Biodata of S.M. Singh and J. Elster, authors of the chapter “Cyanobacteria inAntarctic Lake Environments: A Mini-review”

Dr. S.M. Singh is currently Scientist-C of the National Centre for Antarctic& Ocean Research, Ministry of Ocean Development, Government of India. Heobtained his Ph.D. from the Lucknow University, India in 1998. Dr. Singh’s sci-entific interests are in the areas of evolutionary biology, polar ecology, andbiotechnology.

E-mail: drsmsingh@yahoo.com

Dr. J. Elster is currently the Head of the Phycology Centre of the BotanyInstitute, Academy of Sciences of the Czech Republic in Trenon, Czech Republic.He is also Associate Professor of the University of South Bohemia in CeskeBudejovice and the Masaryk University in Brno, Czech Republic. He obtainedhis Ph.D. from the Czechoslovak Academy of Sciences in 1992. Dr. Elster’s sci-entific interests are in the areas of biology, ecology, and ecophysiology ofcyanobacteria and algae in extreme environments with polar habitat preferences.

E-mail: jelster@butbn.cas.cz

J. Seckbach (ed.), Algae and Cyanobacteria in Extreme Environments, 303–320.© 2007 Springer.

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CYANOBACTERIA IN ANTARCTIC LAKE ENVIRONMENTS:A Mini-review

SHIV M. SINGH1 AND JOSEF ELSTER2

1National Centre for Antarctic and Ocean Research, HeadlandSada, Vasco-Da-Gama, Goa-403804, India. 2Institute of Botany,Academy of Sciences of the Czech Republic, Trebon and Facultyof Biological Sciences, University of South Bohemia,Ceske Budejovice, Czech Republic

1. Introduction

The Antarctic habitats are some of the driest and coldest ecosystems on theEarth. Earlier there was a general acceptance that polar deserts harbored little life(Priscu, 1999). But, recent studies have revealed the existence of microbes in: thesnow near the South Pole (Carpenter et al., 2000), the 3.5 km deep in Vostok ice(Karl et al., 1999; Priscu et al., 1999a), exposed soils (Wall and Virginia, 1998),sandstones (Friedmann et al., 1993), meltwater ponds (Vincent, 1988), liquidwater column of permanently ice-covered lakes (Priscu et al., 1999b), and the icecovers of permanent lake ice (Priscu et al., 1998; Psenner et al., 1999). Most ofthe microbes found in these habitats are prokaryotic (Vincent, 1988; Gordonet al., 2000; Brambilla et al., 2001). Among these microbes, one of the mostimportant components is the photosynthetically active cyanobacteria. They pro-vide for an adequate quantity of fixed carbon via photosynthesis to drive awell-developed ecosystem (Vincent, 1988). On the contrary, in those habitatswhere there is a lack of cyanobacteria, biomass production by the addition ofnew carbon and nitrogen is slowed. Thus, such habitats are poor in biodiversityand also poor in trophic levels. In Antarctic habitats the cyanobacteria areadapted and acclimated to their environment in terms of temperature, freeze/thawsurvival photoprotection, as well as light acquisition for photosynthesis (Vincentet al., 1993a, b, c; Tang et al., 1997; Nadeau et al., 1999; Tang and Vincent, 1999;Nadeau and Castenholz, 2000). Though cyanobacteria play a significant role inecosystem dynamics, only a few of them have been considered true psychrophiles(Tang et al., 1997; Fritsen and Priscu, 1998). They are classified as psychrotoler-ant or psychrotrophic due to their ability to metabolize near 0ºC and also becausetheir temperature optima for growth are typically above 15ºC. Some of thecyanobacterial groups, for example, Leptolyngbya, Phormidium, Oscillatoria, andNostoc are cosmopolitan and occur in highly divergent environmental extremes.

The distribution of microbes in Antarctic habitats can be recorded by theanalysis of particulate organic carbon (POC) and DNA sequence distribution(Burkins et al., 2000; Fritsen et al., 2000; Gordon et al., 2000; Brambilla et al.,

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2001; Burkins et al., 2001). The cyanobacterial mats of streams, lakes, and pondsare the primary sources of organic carbon, and support the contemporary soilmetabolism (Vincent et al., 1993c; Moorhead and Priscu, 1998; Lyons et al., 2000;Burkins et al., 2001; Elster and Komárek, 2003). DNA hybridization studiesbetween cyanobacteria and other prokaryotes have revealed that cyanobacterialmats in ephemeral streams provide the biological seed for the lake cyanobacteria(Gordon et al., 1996; Priscu et al., 1998; Gordon et al., 2000). It is clear that lakesand streams colonized by cyanobacteria are inoculum for the life-support systemof the Antarctic polar deserts. They provide organic carbon to this extremely dryecosystem and seed it with numerous microbe spores.

With these points in mind, the following polar habitat classification has beenproposed (Elster, 2002). This classification was established on the bases of thewater gradient, which reflects local climate; the presence or absence of water,directly or indirectly, determining the properties of the Antarctic ecosystem; andas well as on the basis of age, which determines the stage of development of thecyanobacteria and, subsequently, of ecosystem development.

Three categories, of Antarctic habitat types, which differ from each other,have been proposed – lacustrine (lake), hydroterrestrial (wetland), and terrestrial(Elster, 2002). The lacustrine (lake) environment is stable with respect to time andhas a special limnological character, although the cyanobacterial benthic com-munities of lakes do overlap, in many cases, with the hydroterrestrial. A commondistinction between hydroterrestrial (wetland) and lacustrine (lake) habitats in theAntarctic ecosystem is that wetlands freeze solid during winter, whereas mostlakes do not (Hawes et al., 1992). In hydroterrestrial environments (wetlands),liquid water is available for almost the entire period of the decisive heat-giving(summer) light. In terrestrial environments, water is available in liquid form foronly a short period (e.g., snow melt, summer rain or snow fall), or is only avail-able as air humidity (vapor absorbed directly from the air).

Of course, the most of above introduced information can be applied also forthe Arctic ecosystem (e.g., Vincent et al., 2000; Elster, 2002; etc.).

