encyclopedia of inland waters || archaea

PROTISTS, BACTERIA AND FUNGI: PLANKTONICAND ATTACHED

Contents

Archaea

Bacteria, Attached to Surfaces

Bacteria, Bacterioplankton

Bacteria, Distribution and Community Structure

Chemosynthesis

Cyanobacteria

Fungi

Microbial Food Webs

Protists

Sulfur Bacteria

Viruses

ArchaeaE O Casamayor, Department of Continental Ecology, Centre d’Estudis Avancats de Blanes-CSIC, Blanes, SpainC M Borrego, Institut d’Ecologia Aquatica, Universitat de Girona, Girona, Spain

ã 2009 Elsevier Inc. All rights reserved.

Introduction: Archaea the Unseen ThirdDomain of Life

Archaea are a relatively newly identified group ofprokaryotic microorganisms that constitute the thirdphylogenetic domain of life together with the morewell-known Bacteria and Eukarya. Only a few yearsago, archaea were thought to be mostly restricted toextreme and anoxic environments but it has recentlybeen established that archaeal biodiversity, abun-dance, and metabolic capabilities are substantiallylarger than the previously assumed. Thus, in a veryshort time two major changes in our perception ofprokaryotic world have occurred. What was the basisfor such marked changes now widely accepted? Whatmakes archaea one of the most exciting current topicsin microbial aquatic research?First, over 30 years ago, Carl Woese and colleagues

started the revolution by analyzing phylogeneticmolecular markers (ribosomal RNA) instead of howorganisms look or act. The comparison of 16S rRNAgene sequences showed that a group of prokaryoteshad genetic differences as high as those observedbetween prokaryotes and eukaryotes. These resultsencouraged more detailed studies, including genomesequencing, leading to the conclusion that life is splitin three big Domains instead of the previously recog-nized two of prokaryotes and eukaryotes.A second contributor to the revolution in under-

standing was the recognition that laboratory cultures

strongly biased views of the archaeal potentials. Thephenotypic range of cultivated archaea indicated thatthese microorganisms were restricted to habitats withextreme values of temperature, pH, salinity, or anaero-bic environments for methanogens. Thus, their meta-bolic diversity and ecological distribution seemed tobe more limited than those of other prokaryotes.After considerable recent effort, a couple of new spe-cies of aerobic nonextremophilic archaea have beencultured in the laboratory, enabling detailed study oftheir metabolism and opening a race to bring intoculture some of the most enigmatic microbes in fresh-water environments.

Finally, widespread use of environmental ribo-somal RNA sequencing has unveiled that unseenarchaea were present in freshwater ecosystems andthat the vast majority of them (excluding methano-gens) were unrelated, or at best distantly related,to counterparts known from culture collections.Therefore, the known metabolic capabilities of theDomain Archaea have increased significantly. Unfor-tunately, the ecological significance, biochemistry,physiology, and impact on freshwater biogeochemicalcycles of archaea still remain largely unknown.

To understand the ecology of archaea, a combina-tion of new cultivation strategies, high-resolutionmolecular technologies, more detailed geochemicalanalytical techniques, traditionalmicrobiologicalmeth-ods, and bioinformatics analyses on genomic data willbe required.As soon as someof theseorganismsbecome

167

168 Protists, Bacteria and Fungi: Planktonic and Attached _ Archaea

cultivated and their metabolic and genetic potentialsare studied in detail, a wide range of new physiologicaland ecological phenotypes will be discovered. In themeantime, scientists are profiting from new moleculargenome-based technologies and from some special fea-tures of archaea, e.g., the specific archaeal membranelipids that have ether-linkages instead of ester-linkagestypical of bacteria and eukaryotes. Some of these lipidscan be used as biomarkers to trace the occurrence ofdifferent archaeal communities in ancient sedimentsor as paleotemperature proxies, useful to extrapolatingwater temperatures and climatic transitions. Altogether,the study of archaea is certainly a timely and excitingtopic with strong evolutionary, ecological, and bio-geochemical implications.

Archaeal Habitats in Inland Waters

The Domain Archaea comprises four main groups(Kingdoms): Crenarchaeota and Euryarchaeota arethe two main Kingdoms; Korarchaeota (detectedonly by 16S ribosomal gene sequences obtained froma variety of marine and terrestrial hydrothermal envir-onments, such as the hot spring Obsidian Pool inYellowstone National Park) and Nanoarchaeota(represented by a nanosized hyperthermophilic sym-biont originally found in a submarine hot vent as wellas in the Obsidian Pool) are less widespread anddiverse.Cultivated species of crenarchaeota have thermo-

acidophilic phenotypes and, in theory, occur in pecu-liar hot freshwater environments with an active sulfurcycle such as sulfureta and thermal springs. Unculti-vated mesophilic crenarchaeota are in turn abundantin other natural environments and evidence exists thatthe largest proportion and greatest diversity of thisgroup is present, surprisingly, in cold environments.In contrast, euryarchaeota consists of cultured

organisms that are more diverse in their physiology,metabolic capabilities, and habitat occurrence. Thisgroup includes well-known obligate anaerobic andwidespread methanogens, the extreme halophiles fromsalt lakes, the hyperthermophiles, and the thermoaci-dophiles (i.e., the Thermoplasmata group lacking cellwalls from hot springs and sulfuretic fields). Again,widespread noncultured mesophilic and cold-adaptedphylotypes have been described for euryarchaeota indifferent freshwater ecosystems (Table 1).

Springs

Freshwater aerobic archaea have been traditionallyassociated with freshwaters influenced by hydro-thermal activity (hot-water vents and fumaroles).

Geothermally heated water percolates through volca-nic material, which strongly influences the chemicalcomposition. The emerging water is often enriched inreduced molecules such as sulfide, methane, and H2,which yield energy for archaeal chemolithotrophicactivity. These high-temperature ecosystems are inter-esting but unusual freshwater habitats. However,they may be useful model systems for understandinglife under extreme environments on earth as well inrelation to astrobiological studies. In addition, thermo-philic archaea (both euryarchaeota and crenarchaeota)and bacteria (e.g.,Thermus aquaticus) inhabiting thesesystems with optimum temperatures around 85 �C, arenatural sources of biotechnological products, e.g.,DNA polymerases.

