Key microbial drivers in Antarctic aquatic environments

33 Pages·2012·0.99 MB·English

REVIEW ARTICLE
Key microbial drivers in Antarctic aquatic environments
David Wilkins1, Sheree Yau1, Timothy J. Williams1, Michelle A. Allen1, Mark V. Brown1,2,
Matthew Z. DeMaere1, Federico M. Lauro1 & Ricardo Cavicchioli1
1SchoolofBiotechnologyandBiomolecularSciences,TheUniversityofNewSouthWales,Sydney,NSW,Australia;and2EvolutionandEcology
ResearchCentre,TheUniversityofNewSouthWales,Sydney,NSW,Australia
Correspondence:RicardoCavicchioli,School Abstract
ofBiotechnologyandBiomolecularSciences,
Antarctica is arguably the world’s most important continent for influencing the
TheUniversityofNewSouthWales,Sydney,
NSW2052,Australia. Earth’s climate and ocean ecosystem function. The unique physico-chemical
Tel.:[phone]; propertiesoftheSouthernOceanenablehighlevelsofmicrobialprimaryproduc-
fax:[phone]; tionto occur.Thisnotonly formsthebase ofa significant fraction oftheglobal
e-mail:[email protected] oceanic food web, but leads to the sequestration of anthropogenic CO and its
2
transport to marine sediments, thereby removing it from the atmosphere; the
Received7May2012;revised11August SouthernOceanaccountsfor~ 30%ofglobaloceanuptakeofCO despiterepre-
2012;accepted1October2012. 2
senting ~ 10% of the total surface area of the global ocean. The Antarctic conti-
DOI:10.1111/1574-6976.12007 nent itself harbors some liquid water, including a remarkably diverse range of
surfaceandsubglaciallakes.Beingoneoftheremainingnaturalfrontiers,Antarc-
Editor:CorinaBrussaard tica delivers the paradox of needing to be protected from disturbance while
requiringscientificendeavortodiscoverwhatisindigenousandlearnhowbestto
Keywords protect it. Moreover, like many natural environments on Earth, in Antarctica,
Antarcticlakes;SouthernOcean;Antarctic microorganismsdominatethegeneticpoolandbiomassofthecolonizableniches
microorganisms;metagenomics;microbial
andplaythekeyrolesinmaintainingproperecosystemfunction.Thisreviewputs
diversity;microbialloop.
intoperspectiveinsightthathasbeenandcanbegainedaboutAntarctica’saquatic
S microbiotausingmolecularbiology,andinparticular,metagenomicapproaches.
W
E
function properly. In low-temperature environments, the
I Introduction
V reducedkineticenergyimposesmanyconstraintsoncellu-
E lar activity; for example, rates of enzyme-catalyzed reac-
Low temperature: akey factor controlling the
R tions are reduced, membranes become rigid, solute
evolution of life on Earth
transport become compromised, and nucleic acids acquire
Y
Microorganisms have evolved to be able to colonize envi- inhibitory secondary structures that impinge on gene
G
ronmental niches that span a broad temperature range, expression and protein synthesis (Feller & Gerday, 2003;
O frombelow(cid:1)10 °Cto above 120 °C.However,individual Cavicchioli,2006;Siddiqui&Cavicchioli,2006;Margesin&
types of microorganisms have evolved a capacity to grow Miteva,2011;Siddiquiet al.,2013).
L
O within a definedtemperature range, typically 40 °C or less In view of the imposition that low temperature has on
(Williamset al.,2011).Asaresult,hyperthermophilesthat cellular processes, it is a striking realization that the
BI canthriveat100 °Ccannotgrowat4 °C.Evenmesophiles majority of microbial biomass resides in cold environ-
O that grow well at 37 °C can struggle to grow at tempera- ments. On the order of 85% of the Earth’s biosphere is
tures below 10 °C. The reason for this thermal effect on permanently below 5 °C, dominated by ocean depths, gla-
R
microorganisms pertains by and largeto the effect oftem- cier, alpine, and polar regions (Margesin & Miteva,
C
perature on kinetics (Feller & Gerday, 2003; Cavicchioli, 2011). Given the apparent irony that cold environments
I
M 2006; Siddiqui & Cavicchioli, 2006; Siddiqui et al., 2013). constrain growth rates yet represent the largest propor-
In effect, an enzyme or molecular machine that functions tion of the biosphere, many questions can be raised about
properlywithinitstemperaturerangewillexperienceinsuf- the characteristics of the indigenous psychrophilic micro-
ficient or excessive movement within its molecular struc- bial communities. Three obvious questions arise: which
ture at temperatures beyond that range to be able to microorganisms are present in cold environments; what
FEMSMicrobiolRev&&(2012)1–33 ª2012FederationofEuropeanMicrobiologicalSocieties
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2 D.Wilkinsetal.
biogeochemical processes do microorganisms in cold Ocean to absorb CO (Le Que´re´ et al., 2007). In addition
2
environments perform; and how have microorganisms to the threat to marine biota caused by ocean acidificat-
evolved and adapted to growth in the cold? This review ion (Kintisch & Stoksta, 2008; McNeil & Matear, 2008;
addresses the first two questions, focusing on the Antarc- Falkowski, 2012), nutrient supply in surface waters is
tic polar environment and reviewing discoveries made expected to decrease, particularly at higher latitudes as a
with the aid of metagenomic and other molecular biology result of increased stratification caused by ocean warming
techniques. The review does not address molecular mech- (Sarmiento and LeQue´re´, 1996; Wignall & Twitchett,
anisms of cold adaptation, and reviews of this topic are 1996; Matear & Hirst, 1999).
