Viruses in the plankton of freshwater and saline Antarctic lakes

1. Virus‐like particle (VLP) abundances in nine freshwater to saline lakes in the Vestfold Hills, Eastern Antarctica (68° S) were determined in December 1999. In the ultra‐oligotrophic to oligotrophic freshwater lakes, VLP abundances ranged from 1.01 to 3.28 × 10⁶ mL^–1 in the top 6 m of the water column. In the saline lakes the range was between 6.76 and 36.5 × 10⁶ mL^–1. The lowest value was found in meromictic Ace Lake and the highest value in hypersaline Lake Williams. Virus to bacteria ratios (VBR) were lowest in the freshwater lakes and highest in the saline lakes, with a maximum of 23.4 in the former and 50.3 in the latter. 2. A range of morphologies among VLP was observed, including phages with short (Podoviridae) and long tails, icosahedric viruses of up to 300 nm and star‐like particles of about 80 nm diameter. 3. In these microbially dominated ecosystems there was no correlation between VLP and either bacterial numbers or chlorophyll a. There was a significant correlation between VLP abundances and dissolved organic carbon concentration (r=0.845, P < 0.01). 4. The data suggested that viruses probably attack a spectrum of bacteria and protozoan species. Virus‐like particle numbers in the freshwater lakes were lower than values reported for lower latitude systems. Those in the saline lakes were comparable with abundances reported from other Antarctic lakes, and were higher than most values published for lower latitude lakes and many marine systems. Across the salinity spectrum from freshwater through brackish to hypersaline, VLP concentrations increased roughly in relation to increasing trophy. 5. Given that Antarctic lakes have a plankton almost entirely made up of bacteria and protists, and that VLP abundances are high, it is likely that viruses play a pivotal role in carbon cycling in these extreme ecosystems.     

Ace Lake: three decades of research on a meromictic,Antarctic lake

Ace Lake (Vestfold Hills, Antarctica) has been investigated since the 1970s. Its close proximity to Davis Station has allowed year-long, as well as summer only, investigations. Ace Lake is a saline meromictic (permanently stratified) lake with strong physical and chemical gradients. The lake is one of the most studied lakes in continental Antarctica. Here, we review the current knowledge of the history, the physical and chemical environment, community structure and functional dynamics of the mixolimnion, littoral benthic algal mats, the lower anoxic monimolimnion and the sediment within the monimolimnion. In common with other continental meromictic Antarctic lakes, Ace Lake possesses a truncated food web dominated by prokaryote and eukaryote microorganisms in the upper aerobic mixolimnion and an anaerobic prokaryote community in the monimolimnion, where methanogenic Archaea, sulphate-reducing and sulphur-oxidizing bacteria occur. These communities are functional in winter at subzero temperatures, when mixotrophy plays an important role in survival in dominant photosynthetic eukaryotic microorganisms in the mixolimnion. The productivity of Ace Lake is comparable to other saline lakes in the Vestfold Hills, but higher than that seen in the more southerly McMurdo Dry Valley lakes. Finally, we identify gaps in the current knowledge and avenues that demand further investigation, including comparisons with analogous lakes in the north polar region.     

The plankton community of a young, eutrophic, Antarctic saline lake

A shallow, saline lake (Rookery Lake) close to the sea and surrounded by a penguin rookery was investigated during the austral spring and summer of 1996/1997. The proximity to the sea means that the lake is likely to have been formed recently during isostatic uplift. Inputs of carbon and nutrients from the penguin rookery have rendered Rookery Lake eutrophic compared with other brackish and saline lakes in the Vestfold Hills. Chlorophyll a concentration, bacterioplankton, heterotrophic nanoflagellate and phototrophic nanoflagellate abundances were all significantly higher than in other non-enriched lakes. The high productivity created seasonal anoxia during winter and spring below ice cover. The ciliate community resembled the marine community, and was dissimilar to that seen in older saline lakes within the Vestfold Hills. Thus Rookery Lake provides valuable evidence of the impact of natural eutrophication on an Antarctic lake, as well as of the evolution of the typical microbial community which dominates the older lakes of the Vestfold Hills. Accepted: 2 May 1999     

The biodiversity and ecology of Antarctic lakes: models for evolution

Antarctic lakes are characterised by simplified, truncated food webs. The lakes range from freshwater to hypersaline with a continuum of physical and chemical conditions that offer a natural laboratory in which to study evolution. Molecular studies on Antarctic lake communities are still in their infancy, but there is clear evidence from some taxonomic groups, for example the Cyanobacteria, that there is endemicity. Moreover, many of the bacteria have considerable potential as sources of novel biochemicals such as low temperature enzymes and anti-freeze proteins. Among the eukaryotic organisms survival strategies have evolved, among which dependence on mixotrophy in phytoflagellates and some ciliates is common. There is also some evidence of evolution of new species of flagellate in the marine derived saline lakes of the Vestfold Hills. Recent work on viruses in polar lakes demonstrates high abundance and high rates of infection, implying that they may play an important role in genetic exchange in these extreme environments.     