Recently, sulfidic streamlets from emerging coldwater (around 10 �C) in a nongeothermal environ-ment have been reported to support the growth of aunique microbial community. A string-of-pearls-like,macroscopically visible structure, mainly composedof a nonmethanogenic euryarchaeota, occurs inthese streamlets and is viable at temperatures rangingfrom –2 to 20 �C in close association with a sulfide-oxidizing bacteria. In this case, close links betweenarchaea and the sulfur cycle arise in meso- to psy-chrophilic environments that compliment the betterknown associations of thermal environments.

Salt Lakes

Salt lakes, another extreme environment, are sig-nificant components of global inland waters. Saltlakes are complex and heterogeneous with distinctvariation of salinity, alkalinity, and other physical/chemical as well as biological properties. Athalasso-haline lakes are inland saline lakes with ionic propor-tions different from those lakes with salt compositionsimilar to seawater. The conventional salinity value of3 g l�1 is taken as the dividing line between fresh andsaline waters. The range of salinity encountered ininland waters can reach up to 350 g l�1 and evenbeyond in certain lakes. The diversity of aquatichaline environments is enormous around the world,but the prokaryotes thriving in inland saline lakes arepoorly known.

Considerable differences are apparent in the struc-ture of archaeal communities along salinity gradients.At the lower end of the range (�50–70 g l�1), bacteriaare the predominant components of the prokaryoticplankton, and mesohaline uncultured euryarchaeotadistantly related to haloarchaea are found. Thisgroup is widespread in mesohaline freshwater envir-onments surveyed so far but no representatives areavailable in culture to allow ecophysiological studies.At the highly saline end (>200 g l�1) the microbial

Table 1 Distribution of main groups of archaea in inland water ecosystems

Environment Archaeal group Comments

Lakes Nonthermophilic Crenarchaeota (uncultured) Distribution throughout the whole water column

Biogeochemical role unknown

Euryarchaeota (uncultured, nonmethanogens) Distributed mainly in oxic and suboxic zones of the watercolumn

Biogeochemical role unknown

Methanogens Anoxic hypolimnia and sediments

MethanogenesisANME (uncultured anaerobic methane

oxidizers)

Mainly in sediments but also in plankton

Occurring either as syntrophic consortia with sulphate-

reducing bacteria or as archaeal aggregatesRivers Eury- and Crenarchaeota Most clones relate to soil archaea

Estuaries Eury- and Crenarchaeota Highly diverse communities due to inputs from different

sources (e.g. rivers, coastal waters, marshes, soil).

Marshes Methanogens Mainly associated to rizosphere. Most clones related to soilarchaeaNonthermophilic Crenarchaeota

Sediments Methanogens Highly diverse environments with different physicochemistry

and nutrient loads

ANMENonthermophilic Crenarchaeota High archaeal abundance and richness

Sulfureta and hot

springs

Thermophilic chemolithotrophic

Eury- and Crenarchaeota

Main source for Crenarchaeota cultured strains

Extreme thermophiles and acidophilesImportant players in the sulphur cycle

Salt and Soda

Lakes, SolarSalterns

Halophilic and extreme Halophilic

Euryarchaeota

Microbial communities dominated by archaeal

representatives at the highest salinities.

Important sources for novel genera and species of extreme

haloarchaea

Acid Mine Drainage Acidophilic chemolithotrophic Eury-(mainlyThermoplasmata) and Crenarchaeota

Extreme acidophiles

Important players in biogeochemical cycling of sulphur and

sulphide metals

Symbionts Methanogens Anaerobic freshwater protozoa (methanogens)Crenarchaeota Freshwater sponges?

ANME: Anaerobic methane oxidizers.

Protists, Bacteria and Fungi: Planktonic and Attached _ Archaea 169

community is dominated by extremely halophilicarchaeal cells of square-shaped morphology thataccount for up to 75% of total prokaryotes beyond350 g l�1. These calcium and magnesium chloridesaturated brines are one of the most extreme habitatsin the world, but cell concentrations at the highersalinities are towards the high end of the rangefound in any natural planktonic system, reaching upto 108 haloarchaeal cells ml�1 in some cases. Highcell densities produce a visible pink-red color, due totheir carotenoid pigments. In these environments,haloarchaea are very abundant but grow at very lowspecific growth rates, similar to a laboratory culturein stationary phase.Haloarchaea are well known from a wide range

of available pure cultures. They use two photosyn-thetic pigments to successfully develop in haline envir-onments: bacteriorhodopsin (a light-driven protonpump that captures light energy and uses it to moveprotons across the membrane out of the cell creating a

proton gradient that generates chemical energy) andhalorhodopsin (which uses light energy to pump chlo-ride through the membranes to maintain osmoticpressure). In addition, haloarchaea contain high con-centration of salts internally and exhibit a variety ofmolecular characteristics, including proteins thatresist the denaturing effects of salts, and DNA repairsystems that minimize the deleterious effects of desic-cation and intense solar radiation. Crenarchaeotalack most of this special enzymatic equipment andare not present in hypersaline environments.

Rivers and Estuaries

Rivers and estuaries transport materials and energyfrom both terrestrial and aquatic sources to themarine environment. Activity and diversity of micro-bial communities change strongly along this transit,especially in the mixing zone where fresh and salinewaters meet. Rivers are characterized by spatial


heterogeneity and variability imposed by differencesin water flow and geomorphology. Accordingly, thestructure of microbial communities greatly differsamong the different river zones and it is also stronglyinfluenced by water velocity. Although there is awealth of information on the structure of microbialcommunities in rivers, studies focusing on archaealoccurrence, diversity, and abundance are scarce.However, the small number of studies do provide a

Table 2 Overall diversity and distribution of archaeal communities

Site Maincharacteristics

Archaeal diversitya

Columbia (USA) Temperate river Marine and freshwater

It drains into aestuary

Euryarchaeota in the es

Sinnamary (French

Guiana)

Tropical river Euryarchaeota (Methan

Thermoplasmatales)Interrupted by adam (Petit Saut)

Duoro (Portugal) Temperate river Archaeal community do

nonthermophilic Cren

cluster)

Study carried out in

estuarysediments

Rio Tinto (Spain) Acidic (pH 2.2),

high metalcontent

Euryarchaeota (Thermo

Ferroplasma)

Aquifer (Idaho,

USA)

Oxic, basalt aquifer Euryarchaeotal clones

methanogens and ext

Crenarchaeota closerclones

Mackenzie

(Canada)

Arctic river (mean

temperature

3 �C), particle-rich waters

Mainly Euryarchaeota (

uncultured)

Marine Group I.1a Cren

Yangtze River

estuarine regionof East China Sea

(China)

Temperate estuary Sequences related to m

of both uncultured EuCrenarchaeota (autot

oxidizer Nitrosopumilu

Planktonic

samplesanalyzed

aPhylogenetic identity of the main clones of 16S rRNA genes recovered.