available (e.g. Feller & Gerday, 2003; Cavicchioli, 2006; A general problem with forecasting the impact of global
Siddiqui & Cavicchioli, 2006; Casanueva et al., 2010; climate change on Antarctic biota is the lack of physical
Margesin and Miteva, 2011; Siddiqui et al., 2013). and particularly biological records for Antarctica (Gille,
2008;McNeil&Matear2008;Rosenzweiget al.,2008;Steig
et al., 2009; AASSP, 2011). Scientific records are available
Antarctica: abrief overview
foronlyatinyfractionofthelandandsurroundingwaters,
Ninety percent of the Earth’s ice is present in Antarctica, and the biodiversity in East Antarctica in particular is the
equating to 60–70% of the Earth’s freshwater supply largest under-sampled region of the continental shelf
(AASSP, 2011). As a frozen deep mass of ice, Antarctica aroundAntarcticamakingitessentiallyimpossibletoapply
reflects the sun’s radiation to buffer against global warm- spatialmanagementtoareaprotection(AASSP,2011).This
ing trends. By maintaining freezing temperatures, cold issue is further compounded by the increasing risk associ-
water masses sink near the Antarctic continent and drive ated with direct anthropogenic impact to the Antarctic
thermohaline circulation of global ocean currents. While environment.SincehumansfirstvisitedAntarcticain1821,
temperatures in the interior of Antarctica have been the number of tourists (and research activities) has
recorded as low as (cid:1)89 °C, Antarctica’s coastal and sur- increasedgreatly,anditisbothchallengingtopreventnon-
roundingSouthernOceanregionsexperienceseasonaltem- indigenous microorganisms from being introduced into
peraturesthatriseabove0 °C. Antarctica(Cowanet al.,2011)andtoremediatesitesthat
As a result of the annual freeze/thaw cycle, the growth have become polluted (AASSP, 2011). Science plans of
(up to 19 9 106 km2) and melting of Antarctic sea ice many nations (e.g. AASSP, 2011) articulate the need for
represent one of the Earth’s most significant seasonal science to deliver information suitable for policy develop-
events (AASSP, 2011). The scale of the Antarctic sea ice ment to meet the challenges of global change, natural
(up to 1.5 9 the area of the Antarctic continent) places resourcesustainability,biodiversityconservation,andman-
into context the influence of anthropogenic climate agement of human impacts on the Antarctic continent.
change on the Antarctic region. Although satellite data While the integration of molecular information (e.g. ge-
suggest a small overall increase in sea ice extent since nomics, proteomics) with ecological principles and physi-
observations started in the 1970s, this masks the highly cal, chemical, and earth sciences represents one of the
variable nature of sea ice extent around the continent. biggest challenges in modern ecology, it also provides the
The effects of global warming have been particularly greatest opportunities for facilitating effective ecosystem
noted for the Antarctic Peninsula and most of West Ant- management (DeLong & Karl, 2005), particularly for the
arctica (Meredith & King, 2005; Murray and Grzymski, Antarctic environment (Hoag, 2003; Clark et al., 2004;
2007; Reid et al., 2009; Steig et al., 2009), extending to Cavicchioli,2007;Murray&Grzymski,2007;Cavicchioli&
South Georgia where some of the fastest warming waters Lauro, 2009; Lauro et al., 2011; Yau et al., 2011; Yau &
on Earth exist (Whitehouse et al., 2008; Hogg et al., Cavicchioli,2011).
2011) and a corresponding decrease in sea ice extent has The following sections review knowledge of microbial
been noted (e.g. Bellingshausen/Amundsen Seas; ~ 5% communities present in Antarctic lake and marine envi-
decrease per decade; Cavalieri & Parkinson, 2008). Con- ronments, emphasizing where available information that
versely, while other sectors of the continent are displaying has been obtained using metagenomics.
small but significant increases in sea ice extent since the
1970s (Zhang, 2007; Cavalieri & Parkinson, 2008), there
Antarctic lakes
is compelling ice-core evidence based on historical levels
of methanesulfonic acid that this apparent increase masks
Antarctica: unique lake systems that are
an ~ 20% decrease in sea ice extent since the early 1950s
sentinels for climate change
(Curran et al., 2003; Liu & Curry, 2010).
Anthropogenic climate change has been particularly Only 0.4% of the total ice area of Antarctica
associated with reducing the capacity of the Southern (12.3 9 106 km2)isseasonallyicefree,comprisingexposed
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MicrobesinAntarcticaquaticenvironments 3
Fig.1. Antarctica and the Southern Ocean. Polar Front (circumpolar full line); Maximum sea ice extent (circumpolar dotted line). Regions of
Antarcticashown,withlakesintheregionslistedinalphabeticalorder.DronningMaudCoast:DronningMaudLand;SchirmacherOasis.Enderby
Land: Syowa Oasis; Thala Hills. Kemp Land: Framnes Mountains; Stillwell Hills; Ufs Island. Marie Byrd Land: Coleman Ridge; Mt Richardson.
McMurdoSound,VictoriaLand,andTransantarcticMountains:BeardmoreGlacier;DarwinGlacierregion;McMurdoDryValleys;RossIsland;Terra
Nova Bay. Mertz Glacier Region: Commonwealth Bay. Prince Charles Mountains: Amery Oasis; Else Platform; Jetty Peninsula; Prince Charles
Mountains. PrydzBay,Vestfold,andLarsemannHills:Bollingen Islands;GillockIsland;Larsemann Hills;RauerIslands;VestfoldHills.WilkesLand
Coast:BungerHills;HaswellIsland;ObruchevHills;WindmillIslands.SouthernOceanregionsshown,withreferencesforstudiesfromtheregions
listedinalphabeticalorder.Agulhas/BenguelaBoundary:Simonetal.(1999);Seljeetal.(2004);Giebeletal.(2009).AntarcticPeninsula:DeLong
etal. (1994); Massana etal. (1998); Murray etal. (1998); Garcı´a-Martı´nez & Rodrı´guez-Valera (2000); Guixa-Boixereu etal. (2002); Hollibaugh
etal. (2002); Short & Suttle (2002); Brinkmeyer etal. (2003); Church etal. (2003); Short & Suttle (2005); Grzymski etal. (2006); Murray &
Grzymski(2007);Kalanetraetal.(2009);Manganellietal.(2009);Strazaetal.(2010);Bolhuisetal.(2011);Ducklowetal.(2011);Piquetetal.
(2011);Grzymskietal.(2012);Williamsetal.(2012a).AtlanticSector:Giebeletal.(2009);Weinbaueretal.(2009).AustralianSector:Oliveretal.
(2004); Abell & Bowman (2005a, b); Evans etal. (2009); Evans etal. (2011); Wilkins etal. (2012); Williams etal. (2012b). Kerguelen Plateau:
Christaki etal. (2008); West etal. (2008); Obernosterer etal. (2011); Ghiglione & Murray (2012). McMurdo Sound, Victoria Land, and
TransantarcticMountains:Murrayetal.(1998).MertzGlacierRegion:Bowman&McCuaig(2003);Bowmanetal.,(2003);Wilkinsetal.(2012).