2. Antarctic Lake Cyanobacterial Ecology

Several studies on cyanobacterial habitats have been conducted on ice-freeexpanses of land in the Antarctic, some examples include: Queen Maud Land(Kashyap et al., 1998), Signy Island (Broady, 1977a, b, c), Campbell Island(Broady, 1982; Ohtani, 1986), and the McMurdo Dry Valleys (Taylor, 1916;Wilson, 1965). Lake ecosystems contain two separate algal communities: phyto-plankton in the water column and the phytobenthos attached to the bottom strata.The responses to environmental variation have the potential to differ greatlybetween the plankton and benthos (Vinebrooke and Leavitt, 1999). Althoughnutrients may severely limit planktonic production, benthic phototrophs may besubject to quantitatively or even qualitatively different controls. Many Antarctic

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lakes contain luxuriant benthic mosses (Sand-Jensen et al., 1999). In addition,cyanobacterial mats may achieve high standing stocks and often dominate overallecosystem productivity (Hawes and Schwarz, 1999; Vincent, 2000a; Hodgsonet al., 2004). A considerable amount of research has been conducted on benthicmats within the lakes (Wharton et al., 1983; Parker and Wharton, 1985; Simmonset al., 1993). The benthic mats and crusts are up to several centimeters thick, andmay completely cover the bottom substrate (Howard-Williams et al., 1986; Daveyand Clarke, 1991; Vincent et al., 1993b). There is diversity in the benthic mat com-position, for example, some mat types are largely products of single cyanobacterialspecies, whereas others are composed of complex microbial communities, withseveral dominant cyanobacteria. Several studies on benthic mats and crusts (mod-ern-day stromatolites) of deep continental Antarctic lakes have been carried out(Parker et al., 1981; Wharton et al., 1983; Parker and Wharton, 1985). Benthicmats are cohesive, skin like, mucilaginous films, flocculi of various colors, and aremainly composed of Phormidium and Nostoc, together with soft Leptolyngbya tri-chomes. Pinckney and Paerl (1996) observed that the most abundantphytopigments of Antarctic lakes were myxoxanthophyll, echinenone, zeaxanthin,and canthaxanthin. They further found that these are all markers for cyanobacte-ria. The species of cyanobacteria, which inhabit the melt ponds and ephemeralstreams, witness and experience several environmental stresses (e.g., high radiationand freeze/thaw cycles), whereas the benthic species of lakes receive lower radia-tion and growth in constant liquid water. Nutrient uptake studies on periphyton ofsome Antarctic systems have indicated that nitrogen and phosphorus may be reg-ulating factor for certain benthic communities (Miller et al., 1992; Vincent et al.,1993b). Except for this, Bonilla et al. (2005) also showed that microbial mat habitatalso allows growth under nutrient-rich conditions despite low nutrients in theoverlying water.

In addition to nutrient constraints, cyanobacterial communities of the polarregions are subject to large variations in light availability, from total winter dark-ness to continuous light in summer, coupled with long periods of freezing and ashort-growing season. During summer ice-out conditions, the phytoplankton andbenthic mats can be abruptly exposed to high levels of PAR and UV radiation(Roos and Vincent, 1998). The communities therefore require a broad set of pig-ment strategies embracing both light harvesting and light protection. In thisconnection, Bonilla et al. (2005) described the pigment characteristics of pho-totrophic communities and determined the array of light- harvesting andlight-screening pigments that allows growth and survival under the low tempera-ture continuous light regime of summers in the extreme polar environment.

The analyses of lake sediment layers showed that viable phototrophs andheterotrophs could occur in deep sediment layers and can become active whenliquid water is available (Priscu, 1997; Priscu et al., 1998). For example, the pres-ence of metabolically active microbial communities has been recorded insediments 2 m below the ice cover in Lake Bonney (Wing and Priscu, 1993). POC,chlorophyll-a, primary productivity, bacterial density, and bacterial activity were

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found to be associated with the depth of lake sediment. The cyanobacteria, by theprocess of photosynthetic inorganic carbon fixation, release extracellular photo-synthate in the form of dissolved organic carbon (DOC) and ammonium. Thissupply of DOC is being utilized as a source of energy and carbon for growth byheterotrophic components of the microbial assemblage. The heterotrophic organ-ism recycles CO2, and in turn supports the photosynthesis in the cyanobacteria.Those lake sediment layers rich in ammonium concentration serve in the activeregeneration of nitrogen. The adsorptive processes between soluble reactive phos-phorus (SRP) and the inorganic sediment materials have been demonstrated(Fritsen and Priscu, 1998; Priscu et al., 1998). The ratio of POC to particulateorganic nitrogen (PON) for the combined data from all studied ice-covered lakesin the Antarctic region averages 8.9 (g:g), which is higher than the ratio of 5.7(g:g) that occurs during the balanced growth of photoautotrophs (Redfield,1958). Besides this, the elevated levels of chlorophyll-a, POC, PON, ammonium,and DOC (Wing and Priscu, 1993) have also been observed in lake ice, and thesefindings have led to the hypothesis that the cyanobacteria occur within the icecover. Their occurrences in the lake ice were not passive, as they grew actively.Subsequent research has shown that there was adequate liquid water present(Adams et al., 1998; Fritsen et al., 1998) to support an active prokaryotic ecosys-tem within the ice. This prokaryotic lake ice ecosystem consists of thecyanobacteria and a diversity of bacterial species (Pinckney and Paerl, 1996;Paerl and Priscu, 1998; Priscu et al., 1998; Gordon et al., 2000).

3. Cyanobacterial Adaptation to the Environment of Antarctic Lakes

Fritsen and Priscu (1998) have shown that despite the low photosynthetic rate ofAntarctic cyanobacterial mats, a large proportion of photosynthate is incorpo-rated into protein. This indicates that cyanobacteria have the efficient capacity fornet cellular growth. Incorporation of 14CO2 into polysaccharides, lipids, and lowmolecular weight metabolites averaged 39%, 4.1%, and 15.9%, respectively.However, cyanobacterial assemblages show variable biomass-specific rates ofphotosynthesis. Photosynthesis versus irradiance experiments have revealed thatphotosynthesis ranged from 0.0043 to 0.0406 µgC µg chlorophyll-a−1 h−1

(Pinckney and Paerl, 1996). It has been shown that 14CO2 incorporation into pro-tein can be used for the computation of carbon-specific growth rates. These rangefrom 0.001 to 0.012 µgC µg chlorophyll-a−1 h−1 (Pinckney and Paerl, 1996). Thiscalculation is in agreement with the pigment labeling results. Hawes and Schwarz(2001) observed the absorption and utilization of irradiance by cyanobacterialmats in Antarctic lakes with contrasting light climates. According to Fritsen et al.(1996), during the months of continuous sunlight, in situ irradiances are abovewhat is required to saturate the photosynthetic capacity of the cyanobacteria. Inaddition, they further suggested that, the in situ growth rate is not likely to belight-limited when liquid water is available. The light-saturated rate of photosyn-thesis, normalized to chlorophyll-a for the cyanobacterial assemblage in Lake

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Fryxell, increased approximately tenfold when the incubation temperature wasincreased from 2ºC to 20ºC. This corresponds to a Q10 value of 3.46. Fritsen andPriscu et al. (1996, 1998) introduced the idea that the temperature response oflight-saturated photosynthesis is near 20ºC, with about 10% of the maximum rateoccurring at in situ growth temperatures. These data support the results of Tanget al. (1997) and Tang and Vincent (1999) who contend that only a few truecyanobacterial psychrophiles are associated with polar freshwater systems. Thefirst Antarctic psychrophilic cyanobacteria were isolated and studied by Nadeauand Castenholz (2000, 2001) from a pond on the Ross Ice Shelf and Comte et al.(2007) from Antarctic peninsula. On the basis of their genetic analysis they con-cluded that psychrotolerant forms are more closely related to the cyanobacteriaof temperate habitats, whereas the true psychrophiles probably had evolved in thepolar habitat.

