland waters Hahn 257

identification of their closest relatives. Most bacterial

sequences retrieved from freshwater habitats were

neither affiliated with known bacterial species nor repre-

sented those phylogenetic groups previously obtained

from freshwater habitats using cultivation methods.

Further investigations also demonstrated that freshwater

and marine bacterioplankton differ substantially in com-

position [6,7]. Cultivation-independent investigations

showed that, in contradiction to previous assumptions,

Gram-positive bacteria are present in freshwater habitats

[3,8,9]. In fact, Actinobacteria were found to comprise large

fractions of bacterioplankton in many freshwater habitats

[9] and Firmicutes were also detected in some freshwater

systems [10�]. In a meta-analysis of previously published

studies, Zwart and coauthors [11] demonstrated that the

majority of bacterial sequences retrieved from freshwater

habitats were most closely related to other freshwater

clones, whereas relatively few were most closely related

to sequences recovered from soil or marine habitats. They

concluded from the habitat-specific clustering that most

bacteria inhabiting freshwater systems are indigenous to

freshwater, and they coined the term ‘typical freshwater

bacteria’ for these organisms [11]. The authors also pre-

sented 34 phylogenetic clusters of bacteria representing

typical inhabitants of freshwater systems (Table 1). Most

of these genus-like clusters did not contain either

described species or cultivated representatives [11],

and therefore nothing or little is known about the phy-

siology and ecological function of members of these

groups.

Ecological factors shaping the compositionof bacterial communitiesSeveral studies demonstrated that the bacterial commu-

nity composition (BCC) of lakes varies temporarily and

spatially within habitats [12–15], as well as between

habitats [15–18]. Several ecological factors shaping

Table 1

Examples of typical freshwater bacteria.

Group Phylum/class Ecological plasti

ACK-M1b Actinobacteria High

Polynucleobacter Betaproteobacteria High

GKS98 Betaproteobacteria High

R-BT065d Betaproteobacteria nke

SOLf Bacteroidetes Highg

Zwart and coauthors initially described 34 putative clusters of typical fresh

[10�,31,34,51�].a Highest relative abundance (expressed as a percentage of total bacteriab The ACK-M1 cluster is a subgroup of the acI clade [11,35].c The acI clade was found to contribute up to 70% of total bacterial numd The R-BT065 cluster is a subgroup of the ‘Rhodoferax’ sp. BAL47 cluste nk, not known.f The SOL cluster includes the previously described LD2 cluster [11].g Pronounced subcluster-specific differences in ecological adaptations weh The filamentous SOL bacteria contribute disproportionately highly to tot

observed contribution to bacterial biovolume was 45% [31].i Only mixed cultures could be established.

www.sciencedirect.com

BCC have been identified so far. Important factors are

water chemistry [19,20,21�], water temperature [21�],metazooplankton predation [22], protistan predation

[23,24�,25�], phytoplankton composition [13], organic

matter supply [26], intensity of ultraviolet radiation

[27], habitat size [28�] and water retention time

[21�,29�]. Although it is well known that these factors

shape the overall BCC, little is known about those factors

specifically shaping the dynamics of particular popula-

tions of freshwater bacteria. Gray et al. [30] demonstrated

that redox conditions controlled the distribution of Achro-matium spp. in lake sediments. Schauer et al. [31] demon-

strated that mainly water chemistry determined which of

two closely related vicarious groups of SOL bacteria

appeared in particular lakes. Simek et al. [24�] demon-

strated that populations of the highly competitive

R-BT065 bacteria (Betaproteobacteria) were strongly con-

trolled by protistan predation. Wu and Hahn [32]

revealed, for the first time, the recurrent seasonal popula-

tion dynamics of planktonic freshwater bacteria. They

also demonstrated that much of the dynamics of the

investigated Polynucleobacter population could be pre-

dicted from the water temperature. Despite these recent

advances, the prediction of the population dynamics of

free-living bacterial species is currently only possible in a

few exceptional cases.