Sources

1. Crump BC and Baross JA (2000) Archaeaplankton in the Columbia River, its

31: 231–239.

2. Dumestre JF, Casamayor EO, Massana R, and Pedros-Alio C (2002) Chang

the water eutrophication of Petit Saut dam reservoir (French Guiana). Aquat

3. Abreu C, Jurgens G, De Marco P, Saano A, and Bordalo AA (2001) Crenar

Applied Microbiology 90: 713–718.

4. Gonzalez-Toril E, Llobet-Brossa E, Casamayor EO, Amann R, and Amils R (2

Applied and Environmental Microbiology 69: 4853–4865.

5. O’Connell SP, Lehman RM, Snoeyenbos-West O, Winston VD, Cummings

Crenarchaeota in an oxic basalt aquifer. FEMS Microbiology Ecology 44: 16

6. Galand PE, Lovejoy C, and Vincent WE (2006) Remarkably diverse and con

Ocean. Aquatic Microbial Ecology 44: 115–126.

7. Zeng Y, Li H, and Jiao N (2007) Phylogenetic diversity of planktonic archaea in t

valuable comparison between the riverine commu-nities and the associated estuarine/coastal waters(Table 2).

Benthic (sediments and biofilms) microbial riverinecommunities are complex and active, althougharchaea usually represent a minor fraction of theprokaryotic assemblages. However, archaeal phylo-types’ richness is usually high, mainly in the particle-attached fraction, supporting the idea that rivers act

studied in different lotic habitats

Observations Year Source

Crenarchaeota Mainly associated with

particulate matter(‘particle-attached

archaea’)

2000 1

tuary

ogens and Detected in all sampling

river stationsdownstream the dam

2001 2

minated by

archaeota (marine

Most of the sequences

were obtained from

surface sedimentlayers

2001 3

plasma and Extreme

chemolithotrophicacidophilic archaea

2003 4

related to

remophiles.

to freshwater

First report on Archaea

inhabiting oxic

temperategroundwater

2003 5

methanogens and High diversity

compared to other

rivers

2006 6

archaeota Clones related to

archaea from soil and

sediments

Possible allochthonousorigin

arine clones

ryarchaeota androphic ammonia-

s maritimus).

Remarkable spatial

differences in archaealcomposition

2007 7

Low abundance but

high diverse archaealcommunities

estuary and the adjacent coastal ocean, USA. FEMS Microbiology Ecology

es in bacterial and archaeal assemblages in an equatorial river induced by

ic Microbial Ecology 26: 209–221.

chaeota and Euryarchaeota in temperate estuarine sediments. Journal of

003) Microbial ecology of an extreme acidic environment, the Tinto River.

DE, Watwood ME, and Colwell FS (2003) Detection of Euryarchaeota and

5–173.

trasting archaeal communities in a large arctic river and the coastal Arctic

he estuarine region of East China Sea.Microbiological Research 162: 26–36.


as collectors of allochthonous archaea from catch-ments and neighboring ecosystems. Studies onarchaeal diversity in rivers from diverse geographiclocations with very different physichochemical con-ditions have revealed both euryarchaeota and cre-narchaeota that are highly similar in their 16SrRNA gene sequence with uncultured archaea fromsoils, rice fields, marshes, and anoxic sedimentsfrom lakes (Table 2). These comparisons suggest anallochthonous origin for riverine archaea. Methano-microbiales and uncultured methanogens from soilsand anoxic sediments are predominant euryarchaeo-tal components among the archaea, and high nutrientloading combined with hypoxic conditions in riversediments may favor their growth and activity. Inturn, most of the crenarchaeotal sequences obtainedfrom rivers affiliate with either marine planktonic orsoil crenarchaeota. Therefore, riverine archaea seemsto be more related to both sediment decompositionand passive transport. Exceptions arise in rivers withextreme conditions, such as the Rio Tinto (Spain), anacid river (pH 2.2 along nearly 100 km) where thecombination of an active sulfur–iron cycle withhigh amounts of dissolved metals (Fe, Cu, Zn) favorthe presence of the iron oxidizing chemolithoauto-troph Ferroplasma (Thermoplasmata). Again in thisexample as for the sulfidic streamlets discussedabove, a linkage between archaea and the sulfur–ironmetabolism arise in a mesophilic environment.The structure and dynamics of the microbial com-

munities thriving in estuarine waters are more com-plex than in rivers due, in part, to themixing regime ofthese environments. Estuaries have strong spatial andtemporal gradients imposed by the contact betweenfreshwater and marine waters, the geomorphology ofthe area, the influence zone of the freshwater input,wind mixing, and tidal action. Moreover, the estuaryusually receives high inputs of organic matter fromthe river and from the coastal marine environment.As a consequence, estuarine microorganisms are amixture of riverine andmarine components. Althougharchaeal phylotypes from plankton and sedimentsbelong mostly to the nonthermophilic marine cre-narchaeota, methanogens have also been detected inthe sediment (Table 2). These results point to a maininfluence of marine waters on estuarine archaeaalthough remarkable spatial differences are observedamong and within systems.

Lakes

Stratified lakes Stratified lakes with seasonal or per-manent oxic–anoxic interfaces have been subject ofintense research by microbial ecologists because ofthe environmental conditions imposed by the vertical

physichochemical gradients and pronounced changesin oxygen concentration. Stratification results in well-defined water compartments with different condi-tions suitable for growth of distinct and highly diversemicrobial assemblages that play different roles in bio-geochemical cycles. Archaea have been found tochange along the vertical profile: archaeal richness,identity, and abundance change between oxic,oxic–anoxic, and anoxic zones for most studiedlakes. This is a first indication that uncultured phylo-types are autochthonous and metabolically activein situ. Another indication can be found in humicstratified boreal lakes. Humic lakes receive largeinputs of allochthonous (terrestrially derived) organicmaterial, and consequently foreign archaeal popula-tions are entering in the lake. However, unculturedplanktonic phylotypes are distantly related to theircounterparts from boreal forest soils suggesting thesepopulations are lacustrine.