Pacific Sector: Hollibaugh etal. (2002). Ross Sea: Murray etal. (1998); Hollibaugh etal. (2002); Gast etal. (2004); Gowing etal. (2004); Gast
etal.(2006);Gentileetal.(2006);Kohetal.(2010,2011);Cowieetal.(2011);Ghiglione&Murray(2012);LoGiudiceetal.(2012).ScotiaSea:
Murray etal. (1998); Garcı´a-Martı´nez & Rodrı´guez-Valera (2000); Lo´pez-Garcı´a etal. (2001); Topping etal. (2006); Giebel etal. (2009);
Manganelli etal. (2009); Murray etal. (2010); Jamieson etal. (2012). Weddell Sea: Garcı´a-Martı´nez and Rodr´ıguez-Valera (2000); Brinkmeyer
etal.(2003).WilkesLandCoast:Bowmanetal.(1997a);Brown&Bowman(2001);Piquetetal.(2008);Patterson&Laybourn-Parry(2012).
FEMSMicrobiolRev&&(2012)1–33 ª2012FederationofEuropeanMicrobiologicalSocieties
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4 D.Wilkinsetal.
mountains (e.g. Ellsworth and Transantarctic Mountains, (Green et al., 1988). Subglacial and epiglacial lakes also
the North Victoria Land mountains, and the nunataks) appear to be prevalent in Antarctica with at least 145 sub-
and coastal areas (e.g. lower-latitude Antarctic Peninsula glacial lakes identified (Siegert et al., 2005; Gibson, 2006;
in West Antarctica, and the Vestfold Hills and McMurdo Cavicchioli, 2007; Pearce, 2009). Epiglacial lakes form as
Dry Valleys) (Poland et al., 2003; Cary et al., 2010) a result of glacier ice melt, on the down-ice flow sides of
(Fig. 1). Within this ice-free 50 850 km2 area of Antarc- mountains that penetrate the polar ice cap, and organ-
tica, the geographic distribution and diversity of types of isms inhabiting the lakes could be recent (postglacial) or
aquaticsystemsareconsiderable,rangingfromfreshtohy- ancient inhabitants of Antarctica (Gibson, 2006; Cavicchi-
persaline, permanently ice covered to perennially ice free, oli, 2007).
andmixedtostratified(dimictic,polymictic,amictic,mer- In the Vestfold Hills (68°33′S, 78°15′E), more than 300
omictic). Lake biota is microbially dominated with gener- lakes and ponds from freshwater (< 0.1%) to hypersaline
ally reduced diversity and few or no metazoans present (32%) have been described, including ~ 20% of the
(Laybourn-Parry, 1997), and distinct communities inhabit world’s meromictic lakes (Gibson, 1999). The Australian
specific niches including ice, the water column, sediment, Antarctic Data Centre describes more than 3000 water
andmicrobialmats. bodies (fresh and saline) mapped in the Vestfold Hills,
The age of water within Antarctic lakes varies consider- ranging in area from 1 to 8 757 944 m2. Fjords also cut
ably, with the subglacial outflow from Blood Falls esti- across the Vestfold Hills. Some of these are large, such as
mated to be 1.5 million years old (Mikucki et al., 2009), Ellis Fjord, which is 10 km long, up to 100 m deep, and
the water in Ace Lake about ~ 5000 years old (Rankin has become a stratified system due to its restricted open-
et al., 1999), and Lake Miers water < 300 years old ing (< 4 m deep) to the ocean (Burke & Burton, 1988).
Table1. MaingroupsofmicroorganismsassociatedwithkeymetabolicprocessesinAntarcticlakesandmats
Detected
Microorganism Keyfunctions inmats? Comments
Cyanobacteria OxygenicphotosynthesisandN fixation Yes Moreprevalentinlowersalinityenvironments,
2
generallydominatemats
Greensulfurbacteria Anaerobicanoxygenicphototrophy,N No Prevalent,predominantinsalinelakesofthe
2
(GSB)(Chlorobi) fixation,andH S/Soxidation VestfoldHills
2
Greennonsulfur Anoxygenicphototrophyandheterotrophy No Mainlydetectedinsalinelakes;limiteddistribution
bacteria(Chloroflexi)
Alphaproteobacteria Heterotrophyandaerobicanoxygenic Yes Metabolicallydiversegeneralistswithwidedistribution;
phototrophy somegroupslinkedtoalgalblooms(e.g.Roseobacter
clade),othersoligotrophic(SAR11clade)
Betaproteobacteria Heterotrophy,nitrification,andanoxygenic Yes Dominatefreshwaterlakes;someassociatedwithalgal
phototrophy blooms(OM43)
Gammaproteobacteria Heterotrophy,anoxygenicphototrophy, Yes Includesheterotrophs(e.g.Alteromonadales/
nitrification,andnitrate/DMSO/metal Oceanospirillales),anoxygenicphototrophs(purple
reduction sulfurbacteria=Chromatiales),sulfuroxidizers
(Thiotrichales);widedistribution
Deltaproteobacteria Dissimilatorysulfur/sulfatereduction Yes Predominantsulfatereducers,foundinanoxicwaters
Firmicutes Fermentationandsulfate/nitrate/metal Yes Mostprevalentinanoxicwaterandsediment
reduction
Actinobacteria Heterotrophy Yes Widedistribution,mayincreaseindominancewith
trophicstatusinfreshwaterlakes
Cytophaga–Flavobacterium Aerobicheterotrophy Yes Widedistribution,linkedwithalgalblooms,prefer
–Bacteroides(CFB)group HMWcarbon
Methanogenic Hydrogenotrophic,acetoclastic,and Yes Limitedtoanoxicwaters,usuallywheresulfateand
Archaea methylotrophicmethanogenesis nitratearedepleted
Haloarchaea Heterotrophy No Limitedtohypersalinelakes
Diatoms Oxygenicphotosynthesis Yes Candominatematcommunities,widedistribution,
speciesvarywithsalinity
Phytoflagellates Oxygenicphotosynthesisandmixotrophy Yes Canbedominantprimaryproducersinlakes;wide
distribution
Flagellatesand Aerobicheterotrophy Yes Mayoccupyhighesttrophiclevel
ciliates
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MicrobesinAntarcticaquaticenvironments 5
Many of the coastal lake systems, including a large num- have also made use of denaturing gradient gel electropho-
ber in the Vestfold Hills, are marine derived, having been resis (DGGE) to provide a molecular ‘fingerprint’ of the
separated from the marine environment ~ 3000–7000 years community (Pearce, 2003; Pearce et al., 2003; Karr et al.,
agobyisostaticreboundoftheAntarcticcontinent(Gibson, 2005; Pearce, 2005; Pearce et al., 2005; Unrein et al.,
1999). The marine-derived systems provide unique 2005; Glatz et al., 2006; Mikucki & Priscu, 2007; Mosier
opportunities for studying the evolution of marine micro- et al., 2007; Schiaffino et al., 2009; Villaescusa et al.,
bial populations to chemically, physically, and temporally 2010). Functional genes have also been targeted using
defined ecosystem changes (e.g. Lauro et al., 2011). Due PCR amplification to assess the potential of biochemical
to global warming, by being exposed annually to longer processes occurring, such as nitrogen fixation (Olsen
periods of temperatures above 0 °C, the lake systems are et al., 1998), ammonia oxidation (Voytek et al., 1999),
at an increasing risk of being physically perturbed (e.g. anoxygenic photosynthesis (Karr et al., 2003), and dissim-
ice cover melt exposing the water column to longer peri- ilatory sulfate reduction (Karr et al., 2005; Mikucki et al.,
ods of wind turbulence, and increasing surface tempera- 2009).