On the basis of above mentioned information, it can be expected that thecyanobacterial assemblages of Antarctic lakes are psychrophilic or psychrotoler-ant. However, Tang et al. (1997), Vincent et al. (1997), and Vincent (2000) havediscussed that the presence or absence of cyanobacteria in Antarctic lake assem-blages may also depend on other selection factors, apart from temperature (e.g.,freeze–thaw and desiccation tolerance, tolerances to high fluxes of solar radiation,etc.). It has been reported that a photosynthesis–irradiance relationship changes inresponse to freezing (Lizotte and Priscu, 1992). It was shown that the photosyn-thesis rate is at its maximum when the irradiance is greater than 600 µmol m−2 s−1.Moreover, the rate of cyanobacterial photosynthesis is equivalent to the respira-tion when irradiance is up to 202 µmol m−2 s−1 before freezing, and 308 µmol m−2 s−1

after freezing. During the Antarctic winter dark period the cyanobacterial O2 con-sumption is 33% lower than during the summer period. Measurements of O2consumption also showed that these values are higher before freezing, than afterfreezing. Thus, during the dark and after freezing the rate of respiration becomeslow. It has been noted (Tang et al., 1997; Vincent et al., 1997; Vincent, 2000a, b,Sabacká and Elster, 2006) that the polar freezing and thawing cycle does not haveany major adverse affect on the Antarctic cyanobacteria over long time-scales.Rather, it has been considered that freezing may be the environmental parameterthat allows the cyanobacteria to be the dominant photosynthetic microorganismsin the Antarctic terrestrial ecosystem, where low light (<200 µmol m−2 s−1) and/orcomplete darkness prevail. This adaptations to increase or decrease respirationwithin the conditions of the Antarctic environment help to protect from losses dueto reduced carbon consumption and to save energy in the ecosystem.

The nutrient bioassay experiments have demonstrated (Priscu et al., 2005)that the photosynthetic activities of cyanobacteria can be enhanced by the addi-tion of ammonium or nitrate as a source of inorganic nitrogen. Since there is anapparent inorganic nitrogen deficiency in Antarctic habitats (Priscu et al., 2005),cyanobacteria are thus a unique tool to fix atmospheric nitrogen. It has beenobserved that the activity of the nitrogen-fixing enzyme nitrogenase is stimulatedby addition of phosphorus and iron (Priscu et al., 2005). Moreover, the molecu-lar analyses have also been remarked (Paerl and Priscu, 1998) that cyanobacteria

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and bacteria in antarctic habitats can fix atmospheric nitrogen because of thestimulatory effect of nitrogenase by light. Paerl and Priscu (1998) suggested thatcyanobacteria are responsible for a majority of the phenotypic expressions of thisenzyme in nature.

The additional source of inorganic nutrients, to this cyanobacterial assem-blage, is the lake sediment. It has been observed that inorganic nutrients are boundto small soil particles and a considerable amount of them can be leached. It hasbeen shown that leaching of phosphorus is significant, mainly during spring melts.The idea that sediments under ice cover leach relatively small doses of phosphoruswas introduced by Priscu (Priscu et al., 2005). In addition, some measurements(Spigel and Priscu, 1998) demonstrated that there is often a deficiency of nitrogenin cyanobacterial assemblages. It has been shown (Priscu et al., 2005) that the aver-age amounts of ammonium and phosphorus that can be leached from lakesediment is 7.1 µgN g−1 and 4.1 µgP g−1, respectively. The ratio of leachable N:P is1.7, which is well below what is required for balanced cyanobacterial growth. Dueto the differential N and P leaching, the microorganisms have a selective advantageto fix atmospheric nitrogen. Though the apparent cyanobacterial nitrogen defi-ciency in Antarctic habitats has been reported (Priscu et al., 2005) assemblagesassociated with the sediment layer indicate that their growth is supported by nitro-gen contained in sediment. The isotope analysis of 15N-NH4 shown that the uptakeof ammonium is either equaled to or exceeded by microbial ammonium regenera-tion. It has been shown that the absolute rates of ammonium uptake andregeneration, relative to the PON pool, range from 0.7% d−1 to 22.0% d−1 and 0.1%d−1 to 22.1% d−1, respectively. The process of atmospheric nitrogen fixation appar-ently replenishes the ammonium pool faster than it is consumed. It has beenobserved that the lake bacterial (<63 µm) fraction is responsible for a majority ofthe ammonium regeneration. The half-saturation constant for ammonium isgenerally below the ammonium levels within the ice.

The concentration of dissolved inorganic carbon (DIC) has been recordedmore often in lake habitats with thick benthic cyanobacterial mat at the bottom(Priscu et al., 2005). This is because of the active cycling of both the organic andinorganic carbon pools. The 14CO2 release by radiolabeled cyanobacterial has shownpronounced mineralization of organic carbon. The cyanobacterial assemblagesdominated by mixed taxa (e.g., Nostoc and Phormidium) have a greater ability tomineralize organic carbon than do the individual taxa (e.g., Phormidium). It hasbeen reported that the turnover of POC in Antarctic lake assemblages ranged from17.5% d−1 in the Nostoc to 57.8% d−1 in the Phormidium mats (Priscu et al., 2005).

4. Antarctic Lake Cyanobacteria and Evolution

A hope for cyanobacterial applications in biotechnology and as tools to helpunderstand the early evolution of life has created interest within the researchcommunity. It is the general view that life on Earth evolved in hot environments

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(Pederson, 1997; Huber et al., 2000). But the recent views have suggestedalternatively that a “hot start” probably is not the only hypothesis for the originof life (Priscu et al., 2005). The thermal origin of life is based on single gene phy-logenetic relationships, that is, small subunit ribosomal RNA (16S rRNA)(Pennisi, 1998, 1999). There are strong arguments for biased construction of the“tree of life”being based on a single gene (Pennisi, 1998, 1999; Nelson et al.,1999). According to Pennisi (1998, 1999) a hierarchical universal classification isimpossible. At this level of controversy, Nelson et al. (1999) has suggested areassessment of the evolutionary pattern. Recently (Priscu et al., 2005) it has beenshown that a hot origin of life is not even supported by

1. Phylogenetic trees based on genes that do not code for ribosomal RNA2. Chemical experiments with alternative structure for the nucleic acid backbone

(Eschenmoser, 1999)3. Considerations about the thermal stability of basic molecules found in all

organisms and4. Statistical analysis of the Guanine-Cytosine content of DNA (Galtier et al.,

1999)