In the upper and well-oxygenated water layers, non-thermophilic freshwater crenarchaeota and severalphylotypes of the uncultured euryarchaeota (mainlyrelated to uncultured freshwater and marine clonesand also distantly related to the Thermoplasmata andrelative groups) have been frequently detected (Table 3),although they usually constitute a minor fraction ofthe picoplankton. At the oxic–anoxic interface, com-plex microhabitats with sharp gradients that favorthe activity of different microbial populations exist.Anoxic layers in the water column as well as anoxicsediments have a combination of anaerobiosis, lowredox potentials, and an accumulation of dissolvedsulfur- and nitrogen-reduced compounds, as well asmethane. Different studies carried out in stratifiedlakes have shown that archaeal abundance increasewith depth. Uncultured euryarchaeota are frequentlyfound at the oxic/anoxic interfaces whereas methano-gens and non-thermophilic crenarchaeota are foundin the anoxic waters and sediments (Table 3).

Cultivation has remained elusive for these newarchaeal groups and there is very little understandingof their metabolism and roles within the ecosystem.Concerning nonthermophilic freshwater crenarch-aeota, recent findings indicate that although theyhave been generally found in plankton and sedimentsfrom very different lakes, they may be less abundantthan their marine and soil counterparts. Also, therichness of nonthermophilic crenarchaeota in suboxicand anoxic water layers is low, yielding very fewphylotypes distantly related to the ubiquitous cre-narchaeota from marine water and sediments orsoils. Phylotypes detected at and below the oxyclineaffiliate with marine benthic groups. This latter clus-ter has been properly named as Miscellaneous Cre-narchaeota Group (MCG) since it includes a large

Table 3 Overall diversity and distribution of archaeal communities studied in different lakes

Site Main characteristics Archaeal diversity Observations Year Source

Alpine and polar lakes

Gossenkollesee (Austria); Crater Lake(Oregon, USA); Pyrenean lakes (Spain)

High-altitude,ultraoligotrophic

lakes

High archaeal richness among lakes Archaeal abundance among lakesfrom 1% to 37% of total prokaryotic

counts

1998, 2001,2007

1, 3, 4, 5

Completelyoxygenated

Spatial segregation between crena- andeuryarchaeota

Higher abundance of Archaea inautumn and after ice-cover

formation (early winter) in alpine

lakes

High UV-radiation The most abundant Crenarchaeota are closelyrelated to nonthermophilic marine planktonic

groups

Crenarchaeota more abundant eitherat the air–water interface and in

deep waters (300–500m depth)

Fryxell (Antarctica) Permanently frozen Mainly Euryarchaeota (methanogens and

uncultured)

Coexistence of cold-adapted

methanogenic and methanotrophicarchaea in the anoxic bottom waters

2006 2

Active

methanogenesisand sulfate

reduction in the

sediment

Crenarchaeota related to uncultured marine

benthic group

Great and large lakesMichigan, Lawrence (WI, USA) Oligo- to

mesotrophic lakes

Euryarchaeota (methanogens) Crenarchaeotal 16S rRNA up to 10%

of total environmental RNA

extracted

1997 6, 7

Sediment samplesanalyzed

Crenarchaeota related to the marine group

Laurentian Great Lakes (USA): Erie,

Huron, Michigan, Ontario and SuperiorOnega; Ladoga (Russia); Victoria

(Africa)

Temperate to cold

waters

All sequences clustered with marine

nonthermophilic planktonic Crenarchaeota

Archaeal rRNA accounted for 1 to

10% of total planktonic rRNA

2003 8

Oligo- to

mesotrophic lakes

Different climatic and

geographicconditions covered

Presence of cosmopolitan

crenarchaeotal phylotypes

Planktonic samples

analyzed

172

Pro

tists,Bacteria

andFungi:Planktonic

andAtta

ched_A

rchaea

Stratified lakes

Sælenvannet (Norway); Vilar (Spain);

Pavin (France)

Meromictic sulfide-

rich lakes

Euryarchaeota (methanogens, methanogens

endosymbionts of anaerobic ciliates, andpopulations distantly related to

Thermoplasmata)

Archaeal abundance increase with

depth and maximal abundancebelow the chemocline

1997 9, 13, 16

2001

Moderate to coldtemperatures

Crenarchaeota (nonthermophilic related to themarine and freshwater groups)

Seasonal dynamics, with higherrelative abundance of

Crenarchaeota in autumn and winter

2007

Charca Verde (France) Freshwater pond Methanogens, populations distantly relatedto Thermoplasmata and anaerobic

methane-oxidizing archaea

Possible cooccurrence ofmethanogenic and methanotrophic

(ANME-related) archaea in the

anoxic water column

2007 18

Sulfide-rich waters No Crenarchaeota detectedValkea Kotinen (Finland) Boreal forest lake Methanogens and uncultured euryarchaeota

distantly related to Thermoplasmata

Archaea up to 7% of total

microscopic counts

2000 11

Anoxic hypolimnion

with methane

Crenarchaeota of the nonthermophilic

freshwater group

No significant changes in abundance

along seasonFreshwater crenarchaeota not related

to soil crenarchaeota

Stratified lakes

Solar Lake (Sinai, Egypt) Hypersaline lake Methanogens and uncultured populationsdistantly related to Thermoplasmata

Archaeal community dominated byhaloarchaea (salinities >10%)

2000 12

Sulfide-rich

hypolimnion

No Crenarchaeota detected Halophilic methanogens present

Active

methanogenesis at

the bottom

Rotsee (Switzerland); Dagow (Germany);Biwa (Japan); Kinneret (Israel)

Samples from anoxicsediments

Methanogens, methanogenic endosymbiontsof anaerobic ciliates and uncultured

euryarchaeota distantly related to

Thermoplasmata

Archaeal abundance (methanogens)accounted for 1 to 7% of total

prokaryotes

1999; 2004;2007

10, 14,15, 17

Mesoeutrophic lakeswith anoxic

hypolimnion

Crenarchaeota detected only in sulfuroussediments (freshwater nonthermophilic group)

Methanogenic endosymbiontsup to 1%

Sources

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Environmental Microbiology 63: 4299–4306.

2. Karr EA, Ng JM, Belchik SM, Sattley WM, Madigan MT, and Achenbach LA (2006) Biodiversity of methanogenic and other Archaea in the permanently frozen Lake Fryxell, Antarctica. Applied and Environmental

Microbiology 72: 1663–1666.

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Hydrobiologia 574: 161–177.