Cosmopolitan distribution versus localadaptationMany groups of typical freshwater bacteria [11] have a

cosmopolitan distribution [5,11,33,34] (i.e. they appear in

freshwater habitats located all over the world) that

includes habitats located in different climatic zones that

consequently differ in their environmental conditions.

Ecophysiological investigations of closely related Actino-bacteria strains, isolated from tropical, subtropical and

temperate habitats but characterized by identical 16S

city Highest relative abundancea Cultivated strains

<70%c Yes

60% Yes

5% Yes

50% No

11%h Yesi

water bacteria [11], additional clusters were then identified

l cell numbers) reported so far.

bers in high mountain lakes [35].

er [11].

re reported [31].

al bacterial biovolume because of their large cell size. The highest

Current Opinion in Biotechnology 2006, 17:256–261

Page 3: The microbial diversity of inland waters

258 Environmental biotechnology

Figure 1

Undersampling of saline inland waters in cultivation-independent

investigations. Only cultivation-independent investigations, which

described the microbial diversity through the analysis of sequences of

cloned ribosomal genes, were considered; investigations using other

methods (e.g. denaturing gradient gel electrophoresis) or focusing on

selected bacterial groups were not considered for this figure. There have

been no investigations of oligosaline and polysaline stagnant inland

waters. Note that the presented plot reflects only a very small part of the

ecological diversity of inland waters. Eusaline inland waters have

equivalent salinities to those found in marine systems. In the case of

some published investigations, pH or salinity values were not reported

and therefore had to be estimated for the purpose of this schematic

figure.

rRNA genes, revealed a temperature adaptation to local

conditions [34]. Members of this cosmopolitan group

were therefore not generally adapted to a wide range

of thermal conditions, but demonstrated a specific adap-

tation to local climatic conditions.

Ecological plasticity of groups versusecological diversity within groupsHigh ecological plasticity was observed for several groups

of typical freshwater bacteria [11,20,21�,33,35]. For

instance, Polynucleobacter bacteria have been detected

in acidic, neutral and alkaline habitats located in different

climatic zones [33], and ACK-M1 bacteria have been

detected in all freshwater habitats investigated for them

so far [20,21�] (Wu et al., personal communication). These

observations lead to the question of whether all members

of such groups have a uniform ecology. Jaspers and Over-

mann [36�] demonstrated that sympatric Brevundimonasalba strains that did not differ in 16S rRNA genes prob-

ably occupy separate trophic niches, so these strains

probably do not have uniform ecological adaptations.

Observed differences in the predation sensitivity of clo-

sely related bacteria [37], as well as within-group differ-

ences in the salinity adaptation of GKS98 bacteria (Wu

et al., personal communication), also indicate that the

observed ecological plasticity of at least some groups of

typical freshwater bacteria is attributed to ecological

diversity within these groups.

The cultivation of freshwater bacteriaNew cultivation strategies [38–41] resulted in the isola-

tion and cultivation of a growing number of typical fresh-

water bacteria. Most of these methods utilized media

mimicking the low substrate concentrations typically

found in inland waters [39,41,42�,43]; it was, however,

also demonstrated that an important part of the freshwater

bacterioplankton could be acclimatized to substrate-rich

media [33,38]. Acclimatization has allowed cultivation on

standard agar plates, enabling a more convenient and less

laborious maintenance of cultivated strains.

Strains with interesting traits have been found among the

strains isolated from freshwater. For instance, aerobic

anoxygenic phototrophic Alphaproteobacteria character-

ized by an unusual metabolism [42�] and ultramicrobac-

terial Actinobacteria characterized by very small cell sizes

[38] could be cultivated. Furthermore, an entire Polynu-cleobacter population, comprising almost 60% of total

bacterioplankton in a humic pond, was successfully cul-

tivated: that is, each ribosomal genotype detected using

cultivation-independent methods could be cultured using

the acclimatization method [44].

Saline inland watersDespite saline lakes constituting 45% of the total water

volume of inland waters, the diversity of their microbial

inhabitants has received little attention [45–47], whereas

Current Opinion in Biotechnology 2006, 17:256–261

the microbial diversity of dynamic saline systems such as

estuaries (e.g. [8,43,48,49]) and man-made solar saltern

(e.g. [50]) has been studied more intensively (Figure 1).