tures and irradiation penetrating deeper and for longer). Empowered by technological advances in DNA
The reduced biodiversity of Antarctic lakes makes them sequencing, the value of applying metagenomics to
ideal model systems to examine microbial influence on microbial communities in Antarctic lakes has been real-
geochemistryasitispossibletoencompassalargepropor- ized (Cavicchioli, 2007; Yau & Cavicchioli, 2011).
tion of the diversity present and relate taxa to particular Metagenomic studies have assessed both the taxonomic
processes (Laybourn-Parry & Pearce, 2007; Lauro et al., composition and genetic potential of lake communities,
2011). Through the use of molecular methods, new and in some cases have linked function to specific mem-
insights are being derived on how microorganisms have bers of the community (Lo´pez-Bueno et al., 2009; Ng
adapted to the Antarctic environment under a diverse et al., 2010; Lauro et al., 2011; Yau et al., 2011; Varin
array of chemical and physical conditions. By being espe- et al., 2012). When coupled with functional ‘omic’ tech-
cially sensitive to climatic influences, these Antarctic lakes niques (to date, metaproteomics has been applied, but
function as sentinels for monitoring climate change. By not metatranscriptomics or stable isotope probing), infor-
understanding plausible functional relationships between mation has also been gained about the genetic comple-
ecosystem components in these lakes, there is capacity to ment that has been expressed by the resident populations
monitor ecosystem health. By providing key sentinel indi- (Ng et al., 2010; Lauro et al., 2011; Yau et al., 2011).
cators,managersofhumanactivities,policymakers,scien-
tists, and the general public can become better informed
Bacterialdiversity: adaptation to unique
about the causes and effects and consequences of human
physical and chemical conditions
activities,includinganthropogenicclimatechange.
The topics in this Antarctic lakes section describe find- The vast majority of molecular studies of Antarctic lakes
ings linked to important members of the Bacteria, have focused on bacteria. Consistent with the wide range
Archaea, Eucarya (Table 1), and viruses that inhabit the of physical and chemical properties of Antarctic lakes, a
water column, assessments of lake microbial mat commu- large variation in species assemblages have been found.
nities, and ‘omic’-based studies that have led to an inte- While exchange of microorganisms must be able to occur
grated view of ecosystem function. between lakes that are in close vicinity to each other, the
picture that has emerged from the data to date is that
microbial populations are relatively unique to each type
Molecular approaches used in Antarctic lake
of isolated system. Nonetheless, certain trends in bacterial
systems
composition are also apparent. Focusing on the similari-
The majority of molecular-based studies of Antarctic ties, lakes of equivalent salinities tend to have similar
aquatic microbial communities have made use of PCR communities. Hypersaline lakes from the Vestfold Hills
amplification of small subunit ribosomal RNA sequences (Bowman et al., 2000b) and McMurdo Dry Valleys (Glatz
to survey the diversity of Bacteria and in some cases et al., 2006; Mosier et al., 2007) were all dominated by
Archaea and Eucarya (Supporting Information, Tables S1 Gammaproteobacteria and members of the CFB group
and S2). Microbial composition has been determined by (= Bacteroidetes) as well as harboring lower abundance
cloning and sequencing of rRNA gene amplicons exclu- populations of Alphaproteobacteria, Actinobacteria, and
sively (Bowman et al., 2000a; Bowman et al., 2000b; Firmicutes. The surface waters of saline lakes resemble
Gordon et al., 2000; Christner et al., 2001; Purdy et al., marine communities dominated by CFB, Alphaproteobac-
2003; Karr et al., 2006; Matsuzaki et al., 2006; Kurosawa teria, and Gammaproteobacteria, but divisions such as
et al., 2010; Bielewicz et al., 2011), although most studies Actinobacteria and specific clades of Cyanobacteria have
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6 D.Wilkinsetal.
been found to be overrepresented compared to the ocean that the inhibition may have been caused by an as yet
(Lauro et al., 2011). Sediments from saline lakes in the unidentified chemical factor (Ward et al., 2005; Glatz
Vestfold Hills (Bowman et al., 2000a) and Nuramake-Ike et al., 2006).
in the Syowa Oasis (Kurosawa et al., 2010) were very The relative isolation and diverse chemistries of the
similar, containing in addition to the surface clades, lakes facilitate biogeographical studies. The anoxic and
Deltaproteobacteria, Planctomycetes, Spirochaetes, Chloro- sulfidic bottom waters of some meromictic lakes form
flexi (green nonsulfur bacteria), Verrucomicrobia, and due to a density gradient that precludes mixing. Although
representatives of candidate divisions. Plankton from sedimentation from the upper aerobic waters may occur,
freshwater lakes were characterized by an abundance of there is little opportunity for interchange of species with
Betaproteobacteria, although Actinobacteria, CFB group, the bottom water of lakes allowing for greater divergence
Alphaproteobacteria, and Cyanobacteria were also promi- in community composition as nutrients can become
nent (Pearce et al., 2003; Pearce, 2005; Pearce et al., 2005; depleted and products of metabolism can accumulate. As
Schiaffino et al., 2009). a result, distinct distributions of bacterial groups can
Differences in bacterial community structure are also inhabit these strata, and different types of microorganisms
influenced by nutrient availability. In studies of freshwa- can be found in equivalent strata in different lakes. A
ter lakes in the Antarctic Peninsula and the South Shet- good example of this is the presence of common types of
land Islands, cluster analysis of DGGE profiles grouped purplesulfurbacteria(Chromatiales) and(GSB= Chlorobi)
together lakes of similar trophic status (Schiaffino et al., in some meromictic lakes and stratified fjords in the
2009; Villaescusa et al., 2010). Most of the variance in Vestfold Hills (Burke & Burton, 1988), compared to
community structure could be explained by related chem- diverse ‘purple nonsulfur bacteria’ in Lake Fryxell in Vic-
ical parameters such as phosphate and dissolved inorganic toria Land (Karr et al., 2003).