5. Auguet JC, and Casamayor EO (2008) A hotspot for cold Crenarchaeota in the neuston of high mountain lakes. Environmental Microbiology 10: in press. DOI: 10.1111/j.1462-2920.2007.01498.x

6. MacGregor BJ, Moser DP, Alm EW, Nealson KH, and Stahl DA (1997) Crenarchaeota in Lake Michigan sediment. Applied and Environmental Microbiology 63: 1178–1181.

7. Schleper C, Holben W, and Klenk HP (1997) Recovery of crenarchaeotal ribosomal DNA sequences from freshwater-lake sediments. Applied and Environmental Microbiology 63: 321–323.

8. Keough BP, Schmidt TM, and Hicks RE (2003) Archaeal nucleic acids in picoplankton from great lakes on three continents. Microbial Ecology 46: 238–248.

9. �vreas L, Forney L, Daae FL, and Torsvik V (1997) Distribution of bacterioplankton in meromictic Lake Sælenvannet, as determined by denaturing gradient gel electrophoresis of PCR-amplified gene fragments

coding for 16S rRNA. Applied and Environmental Microbiology 63: 3367–3373.

10. Falz KZ, Holliger C, Grobkopf R, Liesack W, Nozhevnikova AN, Muller B, Wehrli B, and Hahn D (1999) Vertical distribution of methanogens in the anoxic sediment of Rotsee (Switzerland). Applied and


11. Jurgens G, Glockner F.-O, Amann R, Saano A, Montonen L, Likolammi M, and Munster U (2000) Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent

in situ hybridization. FEMS Microbiology Ecology 34: 45–56.

12. Cytrin E, Minz D, Oremland RS, and Cohen Y (2000) Distribution and diversity of archaea corresponding to the limnological cycle of a hypersaline stratified lake (Solar Lake, Sinai, Egypt). Applied and


13. Casamayor EO, Muyzer G, and Pedros-Alio C (2001) Composition and temporal dynamics of planktonic archaeal assemblages from anaerobic sulfurous environments studied by 16S rDNA denaturing gradient

gel electrophoresis and sequencing. Aquatic Microbial Ecology 25: 237–246.

14. Glissmann K, Chin KJ, Casper P, and Conrad R (2004) Methanogenic pathway and archaeal community structure in the sediment of eutrophic Lake Dagow: effect of temperature.Microbial Ecology 48: 389–399.

15. Koizumi Y, Takii S, and Fukui M (2004) Depth-related changes in archaeal community structure in a freshwater lake sediment as determined by denaturing gradient gel electrophoresis of amplified 16S rRNA

genes and reversely transcribed rRNA fragments. FEMS Microbiology Ecology 48: 285–292.

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diversity of sequences retrieved from different envir-onments such as soils, terrestrial environments, deep-paleosoils and forest lakes.In contrast with the limited understanding of the

MCG group, methanogens are active key playerswithin the carbon cycle in anoxic waters and sediment,and their richness, abundance, and activity in lakes ofdifferent trophic status around the world have beenextensively documented. Further, methanogenic endo-symbionts of anaerobic ciliates have been also observedin oxic–anoxic interfaces and anoxic water zones ofstratified lakes. Interest in methanogens is linked toglobal warming produced by the strong greenhouseeffects of methane gas in the atmosphere. Dependingon the energy and carbon source used to generatemethane, methanogens can be divided in hydro-genotrophic, if they use H2/CO2, and acetoclastic, ifthey use acetate. Interestingly, mixed communities ofacetoclastic methanogens (family Methanosaeteceaeand relatives) and hydrogenotrophic methanogens(families Methanobacteriaceae, Methanospirillaceae,and Methanomicrobiaceae) alternate in dominance ofthe community dependingmainly on temperature (hightemperatures favor hydrogenotrophs) and substrateavailability (i.e., H2, acetate, and simple methylatedcompounds).The unexpected discovery of archaea able to anaero-

bically oxidize methane in deep-sea anoxic sedi-ments is a significant new finding about methanecycling in anoxic environments. The first describedanaerobic methane oxidizers (ANME) were foundto be in close association with sulfate-reducing bac-teria forming a syntrophic consortium whereas thearchaeal partner oxidizes methane and further trans-fers electrons to bacteria, which reduce sulfate tohydrogen sulfide. Anaerobic methane oxidizationalso occurs in freshwater anoxic hypolimnia andsediments with planktonic single cells, short chains,or small aggregates of ANME archaea reaching upto 1% of total prokaryotes at certain depths. Inaddition, a new bacteria/archaea consortium thatoxidizes methane to carbon dioxide coupled to deni-trification has been recently described in a methane-saturated freshwater sediment. Altogether, differentconsortia of ANME appear to be distributed world-wide. To date, however, no pure cultures of metha-notrophic archaea are available.

Great lakes A handful of large lakes have been sur-veyed for archaeal abundance and 16S rRNA genediversity. Quantitative rRNA hybridizations revealedthat the percentage of archaeal nucleic acid wasbetween 0.7% and 10% of the picoplankton col-lected from the epilimnion and hypolimnion of theLaurentian Great Lakes in North America, Africa’s

Lake Victoria, and Lakes Ladoga and Onega in Rus-sia. In addition, analysis of sedimentary archaealrRNA and mostly archaeal membrane lipids (cren-archaeol) from the top surface sediments of severallarge lakes representative of different climatic andphysical scenarios (Lake Superior and Lake Michiganin North America, Lake Malawi in the East Africa,and Lake Issyk Kul in Central Asia) suggest ubiqui-tous and widespread distribution of nonthermophilicplanktonic crenarchaeota in large freshwater bodies.The lipid structure was identical to the marine coun-terparts and would indicate a very close relationshipboth in phylogeny and metabolism for marine andlarge lake archaea. The phylogenetic analysis carriedout with 16S rRNA genes points in the same direc-tion. Altogether, the limited studies in large lakes havebeen sufficient to increase the overall absolute abun-dance of freshwater crenarchaeota several orders ofmagnitude, and subsequently increase their expectedimpact in biogeochemical cycling.