Balter (1999) has suggested that the adaptation to life in hot environments mayeven be a late adaptation. Thus there is an urgent need for intensive research todetermine whether life originated in hot or cold environments, or if evolutiontook place in parallel within both environmental types. It seems clear that coldenvironments have acted as a refuge for life during major glaciations. Hoffmanet al. (1998), Hoffman and Schrag (2000), and Schrag and Hoffman (2001) haveall suggested that during the Neoproterozoic (around 600 million years ago),early microbes endured an ice age of such intensity that even the tropic regionsfroze over. According to the “Snowball Earth Hypothesis,” the Earth was com-pletely covered by ice for 10 million years, or more. The ice thickness during thisperiod was more than 1 km, and only the deepest oceans would have containedliquid water. However, the Snowball Earth Hypothesis has been criticized(Williams et al., 1998) on the basis that such a thick ice cover over the world’soceans would have cut off the supply of sunlight to organisms in the seawater, andthereby eliminated photosynthesis, and all life associated with photosyntheticcarbon production. Williams et al. (1998) have postulated that global-scale freez-ing would extinguish all surface life. In addition, Koop et al. (2005) introducedthe potential role of cyanobacteria in process of atmospheric oxygen build-up,which have led to massive oxidation and loss of methane and consequently globalfreeze-up. They proposed a simple cyanobacterial growth model incorporatingthe range of C, Fe, and P fluxes expected during a partial glaciation in an anoxicworld with high Fe oceans content indicating that oxygenic photosynthesis couldhave destroyed a methane greenhouse and triggered a snowball event on time-scales as short as 1MY. Thus they concluded that cyanobacteria are directlyresponsible for methane green house collapse and planetary glaciation. Hoffman

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and Schrag (2000), Vincent et al. (2000), and Vincent and Howard-Williams(2001) also have suggested that photosynthetic cyanobacteria and bacteria, simi-lar to those found in the permanent ice-covered lakes, may have acted as an icybiotic refuge during these extreme cold events.

The presence of microbial populations in the polar environment suggests thatthere are intense chemical and biological interactions between species. According toVincent et al. (2000) there were interactions between species for the development ofsymbiotic associations, which eventually developed a eukaryote during the course ofevolution. Subsequently (Vincent et al., 2004) in more detail analyses have postulatedthat the polar freshwater microbial mats can be considered as ideal environments forevolutionary process. The microbial mats consortia consist of highly concentratedpopulations from diverse functional groups, which are in close contact with eachother. The physical and chemical interactions can be strong in such communities andcould lead to mutualism, symbiosis, even eukaryogenesis. These organisms also thriveprolonged freeze-up and dormancy, and offer insights into how complex life mayhave persisted and evolved, even during the glacial upheavals of the Precambrian.

On the basis of thermal microbial mat communities, Margulis and Sagan(1997) suggested a “density-speeds-evolution” theory. It seems that ice habitatsalso provided opportunities for microbial evolution, inducing the radiation of theeukaryotic cell type at the onset of the Neoproterozoic (Knoll, 1994; Hoffmanand Schrag, 2000). The molecular responses of cyanobacterial cells to low tem-perature of Antarctica’s stressful environment can be divided into two steps:

1. The cold-induced desaturation of fatty acids in membrane lipids, which flu-idizes membranes to compensate for decreases in membrane fluidity at lowtemperatures (Murata and Los, 1997; Wall and Virginia, 1998) and

2. The cold-induced synthesis of certain enzymes that are involved in transcrip-tion and translation. Such enzymes compensate for the decrease in theefficiency of transcription and translation at low temperatures (Friedmannet al., 1993; Sato, 1995).

The growth and biological activity of Antarctic taxa depend on the temperatureprofile. For example, cyanobacteria in the water pockets of Antarctic lake ice,where temperatures are always below 0ºC, are metabolically active and retain thecapacity for oxygenic photosynthesis (Paerl and Priscu, 1998). It has beenobserved that cyanobacteria metabolize even at −20ºC in the Antarctic (Psennerand Sattler, 1998). This adaptation has been examined in Anabaena variabilis,Synechocystis, Synechococcus (Priscu et al., 1999a), and thermophilic speciesSynechococcus vulcanus (Priscu et al., 1998). The analysis of gene transcript dur-ing the downward shift in temperature revealed that the increase in desaturationoccurs due to stimulation of expression of those genes appropriate for the desat-urases (Psenner et al., 1999; Gordon et al., 2000; Brambilla et al., 2001). Theimpact of the cold induces the expression of several genes for ribosomal proteins(Nadeau et al., 1999; Vincent, 2000). It has also been observed that caseinolytic

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proteases act as cold-shock chaperones and proteases (Nadeau and Castenholz,2000). The fluidity of membrane lipids depend upon the extent of unsaturation ofmembrane lipids (Tang and Vincent, 1999). There is feedback between membranefluidity and the expression of genes for the desaturases. This suggested the pres-ence, in the cyanobacterial cytoplasmic membrane, of a temperature sensor thatperceives a change in the physical motion of membrane lipids and transmits thesignal to a mediator that then activates the expression of genes for the desaturases(Wall and Virginia, 1998; Karl et al., 1999). For cold temperature regulation thereis a cold-sensing histidine kinase system in cyanobacteria. This histidine kinasemight be able to regulate all the gene expression responses to low temperatureshock. Recently, the studies on a mutant form of Hik33 noted that not all cold-inducible genes are controlled by this histidine kinase (Nadeau et al., 1999). Thus,it seems that some other cold sensors exist that might control gene expression bysome unknown mechanism (Nadeau et al., 1999; Tang and Vincent, 1999).

Roos and Vincent (1998) also observed the temperature dependence ofultraviolet radiation (UVR) effects on pigment composition, growth rate, andphotosynthetic characteristics in mat forming Antarctic cyanobacterium. Theirresult implies that phototrophic organisms living in cold environments may beespecially prone to the damaging effects of UVR. However, offset against this evi-dence of toxic UVR effects was the observation that Phormidium murrayigradually increases its growth rate under UVR, indicating an ability to build uptolerance against this environmental stress. This acclimation could proceed by avariety of mechanisms, including increased efficiency of damage repair. Thespeed of these acclimation processes will depend on biosynthetic rates and thus,like the direct effects of temperature on the damage–repair balance, will also beaffected by temperature.

In addition to the above mentioned changes, which occur in cells under lowtemperature conditions, Antarctic cyanobacteria have a wide range of adapta-tion/acclimation strategies which help them to overcome extremes related to theperiodic desiccation and freezing/thawing events. The main coping strategies forliving in an Antarctic habitat are avoidance and protection.

1. Avoidance – Antarctic cyanobacterial communities have a diverse range ofboth ecological and physiological life strategies and behaviors to avoid lowtemperatures and fluctuations in water status (Elster and Benson, 2004).Cyanobacteria are poikilohydric organisms that are able to tolerate desiccationto differing extents. The external environment directly manages the metabolicactivity of poikilohydric cyanobacteria by affecting the presence or absence ofwater. The poikilohydric organisms have a great ecological advantage in thesevere Antarctic environment. Shelter strategies present another type of avoid-ance mechanism against the low temperatures and water status fluctuations.These strategies, which are mainly important in lakes because of their physi-cally stable environment, protect against stress factors caused by dynamictemperature and water-gradients. The poikilohydricity and shelter strategies

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are intercalated, and when they are combined with cellular and physiologicalmodifications such as: cell motility; development of complex life cycles; multi-layered cell wall, sheet, and mucilage production, they afford greateradvantages. Elster and Benson (2004) suggested that these avoidance regimeshave thus been developed because of considerable evolutionary pressures. Themobility of cyanobacteria facilitates avoidance of the most stressful condi-tions, and propels the organism to a more favorable environment (Castenholzet al., 1991; Spauldin et al., 1994; Wiedner and Nixdorf, 1998). The filamen-tous cyanobacteria move using straight-line gliding (Castenholz, 1982, etc.). Acomplex life cycle is also a major avoidance strategy and this usually involvesthe development of resting (dormant), vegetative, and reproductive stages thatchange during an organism’s life cycle to accommodate the seasonally incurredenvironmental fluctuations. The dormant stages of cyanobacteria facilitatetheir transportation around the world and across the Polar Regions. This hasimplications in terms of influencing global microbial geneflow and distribu-tion of genomes across long distances (Elster and Benson, 2004). The dormantstages accumulate high concentrations of soluble carbohydrates which substi-tute for water molecules during dehydration. This stabilizes the structure andfunctions of macromolecules, membranes, and cellular organization (Croweet al., 1984). The presence of protective sugars in cells enables the vitrificationof the cytoplasm upon drying, and supports the formation of a high-viscosity,metastable glassy state (Bruni and Leopold, 1991). This, in turn, preserves cellviability during dry frozen storage by immobilizing cellular constituents andsuppressing deleterious chemical or biological reactions that threaten survival(Sun and Leopold, 1994a, b).