nitrogen. Similarly, three freshwater lakes, Moss, Sombre, In Lake Bonney, the east and west lobes harbor over-
and Heywood on Signy Island, are alike except that Hey- lapping but distinct communities in the suboxic waters
wood Lake is enriched by organic inputs from seals. Bac- (Glatz et al., 2006). The east lobe was dominated by
terial composition in each lake changed from winter to Gammaproteobacteria and the west lobe by CFB, illustrat-
summer, and this was again correlated to variation in ing how divergent communities can form from the same
physico-chemical properties (Pearce, 2005). The bacterial seed population. In contrast, ice communities are more
population of Heywood Lake had shifted from a domi- readily dispersed by wind, aerosols, and melt water, and
nance of Cyanobacteria toward a greater abundance of 16S rRNA gene probes designed from bacteria trapped in
Actinobacteria and marine Alphaproteobacteria (Pearce the permanent ice cover of Lake Bonney hybridized to
et al., 2005). This hints at a link between a copiotrophic microbial mat libraries sourced up to 15 km away
lifestyle in the Heywood Lake Actinobacteria and inhibi- (Gordon et al., 2000). This demonstrates how a single
tion of Antarctic freshwater Cyanobacteria by eutrophica- lake may encompass microorganisms that are biogeo-
tion. This type of study exemplifies how inferences can be graphically dispersed, while also harboring others that
made about taxa and function by examining population have restricted niches and are under stronger selection
changes over time and over gradients of environmental pressure.
parameters. Subglacial systems, such as Lake Vostok, have been iso-
Inferring functional potential from taxonomic surveys lated from the open environment for hundreds of thou-
can be problematic due to species- or strain-level differ- sands to millions of years (Siegert et al., 2001). As a
ences in otherwise related bacteria. For example, the result, they provide a reservoir of microorganisms that
majority of the Gammaproteobacteria in hypersaline lakes may have undergone significant evolutionary divergence
were relatives of Marinobacter suggesting that this genus from the same seed populations that were not isolated by
is particularly adapted to hypersaline systems (Bowman the Antarctic ice cover. The uniqueness of these types of
et al., 2000b; Glatz et al., 2006; Matsuzaki et al., 2006; systems also creates a conundrum for studying them.
Mosieret al.,2007).Nonetheless,Marinobacterspeciesfrom Lake Vostok is approximately 4 km below the continental
different lakes appeared biochemically distinct as isolates ice sheet making it extremely difficult to determine suit-
from hypersaline lake Suribati-Ike were all able to respire able means for accessing the lake without inadvertently
dimethylsulfoxide (DMSO) but not nitrate (Matsuzaki contaminating it with biological (e.g. surface microorgan-
et al., 2006). In contrast, those from the west lobe of Lake isms) or chemical (e.g. drilling fluid) matter (Inman
Bonney were all able to respire nitrate (Ward & Priscu, 2005; Wingham et al., 2006; Lukin & Bulat 2011; Gram-
1997). Interestingly, in the east lobe of the same lake, ling, 2012; Jones, 2012). To date, molecular microbial
nitrate respiration was inhibited although a near-identical studies have concentrated on the accretion ice above the
Marinobacter phylotype was present; it was speculated ice–water interface (Priscu et al., 1999; Christner et al.,
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MicrobesinAntarcticaquaticenvironments 7
2001). Accretion ice has been found to contain a low environments with the phylotypes differing between the
density of bacterial cells from Alphaproteobacteria, Beta- lakes examined (Bowman et al., 2000a). While a phylo-
proteobacteria, Actinobacteria, and CFB divisions closely type similar to Methanosarcina was identified, the major-
allied to other cold environments. Molecular signatures of ity were highly divergent. Similarly, Methanosarcina and
a thermophilic Hydrogenophilus species were also identi- Methanoculleus were detected in Lake Fryxell but other
fied in accretion ice raising the possibility that chemoau- members of the Euryarchaeota and Crenarchaeota (a sin-
totrophic thermophiles were delivered to the accretion ice gle sequence) were divergent, clustering only with marine
from hydrothermal areas in the lake’s bedrock (Bulat clones (Karr et al., 2006). Based on the lake chemical gra-
et al., 2004; Lavire et al., 2006). However, interpretation dients and the location of these novel phylotypes in the
of results from samples sourced from the Lake Vostok water column, the authors speculated these Archaea may
bore hole is very challenging as it is difficult to differenti- be have alternative metabolisms such as anoxic methano-
ate contaminants from native Vostok microorganisms. trophy or sulfur utilization. In sediments from Lake Nur-
From a study that assessed possible contaminants present ume-Ike in the Langhovde region, 205 archaeal clones
in hydrocarbon-based drilling fluid retrieved from the grouped into three phylotypes, with the predominant
Vostok ice core bore hole, six phylotypes were designated archaeal clone being related to a clone from Burton Lake
as new contaminants (Alekhina et al., 2007). Two of these in the Vestfold Hills, while the other two did not match
were Sphingomonas phylotypes essentially identical to to any cultivated species (Kurosawa et al., 2010). Consis-
those found in the accretion ice core (Christner et al., tent with these observations, from a metagenomic study
2001), which raises question about whether bacterial sig- that involved the analysis of ~ 9 million genes, a high
natures identified from the ice cores are representative of level of divergence was found for the Archaea present in
Lake Vostok water, and further highlights the ongoing the bottom waters of Ace Lake, the majority of which did
problem of causing forward contamination into the lake. not match to known methanogens including M. frigidum
and M. burtonii that were isolated from the lake (Lauro
et al., 2011). However, high levels of methane are present
Archaea:methanogens and haloarchaea
in Ace Lake bottom waters, and this is likely to have been
Archaea have been detected mainly in anoxic sediments produced gradually by the methanogenic community, and
and bottom waters from lakes that range in salinity from retained in the lake due to the very low potential for aer-
fresh to hypersaline, and those with known isolates are obic methane oxidation and the apparent absence of
affiliated with methanogens or haloarchaea (Bowman anaerobic methane-oxidizing Euryarchaeota (Lauro et al.,
et al., 2000a, b; Purdy et al., 2003; Kurosawa et al., 2010; 2011).