High-altitude and polar lakes 16S rRNA genesurveys have indicated that the largest proportionand greatest diversity of archaea exist in permanentlycold environments, and the study of cold-adaptedarchaea is a growing area of research. Little isknown about these cold-water archaea in freshwatersexcept that they are present in considerable numbersup to 104–105 ml�1 (i.e., 5–30% of total prokaryoticplankton). They are found in the Antarctic, theArctic, and in high mountain lakes but very few dataon abundance, composition, and other attributes areavailable so far. A recent study carried out in Pyre-nean lakes points to the hydrophobic surface filmat the air–water interphase (neuston) as being a pos-sible hotspot for nonthermophilic crenarchaea (seeTable 3). In general, these remote systems are difficultto reach and aquatic biota experience extreme physi-cal conditions such as low temperatures and high UVexposure. In addition, many of these lakes are icecovered most of the year and have extreme oligotro-phic conditions. Pelagic archaeal population dynam-ics are related to the dynamics of the lake. Archaeaseem to be abundant in the plankton only duringautumn thermal mixing and abundances decreasethereafter, as depicted from a detailed monthly study(see Table 3). Again, these results indicate thatarchaea are metabolically active in situ. In fact, recentobservations indicated that archaeal 16S rRNA genesfrom high mountain lakes and perennially cold orpermanently frozen Antartic lakes belong to metha-nogens, uncultured euryarchaea (distantly related toThermoplasmata), and crenarchaeota. There is a con-siderable distance between any ribosomal sequencefor these aquatic forms relative to terrestrial archaea.


These freshwater archaea are likely involved in themajor biogeochemical cycles that occur in these eco-systems. Interestingly, freshwater uncultured plank-tonic crenarchaeota are very abundant at certaindepths in several surveyed high mountain lakes andclosely similar to the marine crenarchaeal group,which is very abundant in the deep ocean. For exam-ple, in Crater Lake (OR, USA), archaea are veryabundant in bottom waters reaching up to 20%of total prokaryotes with a single predominant phy-lotype related to the marine crenarchaeota and incertain Pyrenean lakes (Spain) archaea reached morethan 30% of total microscopic counts. As other casesdiscussed in this article, there is undoubtedly ampleroom for new and exciting discoveries related toarchaea and cold-water habitats in lakes.

Functional Role: the Known and theKnowable

The Known Functional Roles

Much knowledge has been gained on the functionalrole of archaea in situ from the cultured representa-tives of the three traditional groups available in thelaboratory (Table 4 and Table 5). The role that ubi-quitous methanogens carry out in the environment iswell characterized. Formation of methane in the finaldegradation step of organic matter under anaerobicconditions is an exclusive attribute of archaea. Inaddition, methanogens are the only known archaeaable to fix N2. Hyperthermophiles are metabolicallyquite diverse, ranging from chemoorganotrophs tochemolithoautotrophs. They are aerobes, facultativeanaerobes, fermenters, or anaerobes respiring sulfateor nitrate on organic substrates. Several species are atthe base of the food web as primary producers oforganic matter using carbon dioxide as sole carbonsource and obtaining energy by the oxidation of inor-ganic substances like sulfur and hydrogen. Finally,haloarchaea are mostly aerobic chemoorganotrophsalthough the ability to use nitrate as a terminal elec-tron acceptor in energy metabolism has been found inseveral studies.In relation to the nitrogen cycle, some cultured

archaea (both euryarchaeota and crenarchaeota) arecapable of denitrification and nitrogen fixation likebacteria. Unlike bacteria, none of the archaea wereinitally thought to be capable of nitrification. Accord-ing to this view, the role of archaea in the nitrogencycle seemed to be important only at a local scale (i.e.,extremophilic freshwater environments) although acareful evaluation must be done after microbial eco-physiologists have explored the potential capabilitiesof uncultured archaea. In fact, recent data indicate

the potential for nitrification in both uncultured andrecently cultured widespread archaea.

The Knowable Functional Roles

Scientists are just beginning to glimpse the functionaldiversity of noncultured freshwater archaea, althoughcurrent data are still scarce and fragmentary (Table 6).Although we suspect that most of archaeal cells areactive under in situ conditions, no clear data is avail-able on the precise physical, chemical, and biologicalcharacteristics of their niche. This characteriza-tion would be very helpful for developing cultureenrichments and further isolation of new archaealspecies. Obtaining pure laboratory cultures will facil-itate the precise determination of their ecophysio-logical, biochemical, and genetic properties. At themoment, new, culture-independent approaches arestarting to provide a better and more comprehensiveunderstanding of the roles of archaea within the eco-system and habitats. These studies indicate that themajority of freshwater archaea, especially crenarch-aeota, are mesophilic or even psychrophilic in con-trast with early views that archaea were primarilythemophilic and/or halophilic. In fact, recent evidencesuggests that some of the ubiquitous pelagic cren-archaeota play an essential role in biogeochemicalcycling in aquatic ecosystems and may act aschemoautotrophs, oxidizing ammonia to nitrate, andfixing inorganic carbon in the dark. Further, the detec-tion of tetraether membrane lipids of freshwater cren-archaeota in both ancient and recent sedimentsindicates crenarchaeota are potential mediators ofCO2 drawdown from the atmosphere to sediments.

Molecular phylogenetic surveys carried out in nat-ural environments for the last 15 years have provideda better comprehension of archaeal diversity and phy-logeny based on the 16S rRNA gene. At present,scientists have a wide array of powerful techniquesthat will advance future studies. These include(1) metagenomics – the study of large DNA fragmentsobtained directly from the environment and the use ofhigh-throughput DNA sequencing on microbialenrichments and further genome reconstructionusing bioinformatics; (2) comparative genomics –using metagenomes and available genomes in data-bases to both make inferences about ecology, biology,and evolution, and to search for relevant functionalgenes linked to archaeal phylogenetic markers inmetagenomic libraries; (3) functional genes surveys –monitoring both at the DNA level and at themRNA level to demonstrate potential and in situexpression, respectively; and (4) isotopically labeledsubstrate tracking combined with fluorescence in situhybridization (FISH) and microautoradiography for

Table 4 Summary of the basic metabolic capabilities, required growth conditions and occurrence of the main groups of Euryarchaeota in inland waters

Group Metabolic process Energy source Carbonsource

e– donor e– acceptor Conditions Occurrence Culturedrepresentatives

Methanogens Methanogenesis O.M. (acetate,format,

methanol, . . .)