2. Protection strategies – the extracellular production of protective compoundsand structures such as multilayered cell walls, sheets, and mucilage is a verycommon phenomenon in polar cyanobacteria, and it protects them againstfluctuations in water status (Elster and Benson, 2004). The sheaths, which sur-round the cells, are rich in carbohydrates and other amino acids. These sheathsattract other bacteria and harbor them inside, for mutual benefit. Thicksheaths have the capability to protect against ice crystal formation, so that dur-ing the prolonged cold and icy winter period the cell walls of thecyanobacterial species are not ruptured, and life hibernates during theseadverse conditions.

The phylogenetic diversity of Antarctic cyanobacteria can be characterized by theanalyses of 16S rRNA genes amplified from environmental DNA (Gordon et al.,1996, 2000). Gordon et al. (1996, 2000) have analyzed the cyanobacteria and bac-teria colonizing sediment particles at the depth of 2.5 m in the permanent icecover of Lake Bonney. The DNA sequencing of 198 clones and oligonucleotideprobe hybridization techniques allowed the introduction of a rRNA gene clonelibrary, which represented the cyanobacteria and other microbial components(proteobacteria, planctomycetales, acidobacterium, green non-sulfur bacteria,and actinobacteria (Gordon et al., 1996, 2000). The cyanobacterial gene clusters

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closely resemble (>97% similarity) those of well-characterized cyanobacterialspecies, Chamaesiphon subglobosus (Priscu et al., 2005). The remaining cyanobac-terial gene clusters resemble (less than a 93% similarity) those of Leptolyngbya sp.and Phormidium sp. The oligonucleotide probes have been made from lake icecyanobacterial clusters, and have also been used to screen environmental 16SrDNA samples obtained from the terrestrial (soil and stream) environment(Gordon et al., 1996, 2000). It has been observed that the probes designed tohybridize to cyanobacterial 16S rRNA genes indicate that these sequences pres-ent in the lake ice are also found in terrestrial cyanobacterial mat samples. TheDNA sequence analysis and physiological data of Antarctic habitats thus indi-cates that the cyanobacterial (and bacterial) communities dominant in lakes arealso common to the terrestrial ecosystem (Gordon et al., 1996, 2000). Priscu et al.(1998) and Gordon et al. (2000) have suggested that the katabatic winds dispersemicroorganisms in the desert environment and provide the biological seeds for thelake ice microbial assemblages. Olson et al. (1998) have observed that the molec-ular characterization of the nifH gene of nitrogenase in lake ice alsodemonstrated the presence of a diverse diazotrophic assemblage. The nifH analy-sis further showed that phototrophic cyanobacteria and heterotrophicmicroorganisms have the potential to fix atmospheric nitrogen. Grue et al. (1996),Olson et al. (1998), and Paerl and Priscu (1998).

5. Conclusions

This chapter was written with two aims in mind:

1. To summarize our present knowledge concerning Antarctic lake cyanobacter-ial ecology, physiology, and molecular biology. Cyanobacteria are well adaptedand acclimated to the Antarctic lake environment in terms of temperature,freeze/thaw survival, photoprotection, and light acquisition for photosynthe-sis. They are the major contributors of biomass to the Antarctic lakeecosystem. It is our estimation that they comprise about 80% of algal flora ofthe Antarctic lake ecosystem. In addition, several the most abundantcyanobacterial groups Chroococcales, Oscillatoriales, and Nostocales are eco-logically important in the Antarctic lake ecosystem because something close to50% (in our personal estimation) of their species are able to fix N2.

2. To compile the background knowledge for an Indian–Czech research projectfocused on Antarctic cyanobacterial lake diversity and ecology.

6. Acknowledgments

We are highly indebted to Dr. P.S. Goel, Secretary, Ministry of OceanDevelopment, Government of India and NCAOR Director Dr. Rasik Ravindrafor all the facilities extended. In addition, the second author was supported by the

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Grant Agency of the Academy of Sciences of the Czech Republic (Grant #A600050515). We also highly appreciate all comments and suggestions on thepaper given by Prof. Warwick F. Vincent.

7. References

Adams, E.E., Priscu, J.C., Fritsen, C.H., Smith, S.R. and Brackman, S.L. (1998) Permanent ice cov-ers of the McMurdo Dry Valley Lakes, Antarctica: bubble formation and metamorphism. In:J.C. Priscu (ed.) Ecosystem Dynamics in a Polar Desert: The McMurdo Dry Valleys, Antarctica.Antarctic Research Series, American Geophysical Union, 72, 281–296.

Balter, M. (1999) Did life begin in hot water? Science 280, 31.Bonilla, S., Villeneuve, V. and Vincent W.F. (2005) Benthic and planktonic algal communities in a high

arctic lake: pigment structure and contrasting responses to nutrient enrichment, J. Phycol. 41,1120–1130.

Brambilla, E., Hippe, H., Hagelstein, A., Tindall, B.J. and Stackbrandt, E. (2001) 16S rDNA diver-sity of cultured and uncultured prokaryotes of a mat sample from Lake Fryxell, McMurdo DryValleys, Antarctica, Extremophiles 5, 23–33.

Broady, P.A. (1977a) The Signy Island terrestrial reference sites VII The ecology of the algae site 2, amoss carpet, Br. Antarct. Surv. Bull. 45, 47–62.

Broady, P.A. (1977b) The Signy Island terrestrial reference sites IX. The ecology of the algae site 2, amoss carpet, Br. Antarc. Surv. Bull. 47, 13–29.

Broady, P.A. (1977c) A preliminary survey of the essential algae of the Antarctic Peninsula and SouthGeorgia, Br. Antarct. Surv. Bull. 48, 47–70.

Broady, P.A. (1982) Taxonomy and ecology of algae in a freshwater stream in Taylor Valley, VictoriaLand, Antarctica, Arch. Hydrobiol. 32, 331–349.

Bruni, F. and Leopold, A.C. (1991) Glassy state in soybean seeds: relevance to anhydrous biology,Plant Physiol. 96, 660–663.