Lauro et al., 2011). Anoxia allows for the growth of In hypersaline lakes where bottom waters do not
methanogenic archaea that mineralize fermentation prod- become completely anoxic, methanogens are not present
ucts such as acetate, and H and CO into methane, and archaea have extremely low abundance. For example,
2 2
thereby performing an important step in carbon cycling. only two archaeal clones of the same phylotype were
The acetoclastic methanogens thrive in environments recovered from deep water samples from Lake Bonney
where alternative terminal electron acceptors such as sul- (Glatz et al., 2006), and Organic Lake in the Vestfold
fate and nitrate have been depleted. One example of this Hills had an extremely low abundance of archaeal clones
is Lake Heywood where methanogenic archaea were related to Halobacteriales (Bowman et al., 2000b). In con-
found to comprise 34% of the total microbial population trast to these stratified hypersaline lakes, the microbial
in the freshwater sediment, the majority of which were community in the extremely hypersaline Deep Lake is
Methanosarcinales, which include acetate and C1-com- dominated by haloarchaea (Bowman et al., 2000b). Many
pound utilizing methanogens (Purdy et al., 2003). Both of the clones identified from Deep Lake are similar to
H : CO (Methanogenium frigidum) and methylamine/ Halorubrum (formerly Halobacterium) lacusprofundi, which
2 2
methanol (Methanococcoides burtonii) utilizing methano- was isolated from the lake (Franzmann et al., 1988). The
gens were isolated from Ace Lake (Franzmann et al., genome sequence of H. lacusprofundi has been completed,
1992, 1997) providing opportunities for genomic analyses and ongoing metagenome studies are examining the
(Saunders et al., 2003; Allen et al., 2009) and a host of microbial community composition and microbial ecology
studies addressing molecular mechanisms of cold adapta- of the lake (R. Cavicchioli et al., unpublished results).
tion (e.g. Cavicchioli, 2006; Williams et al., 2011).
In general, archaeal populations appear to be adapted
Eucarya perform multiple ecosystem roles
to their specific lake environment. Sediments from saline
lakes of the Vestfold Hills were inhabited by members of Single-celled Eucarya are important members of Antarctic
the Euryarchaeota typically found in sediment and marine aquatic microbial communities. In many Antarctic systems,
FEMSMicrobiolRev&&(2012)1–33 ª2012FederationofEuropeanMicrobiologicalSocieties
PublishedbyBlackwellPublishingLtd.Allrightsreserved
8 D.Wilkinsetal.
eucaryal algae are the main photosynthetic organisms, picoeucaryal member of the Chlorophyta, and that phy-
and in others, only heterotrophic protists occupy the top codnaviruses were likely to be controlling the seasonal
trophic level. As eucaryal cells are generally large with population dynamics of this alga (Lauro et al., 2011);
characteristic morphologies, microscopic identifications previously, it was interpreted that the virus-like particles
have been used. However, microscopy is unable to classify were likely to be bacteriophages infecting bacteria (Madan
smaller cells such as nanoflagellates with high resolution, et al., 2005). Further studies are necessary to determine
although these may constitute a high proportion of algal the basis for apparent specific adaptations of some species
biomass. For example, five morphotypes of Chrysophyceae to particular lakes or lake strata, and for the cosmopoli-
evident in Antarctic lakes were unidentifiable by light tan distribution of others. Here, molecular-based research
microscopy but were able to be classified using DGGE of the kind that has been applied to bacteria such as
and DNA sequencing (Unrein et al., 2005). Consistent functional gene surveys will undoubtedly help answer
with this, molecular studies specifically targeting eucaryal these questions.
diversity (Unrein et al., 2005; Mosier et al., 2007; Bie-
lewicz et al., 2011) have identified a much higher level of
Antarctic virus diversity and top-down
diversity than previously suspected, and the studies have
ecosystem control
discovered lineages not previously known to be present
such as silicoflagellates (Unrein et al., 2005) and fungi In the absence of metazoan grazers, viruses are hypothe-
(Mosier et al., 2007; Bielewicz et al., 2011). sized to play an increased role in the microbial loop in
Most eucarya in Antarctic lakes are photosynthetic Antarctic systems (Kepner et al., 1998) and as drivers of
microalgae that are present in marine environments with microbial evolution (Anesio & Bellas, 2011). This idea
a wide distribution including chlorophytes, haptophytes, has been supported by microscopy-based observations of
cryptophytes, and bacillariophytes. Molecular methods viral density, virus-to-bacteria ratios, and infection rates
have afforded deeper insight into the phylogenetic diver- that are different in Antarctic lakes than lower-latitude
sity within these broader divisions and have revealed systems (Laybourn-Parry et al., 2001; Madan et al., 2005;
some patterns in their distribution. Using 18S rRNA gene Laybourn-Parry et al., 2007; Sa¨wstro¨m et al., 2007).
amplification and DGGE, the same chrysophyte phylo- Morphological examination of virus-like particles only
types were identified in lakes from the Antarctic Penin- provides limited insight into viral physiology and diver-
sula and King George Island despite being 220 km apart sity. Metagenomics has enabled unprecedented insight
(Unrein et al., 2005) indicating these species may be well into viruses by permitting more precise classification,
adapted to Antarctica or highly dispersed. Similarly, an information on genetic content, and discovery of novel
unknown stramenopile sequence was detected throughout species.