O.M.a O.M. O.M. Extreme anaerobiosis Anoxic waters of stratifiedlakes

Methanococcus,Methanobacterium,

Methanosphaera

Sediments, rice fields

H2 CO2 H2 CO2 Low redox potential Anoxic microhabitats in solarsalterns, soda lakes and salt

marshes

Most methanogens

Sewage digestors

Methanotrophs Anaerobicoxidation of

methane

CH4 O.M. CH4 SO42– Extreme anaerobiosis Anoxic sediments None

Nitrite Low redox potentials

Sulfate-reducingbacteriab

Anoxic conditions

Active sulphur cycleHalophiles Aerobic respiration O.M. (sugars,

aminoacids,

glycerol)

O.M. O.M. O2 Moderate to extreme

salinities (from 7% to

37% NaCl)

Salt lakes Haloarcula, Haloferax,

Halorubrum,

Natrinema

Anaerobicrespiration

O.M. Nitrate,DMSO,

organic

acids

High Ph Soda lakes Halobacterium,Haloarcula, Haloferax

Fermentation Sugars,aminoacids

O.M. O.M. Oxic, anoxic Hypersaline Antarctic lakes Halobacterium

Nonphotosynthetic

photoheterotrophycLight O.M. O.M. – Solar salterns Halobacterium

aOrganic matter.bAnaerobic methane oxidation involves a symbiosis between archaeal cells and sulfate-reducing bacteria forming syntrophic consortia with different structures and cell numbers. Some studies have shown that

methanotrophic archaea can oxidize methane without bacterial consortia.cUnder suboxic or anoxic conditions, light-induced isomerization of retinal in Bacteriorhodopsins causes a translocation of protons across the membrane that is used to generate ATP.

Pro

tists,Bacteria

andFungi:Planktonic

andAtta

ched_A

rchaea

177

Table 5 Summary of the basic metabolic capabilities, required growth conditions, and occurrence of the main groups of Crenarchaeota in inland waters

Group Metabolic process Energy source Carbonsource

e– donor e– acceptor Conditions Occurrence Cultured representatives

Thermophiles Aerobic

chemolithotrophy

S0 CO2 S0 O2 High temp. (40–97 �C); AcidicpH (1–5.5); Oxic to anoxicconditions

Oxic–anoxic

microhabitats inthermal sulphur

springs

Acidianus, Sulfolobus

Aerobic respiration O.M.a(sugars,

peptides,aminoacids,

alcohols)

O.M. O.M. O2 Oxic zones of thermal

sulphur springs

Thermoproteus,

Sulfolobus

Anaerobic

chemolithotrophy

H2 CO2 H2 S0, Nitrate,

Fe3+Suboxic–anoxic zones

in thermal sulphursprings

Acidianus, Pyrodictium

Anaerobic respiration O.M. (sugars,

peptides,

aminoacids,alcohols)

O.M. O.M. S0, Nitrate,

Nitrite

Suboxic–anoxic zones

in thermal sulphur

springs

Pyrococcus,

Thermoproteus.

Thermococcus,Pyrobaculum

Fermentation O.M. (sugars,

peptides,aminoacids,

alcohols)

O.M.b O.M. S0 Anoxic zones in

thermal sulphursprings

Pyrococcus,

Thermococcus

aOrganic matter.bNot completely oxidized to CO2.

178

Pro

tists,Bacteria

andFungi:Planktonic

andAtta

ched_A

rchaea

Table 6 Summary of the putative metabolic capabilities, required growth conditions, and occurrence of the main groups of nonthermophilic Crenarchaeota detected so far in

inland waters

Group Putative metabolicprocess

Energy source Carbonsource

e– donor e– acceptor Conditions Occurrence Culturedrepresentatives

Nonthermophiles Aerobic

chemolithotrophy

NH4+ CO2 NH4

+ O2 O2 and reduced

nitrogencompounds

(NH4+)

Close relatives detected

in great lakes andalpine lakes

Candidatus

Nitrosopumilusmaritimusa

Oligotrophy

Aerobicchemoorganotrophy?;

Mixotrophy?

O.M.b

(aminoacids)O.M. O.M. O2 Oxic

conditionsNone

Oligo- to

mesotrophicAnaerobic

chemolithotrophy?

H2, H2S CO2 H2, H2S S0, Nitrate, Fe3+ Suboxic to anoxic

conditions

Suboxic–anoxic zones in

stratified lakes (meta- and

hypolimnia)

None

Reduced sulphur

compounds

Sediments

Meso- to Eutrophic

Anaerobicchemoorganotrophy?

O.M.(sugars, peptides,

aminoacids,

alcohols)

O.M. O.M. S0, Sulfate,Nitrate, Nitrite

Suboxic toanoxic conditions

Suboxic–anoxic zonesin stratified lakes (meta-

and hipolimnia)

None

Meso- to eutrophic Sediments

aIsolated from marine environment.bOrganic matter.

Pro

tists,Bacteria

andFungi:Planktonic

andAtta

ched_A

rchaea

179


detection of nutrient uptake by specific archaeal cellsin mixed communities.Microbial ecologists have already started to apply

these methodologies on marine and soil unculturedarchaea as well as those from inland waters. New andexciting results are continuously arising. In one exam-ple, the ANME archaea are offering clues for thecomplete understanding of the methane cycle, as indi-cated earlier. In another example, nonthermophiliccrenarchaeota from the ocean and soils have beenrecently proposed to be chemolithoautotrophs, oxi-dizing ammonia using an archaeal ammonia mono-oxygenase (AOA), which is phylogenetically distantlyrelated with the same enzyme present in bacterialnitrifiers (AOB). Pure cultures and complex mixturesin laboratory enrichments of nonthermophilic cren-archaeota are starting to become available for eco-physiological experiments. Field data suggest thatplanktonic communities either contain both autotro-phic and heterotrophic archaealmembers or are largelycomposed of cells with a mixotrophic metabolism.Archaea may also be capable of nitrification based onemerging information. The present knowledge onuncultured archaea will benefit very soon from allthese methodological improvements leading to the elu-cidation of the precise role of these microorganisms inthe biogeochemical cycling of inland waters.

Concluding Remarks

Overall, archaea are a common component of fresh-water plankton and different groups of unculturedarchaea tend to occupy different ecological niches,although the metabolism and physiological rolesremain challenging questions. Our knowledge haslargely increased as the number of studies performedand the diversity of biotopes sampled have increased.In general, archaea seem to be within a range <10%of total prokaryotic plankton and might be playingimportant and previously unrecognized roles ininland water ecosystems. From the few studies avail-able, it can be deduced that archaea show spatial andtemporal differences in abundance, and more detailedspatiotemporal surveys will unveil the conditionsunder which archaea reach higher numbers in fresh-water habitats. Further studies combining ecologyand several of the molecular and genomic tools avail-able, as well as traditional microbiology, are stillneeded to enlarge our view on the ecology of archaeain lakes, rivers, and streams. As soon as some of theseorganisms become cultivated and their metabolic andgenetic potentials are studied in detail, new physio-logical and ecological phenotypes will be discovered.It seems clear that the roles that archaea play in the

ecosystems have been grossly underestimated andthat scientists have begun to realize this fueling therecent burst forward in new knowledge.