Burkins, M.B., Virginia, R.A. Chamberlain, C.P. and Wall, D.H. (2000) Origin and distribution of soilorganic matter in Taylor Valley, Antarctica, Ecology 81, 2377–2391.

Burkins, M.B., Virginia, R.A. and Wall, D.H. (2001) Organic carbon cycling in Taylor Valley,Antarctica: quantifying soil reservoirs and soil respiration, Glob. Change Biol. 7, 113–125.

Carpenter, E.J., Lin, S. and Capone, D.G. (2000) Bacterial Activity in South Pole snow, Appl. Environ.Microbiol. 66, 4514–4517.

Castenholz, R.W. (1982) Motility and taxes. In: N.B. Carr and B.A. Witton (eds.) The Biology ofCyanobacteria, Botanical Monographs, Vol. 19, Blackwell Scientific Publishers, Oxford, pp. 9–45.

Castenholz, R.W., Jorgensen, B.B., D`Amelio, E. and Bauld, J. (1991) Photosynthetic and behavioralversatility of the cyanobacterium Oscillatoria boryana in a sulfide-rich microbial mat, FEMSMicrobiol. Ecol. 86, 43–58.

Comte, K., Sabacká, M., Cadel, S., Elster, J. and Komárek, J. (2007) Relationship of selectedOscillatorian cyanobacteria isolates from the Arctic and the Antarctic. FEMS Microbiol. Ecol.59 (2), 366–376.

Crowe, J.H., Crowe, L.M. and Chapman, D. (1984) Preservation of membranes in anhydrobioticorganisms: the role of trehalose, Science 223, 701–703.

Davey, M.C. and Clarke, K.J. (1991) The spatial distribution of microalgae on Antarctic fellfield soils,Antarct. Sci. 3, 257–263.

Elster, J. (2002) Ecological classification of terrestrial algae communities of polar environment. In:L. Beyer and M. Bolter (eds.) GeoEcology of Antarctic Ice-Free Coastal Landscapes, EcologicalStudies, Vol. 154, Springer, Berlin, pp. 303–326.

Elster, J. and Komárek, O. (2003) Periphyton ecology of two snow-fed streams in the vicinity ofH. Arctowski station, King George Island, South Shetlands, Antarctica, Antarct. Sci. 15 (2),189–201.

316 SHIV M. SINGH AND JOSEF ELSTER

Seckbach_Ch15.qxd 17/8/07 12:29 PM Page 316

Elster, J. and Benson, E.E. (2004) Life in the Polar terrestrial environment with a focus on algae andcyanobacteria. In: B.J. Fuller, N. Lane and E.E. Benson (eds.) Life in Frozen State, CRC Press,London, pp. 111–150.

Eschenmoser, A. (1999) Chemical etiology of nucleic acid structure, Science 284, 2118–2124.Friedmann, E.I., Kappen, L., Meyer, M.A. and Nienow, J.A. (1993) Long-term productivity in the

cryptoendolithic microbial community of the Ross Desert, Antarctica, Microb. Ecol. 25, 51–69.Fritsen, C.H. and Priscu, J.C. (1998) Cyanobacterial assemblages in permanent ice covers of Antarctic

lakes: distribution, growth rate, and temperature response of photosynthesis, J. Phycol. 34, 587–597.Fritsen, C.H., Christian, H. and Priscu, J.C. (1996) Photosynthetic characteristics of cyanobacteria in

permanent ice-covers on lakes in the McMurdo Dry Valleys, Antarctica, Antarct. J. US 31,216–218.

Fritsen, C.H., Adams, E.E., McKay, C.M. and Priscu, J.C. (1998) Permanent ice covers of theMcMurdo Dry Valley Lakes, Antarctica: liquid water content. In: J.C. Priscu (ed.) EcosystemDynamics in a Polar Desert: The McMurdo Dry Valleys, Antarctica. Antarctic Research Series,American Geophysical Union, 72, 269–280.

Fritsen, C.H., Grue, A. and Priscu, J.C. (2000) Distribution of organic carbon and nitrogen in surfacesoils in the McMurdo Dry Valleys, Antarctica, Polar Biol. 23, 121–128.

Galtier, N., Tourasse, N. and Gouy, M. (1999) A non-hyperthermophilic common ancestor to extantlife forms, Science 283, 220–222.

Gordon, D.A., Lanoil, B., Giovannoni, S. and Priscu, J.C. (1996) Cyanobacterial communities asso-ciated with mineral particles in Antarctic lake ice, Antarct. J. US 31, 224–225.

Gordon, D.A., Priscu, J.C. and Giovannoni, S. (2000) Distribution and phylogeny of bacterial com-munities associated with mineral particles in Antarctic lake ice, Microb. Ecol. 39, 197–202.

Grue, A.M., Fritsen, C.H. and Priscu, J.C. (1996) Nitrogen fixation within permanent ice covers onlakes in the McMurdo Dry Valleys, Antarctica, Antarct. J. US 32, 218–220.

Hawes, I. and Schwarz, A.M. (1999) Photosynthesis in an extreme shade environment: benthic micro-bial mats from Lake Hoare, a permanently ice-covered Antarctic lake, J. Phycol. 35, 448–459.

Hawes, I. and Schwarz, A.M. (2001) Absorption and utilization of irradiance by cyanobacterial matsin two ice-covered Antarctic lakes with contrasting light climates, J. Phycol. 37, 5–15.

Hawes, I., Howard-Williams, C. and Vincent, W.F. (1992) Desiccation and recovery of Antarcticcyanobacterial mats, Polar Biol. 12, 587–594.

Hodgson, D.A., Vyverman, W., Verleyen, E., Sabbe, K., Leavitt, P.R., Taton, A., Squier, A.H. andKeely, B.J. (2004) Environmental factors influencing the pigment composition of in situ benthicmicrobial communities in east Antarctic lakes, Aquat. Microb. Ecol. 37, 247–263.

Hoffman, P.F. and Schrag, D.P. (2000) Snowball Earth, Sci. Am. 282, 68–75.Hoffman, P.F., Kaufman, A.J. Halverson, G.P. and Schrag, D.P. (1998) A neo-proterozoic Snowball

Earth, Science 281, 1342–1346.Howard-Williams, C., Vincent, L., Brody, P.A. and Vincent, W.F. (1986) Antarctic stream ecosystems:

variability in environmental properties and algal community structure, Int. Rev. GesamptenHydrobiol. 71, 511–544.

Huber, R., Huber, H. and Stetter, K.O. (2000) Towards the ecology of hyperthermophiles: biotopes,new isolation strategies and novel metabolic properties, FEMS Microbiol. Rev. 24, 615–623.

Karl, D.M., Bird, D.F., Bjorkman, K., Houlihan, T., Shackelford, R. and Tupas L. (1999)Microorganisms in the Accreted Ice of Lake Vostok, Antarctica, Science 286, 2144–2147.

Kashyap, A.K., Gupta, R.K. and Pandey, K.D. (1998) Check-list of cyanobacteria occurring inSchirmacher Oasis, Antarctica, J. Sci. Res., BHU, Varanasi 47, 171–179.