the 18S rRNA clone libraries of Lake Bonney demonstrat- Metagenomic analysis of the viriome of the freshwater
ing a previously unrecognized taxon occupied the entire Lake Limnopolar, Livingston Island, uncovered the great-
photic zone in the lake (Bielewicz et al., 2011). In con- est depth of viral diversity of any aquatic system to date
trast, other groups showed distinct vertical and temporal (Lo´pez-Bueno et al., 2009). Representatives from 12 viral
distributions with cryptophytes dominating the surface, families were detected, but unlike the two previous viro-
haptophytes the midwaters, and chlorophytes the deeper mes that had been published at that time using compara-
layers during the summer while stramenopiles increased ble techniques, ssDNA viruses, and large dsDNA viruses
in the winter (Bielewicz et al., 2011). that putatively infect Eucarya were the dominant viral
The influence of flagellates on ecosystem function is types rather than bacteriophages. The ssDNA viruses were
not necessarily clear-cut as they can simultaneously inha- related to circoviruses, geminiviruses, nanoviruses, and
bit several trophic levels. For instance, in Ace Lake, the satellites; viruses previously only known to infect plants
mixotrophic phytoflagellate Pyramimonas gelidocola derives and animals indicating they are much more diverse than
a proportion of its carbon intake through bacterivory previously suspected and may constitute new viral fami-
(Bell & Laybourn-Parry, 2003) but in the nearby Highway lies. Samples taken in summer showed a shift in the viral
Lake, it uptakes dissolved organic carbon (DOC) (Laybo- community composition toward phycodnaviruses similar
urn-Parry et al., 2005). This again illustrates potential to Ostreococcus tauri virus, OtV5. This shift potentially
limitations for deriving ecosystem-level functions from reflects an increase in the host algae that are stimulated
taxonomic studies alone, even with taxa that appear phys- to bloom by the increased light availability.
iologically straightforward. A good illustration of this was Metagenomic data from Ace Lake revealed a viral com-
the finding from shotgun metagenomics that a large munity comprising Phycodnaviridae, Myoviridae, Siphovir-
proportion of the 18S rRNA gene sequences in the idae, Podoviridae, and unidentified viral families (Lauro
aerobic zone of Ace Lake were related to Mantoniella, a et al., 2011). Bacteriophages were abundant in the bottom
ª2012FederationofEuropeanMicrobiologicalSocieties FEMSMicrobiolRev&&(2012)1–33
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MicrobesinAntarcticaquaticenvironments 9
waters, whereas the surface summer community, similar close association of organisms facilitates diverse metabolic
to Lake Limnopolar (Lo´pez-Bueno et al., 2009), was processes, biogeochemical cycling, and niche differentia-
dominated by phycodnaviruses (Lauro et al., 2011). Most tion, which affords greater microbial growth and survival
notably, no viral signatures were found at 12.7 m depth, than would be possible for individual species alone (Paerl
which is a zone occupied by a near-clonal population of et al., 2000). Cyanobacterial mat systems are widespread
GSB. Mathematical modeling predicted that the absence in the lake environments of Antarctica, and they often
of phage predation in the GSB could be due to an adap- dominate the total biomass and productivity in these eco-
tation to longer cycles of growth and inactivity in systems (Vincent, 2000; Moorhead et al., 2005; Laybourn-
response to the polar light regime. Phototrophs with fas- Parry & Pearce, 2007).
ter growth rates, such as eucaryal algae and Cyanobacteria Although microbial mats are common across Antarc-
in the surface water, were predicted to be more suscepti- tica (Fig. 1, Table S2), the specific organisms present in a
ble to viral predation. The viral susceptibility of these mat may vary considerably. Certain groups are regularly
phototrophs was predicted to lead to increased host detected in Antarctic mats: Cyanobacteria, particularly
genetic variation, and this was borne out in the analysis members of the Oscillatoriales such as Leptolyngbya and
of the metagenome data (Lauro et al., 2011). Phormidium, and the Nostocales (Taton et al., 2003;
Metagenome analysis also unveiled some unexpected Jungblut et al., 2005; Taton et al., 2006; Ferna´ndez-
findings about viral–host interactions in Organic Lake in Valiente et al., 2007; Sutherland, 2009; Borghini et al.,
the Vestfold Hills. In the metagenome, a relative of the 2010; Verleyen et al., 2010; Anderson et al., 2011; Callejas
newly described virophage family (La Scola et al., 2008; et al., 2011; Fernandez-Carazo et al., 2011), Proteobacteria,
Fischer & Suttle, 2011) was discovered (Yau et al., 2011). the CFB group, Actinobacteria, and Firmicutes (Brambilla
A virophage depends upon a giant helper or ‘host’ virus et al., 2001; Van Trappen et al., 2002; Peeters et al., 2011;
to replicate but is detrimental to its helper (La Scola Antibus et al., 2012a; Varin et al., 2012). Less commonly
et al., 2008). Termed the Organic Lake virophage (OLV), reported are Deinococcus-Thermus, Planctomycetes, Ver-
genomic evidence pointed toward OLV being a virophage rucomicrobiales, and others (Brambilla et al., 2001; Anti-
of Organic Lake phycodnaviruses (OLPV) that infect bus et al., 2012b; Peeters et al., 2012; Varin et al., 2012).
eucaryal algae (Yau et al., 2011). Modeling of the OLV– Diatoms may be absent (Anderson et al., 2011), present
OLPV and algal host dynamics indicated that the pres- at low levels alongside dominant Cyanobacteria (Suther-
ence of OLV may contribute to stability of the algal land, 2009; Hawes et al., 2011), or in some cases present
populations by increasing the frequency of algal blooms, as the dominant phototrophs (Ferna´ndez-Valiente et al.,
and contributing to the carbon flux throughout the lake. 2007). Other Eucarya such as green algae, fungi, and tar-
The major capsid protein gene sequence was also detected digrades have been noted in a wide range of mats (Verl-
in Ace Lake, and a number of temperate aquatic environ- eyen et al., 2010). Many studies report detection of novel
ments suggesting that virophages may have widespread bacterial species and genera (Brambilla et al., 2001; Peet-
ecological influence. ers et al., 2011; Peeters et al., 2012), and there is no
Understanding of Antarctic viral diversity and ecology doubt mat communities are a reservoir of considerable
is still in its early days, because a complete viral survey is new biodiversity. In contrast, archaeal diversity in Antarc-
problematic due to the lack of a universal viral gene or tic mats is yet to be well studied, with only a few studies
even universal genetic material. Furthermore, the enor- examining their presence (Brambilla et al., 2001; Varin
mous depth of viral diversity remains largely unsampled et al., 2012), and viral populations in mats are almost
so most viral sequences have no significant similarity to completely undocumented.