Glossary

Acetoclastic – Type of methanogens that producemethane using acetate as energy and carbon source.

Ammonia monooxygenase (AMO) – The key func-tional enzyme responsible for the conversion ofammonia to hydroxylamine (which is further con-verted to nitrite by hydroxylamine oxidoreductase).

ANME – ANME stands for anaerobic methane oxi-dation. A process carried out by methanotrophicarchaea in a sort of syntrophic consortium withsulfate-reducing bacteria. These consortia werefirst described in deep-sea anoxic sediment but re-cent data have demonstrated their presence in an-oxic waters and sediments of some freshwaterhabitats.

Bacteriorhodopsins – Integral membrane proteinscontaining retinal present in many halophilicarchaea. Bacteriorhodopsins use light energy togenerate a transmembrane proton motive force(proton pumps) subsequently converted into ATP.Some halophiles contain halorhodopsins, modifiedbacteriorhodopsins that act as light-driven chlo-ride pumps.

Chemolithoautotroph – An organism that obtainsenergy from reduced inorganic compounds and car-bon from CO2.

Chemoorganoautotroph – An organism that obtainsenergy from organic compounds and carbonfrom CO2.

Chemoorganoheterotroph – An organism that obtainsenergy and carbon from organic compounds.

Crenarchaeol – Glycerol dialkyl glycerol tetraetherthought to be solely produced by ‘cold’ crenarch-aeota (i.e., nonthermophilic). Excellent biomarkerand paleotemperature proxy.

Crenarchaeota – One of the four phyla (kingdoms) ofthe Domain Archaea. Members of this group areeither extremophiles or nonextremophiles inhabit-ing the most diverse environments.

Euryarchaeota – One of the four phyla (kingdoms) ofthe Domain Archaea. Methanogens and halophilesare the most known members of this phylum.

Extremophile – An organism that occupy environ-ments judged by human standards as harsh because


of both physical and chemical extremes. Literally‘extreme-loving.’

Hydrogenotrophic – Type of methanogens that pro-duce methane using H2 and CO2 as energy andcarbon sources, respectively.

Korarchaeota – One of the four phyla (kingdoms) ofthe Domain Archaea. Members of this kingdomhave been identified only by environmental DNAsequences in high-temperature environments.

Methylotrophic – Type of methanogens that producemethane using simple C1 compounds as energy andcarbon source.

Nanoarchaeota – The most recent phylum (kingdom)discoveredwithin theDomain Archaea.Members ofthis phylum are very small in size and they are allsymbionts of hyperthermophilic archaea.

Phylotype – In the context of microbial ecology refersto a uncultured microorganisms only described bytheir ribosomal gene sequence (mainly 16S or 18S)

Picoplankton – The portion of the plankton com-prised between the 2–0.2 mm size range.

Sulfureta – Natural environments usually foundaround active volcanoes very rich in sulfur-reducedcompounds.

Syntrophy – Cooperation of two or more microor-ganisms that combine their metabolic capabilities todegrade a substance not capable of being degradedby either one alone.

Further Reading

Brock TD (1997) Prokaryotic diversity: Archaea. In: Madigan MT,Martinko JM, and Parker J (eds.) Biology of Microorganisms,8th edn, pp. 635–740. Englewood Cliffs, NJ: Prentice Hall.

Cavicchioli R (2006) Cold-adapted archaea. Nature ReviewsMicrobiology 4: 331–343.

Chaban B, Ng SYM, and Jarrell KF (2006) Archaeal habitats—

From the extreme to the ordinary. Canadian Journal of Microbi-ology 52: 73–116.

DeLong EF (1998) Everything in moderation: archaea as ‘nonex-

tremophiles’ Current Opinion in Genetics and Development8: 649–654.

Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, and

Stackebrandt E (eds.) (2006) The Prokaryotes—A Handbookon the Biology of Bacteria, Vol. 3: Archaea, 3rd edn. New York:

Springer-Verlag.Garcia J-L, Patel BKC, and Ollivier B (2000) Taxonomic, phyloge-

netic and ecological diversity of methanogen archaea. Anaerobe6: 205–226.

Hershberger KL, Barns SM, Reysenbach AL, et al. (1996) Widediversity of Crenarchaeota. Nature 384: 420.

Huber R, Huber H, and Stetter KO (2000) Towards the ecology of

hyperthermophiles: Biotopes, new isolation strategies and novelmetabolic properties. FEMSMicrobiology Reviews 24: 615–623.

Nicol GW and Schleper C (2006) Ammonia-oxidizing Crenarch-

aeota: Important players in the nitrogen cycle? Trends in Micro-biology 14: 207–212.

Oren A (1994) The ecology of the extremely halophilic archaea.

FEMS Microbiology Reviews 13: 415–440.Powers LA, Werne JP, Johnson TC, et al. (2004) Crenarchaeotal

membrane lipids in lake sediments: A new paleotemperatureproxy for continental paleoclimate reconstruction? Geology 32:

613–616.

Rudolph C, Wanner G, and Huber R (2001) Natural communitiesof novel archaea and bacteria growing in cold sulfurous springs

with a string-of-pearls-like morphology. Applied and Environ-mental Microbiology 67: 2336–2344.

Schleper C (2005) Genomic studies of uncultivated archaea.NatureReviews Microbiology 3: 479–488.

Woese CR (1987) Bacterial evolution.Microbiological Reviews 51:221–271.

Relevant Websites

http://archaea.ws/index.html – A scholarly journal providing rapid

peer review and publication of articles dealing with any aspect of

research on the archaea.

http://www.archaea.unsw.edu.au – ArchaeaWeb is an informationresource for researchers working with archaea and extremo-

philes.

http://www.ucmp.berkeley.edu/archaea/archaea.html – An intro-

ductory page on the main characteristics of the archaea, main-tained by the University of California at Berkeley.

http://tolweb.org/tree?group¼Archaea&contgroup¼Life_on_Earth –

A page dedicated to the archaea in the Tree of Life web project.

http://archaea.ws/index.html

http://www.archaea.unsw.edu.au

http://www.ucmp.berkeley.edu/archaea/archaea.html

http://tolweb.org/tree

encyclopedia of inland waters || archaea

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