Knoll, A.H. (1994) Proterozoic and early Cambrian protists: evidence for accelerating evolutionarytempo, Proc. Natl. Acad. Sci. U.S.A. 91, 6743–6750.

Koop, R.E., Kirschvink, J.L., Hilburn, I.A. and Nash, C.Z. (2005) The Paleoproterozoic SnowballEarth: a climatic disaster triggered by the evolution of oxygenic photosynthesis, Proc. Natl.Acad. Sci. U.S.A. 102 (32), 11131–11136.

Lyons, W.B., Fountain, A., Doran, P., Priscu, J.C. and Neumann, K. (2000) The importance of land-scape position and legacy: the evolution of the Taylor valley Lake District, Antarctica, Freshw.Biol. 43, 355–367.

CYANOBACTERIA IN ANTARCTIC LAKE ENVIRONMENTS 317

Seckbach_Ch15.qxd 17/8/07 12:29 PM Page 317

Lizotte, M.P. and Priscu, J.C. (1992) Spectral irradiance and bio-optical properties in perenniallyice covered lakes of the dry valleys (McMurdo Sound, Antarctica), Antarct. Res. Ser. 57,1–14.

Margulis, L. and Sagan, D. (1997) Micro-cosmos: Four Billion Years of Microbial Evolution.University of California Press, Berkeley, 304 p.

Miller, M.C., DeOliveira, P. and Gibeau, G.G. (1992) Epilithic diatom community response to yearsof PO4 fertilisation: Kuparuk River, Alaska (68 N Lat.), Hydrobiologia 240, 103–119.

Moorhead, D.L. and J.C. Priscu (1998) Linkages among ecosystem components within theMcMurdo Dry valleys: A synthesis. In: J.C. Priscu (ed.) Ecosystem Dynamics in a Polar Desert:TheMcMurdo Dry Valleys. Antarctic Research Series, American Geophysical Union, 72,351–364.

Murata, N. and Los, D.A. (1997) Membrane fluidity and temperature perception, Plant Physiol. 115,875–879.

Nadeau, T. and Castenholz, R.W. (2000) Characterization of psychrophilic oscillatorians (cyanobac-teria) from Antarctic meltwater ponds, J. Phycol. 36, 914–923.

Nadeau, T. and Castenholz, R.W. (2001) Evolutionary relationships of cultivated Antarctic oscillato-rians (cyanobacteria), J. Phycol. 37, 650–654.

Nadeau, T., Howard-Williams, C. and Castenholz, R.W. (1999) Effects of solar UV and visible irra-diance on photosynthesis and vertical migration of Oscillatoria sp. (cyanobacteria) in anAntarctic microbial mat, Aquat. Microb. Ecol. 20, 231–243.

Nelson, K.E., Clayton, R.A., Gill, S.R., Gwinn, M.L., Dodson, R.J., Haft, D.H., Hickey, E.K.,Peterson, J.D., Nelson, W.C., Ketchum, K.A., McDonald, L., Utterback, T.R., Malek, J.A.,Linher, K.D., Garrett, M.M., Stewart, A.M., Cotton, M.D., Pratt, M.S., Phillips, C.A.,Richardson, D., Heidelberg, J., Sutton, G.G., Fleischmann, R.D., Eisen, J.A., White, O.,Saltzberg, S.L., Smith, H.O., Venter, J.C. and Fraser, C.M. (1999) Evidence for lateral genetransfer between Archaea and Bacteria from genome sequence of Thermotoga maritime, Nature399, 323–328.

Olson, J.B., Steppe, T.F., Litaker, R.W. and Paerl, H.W. (1998) N2-Fixing microbial consortia associ-ated with the Ice Cover of Lake Bonney, Antarctica, Microb. Ecol. 36, 231–238.

Ohtani, S. (1986) Epiphytic algae on moss in vicinity of Syowa station, Antarctica, Mem. Natl. Inst.Polar Res. Special. Issue 44, 2009–2219.

Paerl, H.W. and Priscu, J.C. (1998) Microbial phototrophic, heterotrophic and diazotrophic activitiesassociated with aggregates in the permanent ice cover of Lake Bonney, Antarctica, Microb. Ecol.36, 221–230.

Parker, B.C. and Wharton, R.A. (1985) Physiological ecology of blue-green algal Mats (modern stro-matolites) in Antarctic oasis lakes, Arch. Hydrobiol. Suppl. 71, 331–348.

Parker, B.C., Simmons, G.M. Jr., Seaburg, K.G., Cathey, D.D. and Allnutt, F.C.T. (1981) Modernstromatolites in Antarctic Dry Valley lakes, Bioscience 31, 656–661.

Pederson, K. (1997) Microbial life in deep granitic rock, FEMS Microbiol. Rev. 20, 399–414.Pennisi, E. (1998) Genome data shake tree of life, Science 280, 672–674.Pennisi, E. (1999) Is it time to uproot the tree of life? Science 284, 1305–1307.Pinckney, J.L. and Paerl, H.W. (1996) Lake ice algal phototroph community composition and growth

rates, Lake Bonney, Dry Valley Lakes, Antarctica, Antarct. J. US 31, 215–216.Priscu, J.C. (1997) The biogeochemistry of nitrous oxide in permanently ice-covered lakes of the

McMurdo Dry Valleys, Antarctica, Glob. Change Biol. 3, 301–305.Priscu, J.C. (1999) Life in the valley of the “dead”, Bioscience 49, 959.Priscu, J.C., Fritsen, C.H., Adams, E.E., Giovannoni, S.J., Paerl, H.W., McKay, C.P., Doran, P.T.,

Gordon, D.A., Lanoil, B.D. and Pinckney J.L. (1998) Perennial Antarctic lake ice: an oasis forlife in a Polar desert, Science 280, 2095–2098.

Priscu, J.C., Adams, E.E., Lyons, W.B., Voytek, M.A., Mogk, D.W., Brown, R.L., McKay, C.P.,Takacs, C.D., Welch, K.A., Wolf, C.F., Kirstein, J.D. and Avci, R. (1999a) Geomicrobiology ofsub-glacial ice above Vostok Station, Science 286, 2141–2144.

318 SHIV M. SINGH AND JOSEF ELSTER

Seckbach_Ch15.qxd 17/8/07 12:29 PM Page 318

Priscu, J.C., Wolf, C.F., Takacs, C.D., Fritsen, C.H., Laybourn-Parry, J., Roberts, E.C. and Lyons W.B.(1999b) Carbon transformations in the water column of a perennially ice-covered AntarcticLake, Bioscience 49, 997–1008.

Priscu, J.C., Fritsen, C.H., Adams, E.E., Paerl, H.W., Lisle, J.T., Dore, J.E., Wolf, C.F. and Mikucki,J.A. (2005) Perennial Antarctic lake ice: A refuge for cyanobacteria in an extreme environment.In: J.D. Castello and S.O. Rogers (eds.) Life in Ancient Ice, Princeton Press. p. 22–49.

Psenner, R. and Sattler, B. (1998) Life at freezing point, Science 280, 2073–2074.Psenner, R., Sattler, B., Willie, A., Fritsen, C.H., Priscu, J.C., Felip, M. and Catalan J. (1999) Lake Ice

microbial communities in Alpine and Antarctic Lakes. In: P. Schinner and R. Margesin (eds.)Adaptations of Organisms to Cold Environments, Springer-Verlag, pp. 17–31.