sequence data repositories (Lo´pez-Bueno et al., 2009; Yau Surprisingly, even some very recent studies of Antarctic
et al., 2011). What is clear is that viruses perform a cru- mats have relied on microscopy, morphological taxon-
cial role in shaping community structure, driving host omy, and culturing rather than employing modern, cul-
evolution, contributing to the dissolved nutrient pool, ture-independent molecular methods for community
and understanding them is essential to understanding characterization. A number of these studies focus on
ecosystem function (Danovaro et al., 2011). Cyanobacteria and their key roles in mat formation, where
morphological taxonomy is possible because of the large
and distinctive cell shapes (Sutherland, 2009; Sutherland
Microbial mats as microcosms of Antarctic life
& Hawes, 2009; Borghini et al., 2010; Anderson et al.,
Microbial mats are dense, vertically stratified communi- 2011). Other studies focused on obtaining bacterial
ties typically dominated by cyanobacteria or algae in isolates, because of the advantages of having novel organ-
which microorganisms orientate themselves in response isms in culture for future characterization and biotechno-
to micrometer-scale light and chemical gradients. The logical exploitation (Brambilla et al., 2001; Van Trappen
FEMSMicrobiolRev&&(2012)1–33 ª2012FederationofEuropeanMicrobiologicalSocieties
PublishedbyBlackwellPublishingLtd.Allrightsreserved
10 D.Wilkinsetal.
et al., 2002; Peeters et al., 2011; Peeters et al., 2012). deep) was drained by a crack in an ice dam (Sutherland,
Nevertheless, more widespread use of molecular methods 2009). The newly created ponds have sizes ranging from
is desirable for gaining greater resolution of species com- 1.2 to 660 m2, conductivities from 2.8 to 22.3 mS cm(cid:1)1,
position and community diversity. The advantage pro- pH from 7.4 to 10.5, and DOC from 18.6 to 140 g m(cid:1)3.
vided is illustrated by the cultivation of isolates from Two years after their formation, the cyanobacterial popu-
ancient algal mats yielding 15 types of cultivable bacteria lation distribution varied greatly among the new ponds
(Antibus et al., 2012b), compared to 215 operational tax- (e.g. Phormidium autumnale ranged from 0% to 83% of
onomic units (OTUs) for the same mats using clone total community in any given pond), while 60% of dia-
libraries (Antibus et al., 2012a). Similarly, in studies tom species remained in common to all ponds. These
focused only on the presence of Cyanobacteria, 16 mor- community shifts have evolved from the original lake
photypes were identified from five mats by microscopy biota functioning as a seed inoculum, and can be related
compared to 28 OTUs by molecular methods (Taton to the conductivity, nitrate, DOC, and desiccation profiles
et al., 2006), and in a separate study of mats from the of the new ponds (Sutherland, 2009).
Transantarctic Mountains, six species were identified by
microscopy and 15 by molecular methods (Fernandez-
Antarctic lakes asmodels to understand whole
Carazo et al., 2011).
ecosystem function
Large-scale metagenomic studies provide a much
greater level of information, and this is well illustrated The relatively low diversity of Antarctic microbial food
by the yield of taxonomic and functional data that was webs existing within effectively closed systems allows for
obtained from an Antarctic microbial mat from fresh an integrative understanding of the microbial community
pond on the McMurdo Ice Shelf (Varin et al., 2012). A and biogeochemical cycling to be obtained. Studies of
total of 83 271 sequences were obtained from the mat, Blood Falls, an outflow of anoxic ferrous brine from the
with ~ 25% having matches in the SEED phylogenetic Taylor Glacier in the McMurdo Dry Valleys, revealed an
profile database and 14% having matches to the SEED unusual iron–sulfur cycle. The water is sulfate rich, exists
metabolic profile subsystems database. In addition to in permanent darkness, and is estimated to have been iso-
documenting the bacterial, archaeal, eucaryal, and viral lated from external inputs for 1.5 million years (Mikucki
taxa present (Table S2), the data enabled inferences et al., 2009). 16S rRNA gene analysis showed the commu-
about which taxa contributed what functional capaci- nity was dominated by a close relative of Thiomicrospira
ties, a boon for understanding the diverse mechanisms arctica, an autotrophic sulfur-oxidizing gammaproteobac-
of adaptation present in this community. For cold terium (Thiotrichales), as well as sequences related to
adaptation, it was inferred that fatty acid desaturases Delta- and Gammaproteobacteria capable of iron and/or
were hallmarks of Cyanobacteria, while DNA gyrase A sulfur compound reduction, and CFB capable of hetero-
genes were present in Betaproteobacteria, Planctomycetes, trophic growth on complex organic compounds (Mikucki
Alphaproteobacteria, and CFB. Chaperones dnaK and & Priscu, 2007). A large proportion of adenosine 5′-phos-
dnaJ were distributed across Cyanobacteria, Alpha- phosulfate reductase genes related to those involved in
and Betaproteobacteria, Actinobacteria, Planctomycetes, and dissimilatory sulfate metabolism were detected. However,
others, while osmolyte (choline and betaine) uptake- dissimilatory sulfite reductase (dsrA) was not present, and
related proteins were most common in Alphaproteobac- radioisotope data indicated sulfide is not produced. The
teria, followed by Betaproteobacteria, Cyanobacteria, implication of this is that sulfate reduction does not
Actinobacteria, and CFB. Other genes involved in adaptive proceed to sulfide as typically occurs in other aquatic
responses included the alternative sigma factor B, which systems, and instead, sulfate is expected to be regenerated
was linked to Cyanobacteria and CFB, while carbon via an alternative cycle with Fe(III) acting as the terminal
starvation response genes were present in Planctomyce- electron acceptor (Mikucki et al., 2009). This is a fasci-
tes, Beta- and Gammaproteobacteria, and other bacteria. nating example of how a closed system has adapted to
The ability to link taxonomic identities to specific func- sustainlife in the absence of light energy through the useof
tions that are important to individual and communal atypical chemical cycling, a pathway that was speculated
adaptation will be valuable for monitoring mat communities to have possibly occurred in the ancient Neoproterozoic
and forecasting how they may respond to ecosystem ocean (1000–500 mya) (Mikucki et al., 2009).
change. A whole systems level approach was employed to piece
The impact of a changing physico-chemical environ- together ecosystem functioning of a moderately complex
ment on microbial communities can be significant, and lake system (Ng et al., 2010; Lauro et al., 2011). Ace Lake
this was effectively described by a study of 13 ponds is a marine-derived meromictic saline lake in the Vestfold
formed after an original larger pond (6712 m2, 10 m Hillsthatwasisolated fromtheocean ~ 5000 ya.Utilizing
ª2012FederationofEuropeanMicrobiologicalSocieties FEMSMicrobiolRev&&(2012)1–33
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