The currently available data indicate, however, that bac-

terial communities of freshwater and saline lakes show

little taxonomical overlap [45,47] (Wu et al., personal

communication), that is, typical freshwater bacteria are

absent, or almost absent, from saline inland waters.

Future research on microbial diversity ininland watersThere is a great ecological diversity of inland waters.

Even stagnant surface waters (lakes and ponds) alone

represent a large ecological diversity of habitats. In com-

parison with marine habitats, stagnant inland waters vary

much more in their water chemistry, hydrological char-

acteristics, productivity and influences from the surround-

ing terrestrial habitats. The number of investigations to

study the microbial diversity of inland waters is far too

low, relative to the large number of different types of

www.sciencedirect.com

Page 4: The microbial diversity of inland waters

Microbial diversity of inland waters Hahn 259

inland waters, to even provide an overview of the micro-

bial diversity in these habitats (Figure 1). Therefore, it

has to be assumed that many microbial inhabitants of

inland waters are so far undiscovered. Because most

investigations focused on the diversity of planktonic

bacteria, knowledge on the diversity of Archaea, sedi-

ment-dwelling bacteria, biofilm-forming microorganisms,

and those eukaryotic microorganisms that cannot be

studied using morphological approaches is scarcer than

for the planktonic bacteria. Even for planktonic bacteria,

however, one has to assume that the relatively small

number of investigations mainly resulted in the discovery

of those bacterial groups characterized by broad ecologi-

cal plasticities. More investigations covering a broader

range of habitats will result in the discovery of more

specialized groups of bacteria that only occur in limited

ranges of habitat types or only appear during temporarily

limited situations. Recent investigations demonstrated

that increased sampling efforts resulted in the discovery

of bacterial groups and genotypes previously not found in

freshwater habitats [10�,51�].

In contrast to surface freshwater habitats, the microbial

diversity in groundwater has received little attention (e.g.

[52�]). Currently, it is not known whether the microbial

communities inhabiting surface and subsurface inland

waters show a significant compositional overlap. The lack

of knowledge of groundwater habitats is in contrast to the

importance of groundwater in drinking-water production.

ConclusionsOur knowledge of the microbial diversity in inland waters

and especially in freshwater habitats has changed funda-

mentally over the past ten years. It was demonstrated that

freshwater and saline inland waters are each populated by

indigenous bacterial communities that almost completely

lack overlap and do not have a significant compositional

overlap with communities of terrestrial and marine habi-

tats. Major bacterial players in freshwater were identified,

their ecological plasticity characterized, and some repre-

sentatives have even been brought into culture. Almost

nothing is known, however, about the ecological function

of these important groups of freshwater bacteria. Despite

the availability of a growing number of cultures, only a

handful of freshwater isolates have been considered for

genome sequencing projects, and only a single strain out

of the groups of typical freshwater bacteria is currently

being subjected to genome sequencing. The lack of

genomic insight into the metabolic capacities of abundant

freshwater bacteria is one of the reasons for the very

limited functional insight into bacterial communities of

freshwater habitats.

The current knowledge of the diversity and function of

microorganisms in freshwater habitats is insufficient for

the sustainable management of freshwater resources. In

particular, the diversity of non-bacterial microorganisms

www.sciencedirect.com

and the diversity–function relationship of bacterial com-

munities have to be addressed by future investigations.

References and recommended readingPapers of particular interest, published within the annual period ofreview, have been highlighted as:

� of special interest

�� of outstanding interest

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21.�

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24.�

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28.�

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29.�

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38. Hahn MW, Lunsdorf H, Wu QL, Schauer M, Hofle MG, Boenigk J,Stadler P: Isolation of novel ultramicrobacteria classified asActinobacteria from five freshwater habitats in Europe andAsia. Appl Environ Microbiol 2003, 69:1442-1451.