Redfield, A.C. (1958) The biological control of chemical factors in the environment, AmericanScientist, September, pp. 205–221.

Sabacká, M. and Elster, J. (2006) Response of cyanobacteria and algae from Antarctic wetland habi-tats to freezing and desiccation stress, Polar Biology, 30 (1), 31–37.

Sato, N. (1995) A family of cold-regulated RNA-binding protein genes in the cyanobacteriumAnabaena variabilis M3, Nucleic Acids Res. 23, 2161–2167.

Roos, J.C.. and Vincent, W.F. (1998) Temperature dependence of UV radiation effects on Antarcticcyanobacteria, J. Phycol. 34, 78–85.

Sand-Jensen, K., Riis, T., Markager, S. and Vincent, W.F. (1999) Slow growth and decomposition ofmosses in Arctic lakes, Can. J. Fish. Aquat. Sci. 56, 388–393.

Schrag, D.P. and Hoffman, P.F. (2001) Life, geology and snowball Earth, Nature 409, 306.Simmons, G.W. Jr., Vestal, J.R. and Wharton, R.A. Jr. (1993) Environmental regulators of microbial

activity in continental Antarctic lakes. In: W.J. Green and E.I. Friedmann (eds.) Physical andBiogeochemical Processes in Antarctic Lakes. Antarctic Research Series, American GeophysicalUnion, 59, 197–214.

Spauldin, S.A., McKnight, D.M., Smith, L.R. and Dufford, R. (1994) Phytoplanktonpopulation dynamics in perennially ice-covered lake Fryxell, Antarctica, J. Plankton Res. 16 (5),527–541.

Spigel, R.H. and Priscu, J.C. (1998) Physical limnology of the McMurdo Dry Valleylakes. In: J.C.Priscu (ed.) Ecosystem Dynamics in a Polar Desert: The McMurdo Dry Valleys, Antarctica.Antarctic Research series, American Geophysical Union, 72, 153–188.

Sun, W.Q. and Leopold, A.C. (1994a) The glassy state and seed storage stability: a viability equationanalysis, Ann. Bot., 74, 601–604.

Sun, W.Q. and Leopold, A.C. (1994b) The role of sugar, vitrification and membrane phase transitionin seed desiccation tolerance, Physiol. Plant. 90, 621–628.

Tang, E.P.Y. and Vincent, W. (1999) Strategies of thermal adaptation by high-latitude cyanobacteria,New Phytol. 142, 315–323.

Tang, E.P.Y., Tremblay, R. and Vincent, W.F. (1997) Cyanobacterial dominance of Polar freshwaterecosystems: are high latitude-mat-formers adapted to low temperature? J. Phycol. 33, 171–181.

Taylor, G. (1916) With Scott: The Silver Lining. Dodd, Mead and Company, New York.Vincent, W.F. (1988) Microbial Ecosystems of Antarctica. Cambridge University Press, UK, 304 pp.Vincent, W.F. (2000a) Cyanobacterial dominance in the Polar Regions. In: W. Potts (ed.)

Cyanobacteria: Their Diversity in Time and Space, Kluwer Academic Publishers, Dordrecht, TheNetherlands, pp. 321–338.

Vincent, W.F. (2000b) Cyanobacterial dominance in the Polar Regions. In: B.A. Whitton and M. Potts(eds.) The Ecology of Cyanobacteria: Their Diversity in Time and Space, Kluwer AcademicPublishers, Dordrecht, The Netherlands, pp. 321–340.

Vincent, W.F., and C. Howard-Williams (2001) Life on Snowball Earth, Science 287, 2421.Vincent, W.F., Howard-Williams, C. and Broady, P.A. (1993a) Microbial communities and processes

in Antarctic flowing waters. In: E.I. Friedmann (ed.) Antarctic Microbiology, New York, JohnWiley, pp. 543–569.

CYANOBACTERIA IN ANTARCTIC LAKE ENVIRONMENTS 319

Seckbach_Ch15.qxd 17/8/07 12:29 PM Page 319

Vincent, W.F., Castenholz, R.W., Downes, M.T. and Howard-Williams, C. (1993b) Antarctic cyano-bacteria: light, nutrients, and photosynthesis in the microbial mat environment, J. Phycol. 29,745–755.

Vincent, W.F., Downes, M.T., Castenholz, R.W. and Howard-Williams, C. (1993c) Communitystructure and pigment organization of cyanobacteria-dominated microbial mats in Antarctica,Eur. J. Phycol. 28, 213–221.

Vincent, W.F., Rae, R., Laurion, I., Howard-Williams, C. and Priscu, J.C. (1997) Transparency ofAntarctic ice-covered lakes to solar UV radiation, Limnol. Oceanogr. 43, 618–624.

Vincent, W.F., Gibson, J.A.E., Pienitz, R. and Villeneuve, V. (2000) Ice shelf microbial ecosystems inthe high Arctic and implications for life on snowball Earth, Naturwissenshaften 87, 137–141.

Vincent, W.F., Mueller, D., Van Hove, P. and Howard-Williams, C. (2004) Glacial periods on earlyEarth and implications for the evolution of life. In: J. Seckbach (ed.) Origins: Genesis, Evolutionand Diversity of Life, Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 481–501.

Vinebrooke, R.D. and Leavitt, P. (1999) Phytobenthos and phytoplankton as potential indicators ofclimatic change in mountain lakes and ponds: a HPLC-based pigment approach, J. North Am.Benthol. Soc. 18, 15–33.

Wall, D. and Virginia, R.A. (1998) Soil biodiversity and community structure in the McMurdo DryValleys, Antarctica. In: J.C. Priscu (ed.) Ecosystem Processes in a Polar Desert: The McMurdoDry Valleys, Antarctica. Antarctic Research Series, American Geophysical Union, 72,323–335.

Wharton, R.A. Jr., Parker, B.C. and Simmons, G.M. Jr. (1983) Distribution, species composition andmorphology of algal mats in Antarctic dry valley lakes, Phycologia 22, 355–365.

Wiedner, C. and Nixdorf, B. (1998) Success of chrysophytes, cryptophytes and dinoflagellates overblue-greens (cyanobacteria) during an extreme winter (1995/96) in eutrophic shallow lakes,Hydrobiologia, 369/370, 229–235.

Williams, D.M., Kasting, J.F. and Frakes, L.A. (1998) Low-latitude glaciation and rapid changes inthe earth’s obliquity explained by obliquity-oblateness feedback, Nature 396, 453–455.

Wilson, A.T. (1965) Escape of algae from frozen lakes and ponds, Ecology 46, 376.Wing, K.T. and Priscu, J.C. (1993) Microbial communities in the permanent ice cap of Lake Bonney,

Antarctica: relationships among chlorophyll a, gravel and nutrients, Antarct. J. US 28, 246–249.

320 SHIV M. SINGH AND JOSEF ELSTER

Seckbach_Ch15.qxd 17/8/07 12:29 PM Page 320