39. Bruns A, Nubel U, Cypionka H, Overmann J: Effect of signalcompounds and incubation conditions on the culturabilityof freshwater bacterioplankton. Appl Environ Microbiol 2003,69:1980-1989.

40. Crosbie ND, Pockl M, Weisse T: Dispersal and phylogeneticdiversity of non-marine picocyanobacteria, inferred from16S rRNA gene and cpcBA - intergenic spacer sequenceanalyses. Appl Environ Microbiol 2003, 69:5716-5721.

41. Page KA, Connon SA, Giovannoni SJ: Representative freshwaterbacterioplankton isolated from Crater Lake Oregon.Appl Environ Microbiol 2004, 70:6542-6550.

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Gich F, Schubert K, Bruns A, Hoffelner H, Overmann J:Specific detection, isolation, and characterization of selected,previously uncultured members of the freshwaterbacterioplankton community. Appl Environ Microbiol 2005,71:5908-5919.

The authors presented the first pure culture isolate affiliated with theactinobacterial acI clade. The environmentally important ACK-M1 cluster[11] is a subgroup of the acI clade.

43. Selje N, Brinkhoff T, Simon M: Detection of abundant bacteriain the Weser estuary by culture-dependent and cultureindependent approaches. Aquat Microb Ecol 2005,39:17-34.

44. Hahn MW, Pockl M, Wu QL: Low intraspecific diversity in aPolynucleobacter subcluster population numericallydominating bacterioplankton of a freshwater pond.Appl Environ Microbiol 2005, 71:4539-4547.

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Microbial diversity of inland waters Hahn 261

45. Humayoun SB, Bano N, Hollibaugh JT: Depth distribution ofmicrobial diversity in Mono Lake, a meromictic soda lake inCalifornia. Appl Environ Microbiol 2003, 69:1030-1042.

46. Demergasso C, Casamayor EO, Chong G, Galleguillos P,Escudero L, Pedros-Alio C: Distribution of prokaryotic geneticdiversity in athalassohaline lakes of the Atacama Desert,Northern Chile. FEMS Microbiol Ecol 2004, 48:57-69.

47. Donachie SP, Hou S, Lee K-S, Riley CW, Pikina A, Belisle C,Kempe S, Gregory TS, Bossuyt A, Boerema J et al.: The HawaiianArchipelago: A microbial diversity hotspot. Microb Ecol 2004,48:509-520.

48. Crump BC, Hopkinson CS, Sogin ML, Hobbie JE: Microbialbiogeography along an estuarine salinity gradient: combinedinfluences of bacterial growth and residence time. Appl EnvironMicrobiol 2004, 70:1494-1505.

49. Kirchman DL, Dittel AI, Malmstrom RR, Cottrell MT:Biogeography of major bacterial groups in the DelawareEstuary. Limnol Oceanogr 2005, 50:1697-1706.

50. Casamayor EO, Massana R, Benlloch S, Øvreas L, Diez B,Goddard V, Gasol JM, Joint I, Rodriguez-Valera F,

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Pedros-Alio C: Changes in archaeal, bacterial andeukaryal assemblages along a salinity gradient bycomparison of genetic fingerprinting methods in amulti-pond solar saltern. Environ Microbiol 2002,4:338-348.

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Crump BC, Hobbie JE: Synchrony and seasonality inbacterioplankton communities of two temperate rivers.Limnol Oceanogr 2005, 50:1718-1729.

This paper demonstrated the highly synchronous seasonal developmentof bacterial communities in two nonintersecting rivers located in the samearea. This observation indicates strong external control of the bacterialcommunity composition in these running waters.

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Miyoshi T, Iwatsuki T, Naganuma T: Phylogeneticcharacterization of 16S rRNA gene clones fromdeep-groundwater microorganisms that pass through0-2-micrometer-pore-size filters. Appl Environ Microbiol2005, 71:1084-1088.

This paper represents one of a few studies that investigated the generalbacterial diversity in groundwater (most other studies focused on thediversity of selected bacterial groups). Only a small overlap between thegroundwater community and surface freshwater communities wasobserved.

Current Opinion in Biotechnology 2006, 17:256–261