The microbial plankton of freshwater lakes in the Vestfold Hills,Antarctica

Summary The plankton of twelve freshwater and slightly saline lakes in the Vestfold Hills, Antarctica was sampled in February 1991. All of the lakes are oligotrophic. The chlorophyll a concentrations in the lakes ranged from 0.10–2.69 g · 1^–1. The majority of the phytoplankton were flagellates or picoplanktonic cyanobacteria with the species composition varying between the lakes. Cyanobacteria were found in five of the lakes. Five to 6 species of ciliated protozoa occurred, among them oligotrichs, including the mixotrophic species Strombidium viride. The concentrations of protists and bacteria were an order to several orders of magnitude lower than reported from lower latitude oligotrophic lakes. Low species diversity and low numbers in the plankton characterise these eastern Antarctica lakes which reflects their low nutrient status and isolation.     

The biology and evolution of Antarctic saline lakes in relation to salinity and trophy

. Five brackish to hypersaline lakes (Highway, Ace, Pendent, Williams and Rookery) in the Vestfold Hills, eastern Antarctica were investigated during the austral summer of 1999/2000. The aims were to characterise the functional dynamics of the plankton and gain an understanding of how the different environments in the lakes have led to the evolution of different communities. The plankton was dominated by microorganisms and differed across the salinity spectrum in relation to trophy, age and the presence of meromixis. However, some elements of the plankton were common to all of the lakes, e.g. the mixtrophic ciliate, Mesodinium rubrum, which reached abundances of 2.7᎒⁵ l^-1 and spanned a salinity gradient of 4-63‰. Marine dinoflagellate species also occurred in all of the lakes, often at high abundances in Highway Lake, Pendent Lake and Lake Williams. During December (mid-summer), primary production showed an increase along the salinity gradient from Highway Lake to Lake Williams; however, it was low in hyper-nutrified Rookery Lake because of the turbidity of the waters. Bacterial production followed the same trend and was extremely high in Rookery Lake (327 µg l^-1 h^-1 in January). The lakes possessed a marine microbial plankton that has become very simplified through time, and now contains a small number of highly successful species, which were pre-adapted to surviving in extreme Antarctic lakes.     

Widespread occurrence of populations of the unique autotrophic ciliate Metodinium rubrum (Ciliophora: Haptorida) in brackish and saline lakes of the Vestfold Hills (eastern Antarctica)

The occurrence of the unique autotrophic ciliate Mesodinium rubrum was investigated in a suite of lakes of various salinities situated in the Vestfold Hills oasis, Princess Elizabeth Land (eastern Antarctica). M. rubrum was found to occur in all but the most hypersaline lakes in the survey but was most numerous in the more brackish lakes. Salinity and water column temperature appeared to be the most important factors controlling the occurrence and abundance of this species. Nutrient levels (phosphate and nitrate) did not appear to be important controlling factors, although their influence may have been distorted by the fact that nutrient concentrations were generally higher in the more saline lakes. The widespread occurrence of this species in brackish and saline lakes of the Vestfold Hills provides opportunities to study the ecology and possible physiological and ultrastructural adaptations to living in a high-latitude environment of this ubiquitous and important species in marine microbial food webs.     

Influence of environmental conditions, bacterial activity and viability on the viral component in 10 Antarctic lakes

The influence of biotic and environmental variables on the abundance of virus-like particles (VLP) and lysogeny was investigated by examining 10 Antarctic lakes in the Vestfold Hills, Antarctica, in the Austral Spring. Abundances of viruses and bacteria and bacterial metabolic activity were estimated using SYBR Gold (Molecular Probes), Baclight (Molecular Probes) and 6-carboxy fluorescein diacetate (6CFDA). Total bacterial abundances among the lakes ranged between 0.12 and 0.47 x 10(9) cells L(-1). The proportion of intact bacteria (SYTO 9-stained cells) ranged from 13.5% to 83.5% of the total while active (6CFDA-stained) bacteria ranged from 33% to 116%. Lysogeny, as determined with Mitomycin C, was only detected in one of the lakes surveyed, indicating that viral replication was occurring predominantly via the lytic cycle. Principal component analysis and confirmatory correlation analysis of individual variables showed that high abundances of VLP occurred in lakes of high conductivity with high concentrations of soluble reactive phosphorus and dissolved organic carbon. These lakes supported high concentrations of chlorophyll a, intact bacteria, rates of bacterial production and virus to bacteria ratios. Thus, it was suggested that viral abundance in the Antarctic lakes was determined by the trophic status of the lake and the resultant abundance of intact bacterial hosts.     

Antarctic terrestrial ecosystems: The Vestfold Hills in context

Antarctic terrestrial ecosystems are briefly described, with emphasis on Signy Island in the maritime antarctic region, and the McMurdo oasis, southern Victoria Land, and Vestfold Hills in the continental antarctic region.As the largest and best known coastal ice-free oasis, the Vestfold Hills contain excellent examples of terrestrial sublithic, epilithic, chasmoendolithic, epiphytic and terricolous algal communities, as well as epilithic, endolithic, and epiphytic lichen communities, and moss communities. Many of the numerous lakes support dense communities of aquatic algae.     

Nematodes from saline and freshwater lakes of the Vestfold Hills,East Antarctica,including the description of <Emphasis Type="Italic">Hypodontolaimus antarcticus</Emphasis> sp. n.

The invertebrate fauna of many Antarctic ice-free areas, even those close to permanent research stations, can be poorly known. Here we describe some nematodes from freshwater and saline, marine-derived lakes of the Vestfold Hills, East Antarctica. The freshwater lakes contained the widespread East Antarctic endemic species, Plectus frigophilus Kirjanova, 1958. The saline lakes were inhabited by two recently described species, Halomonhystera halophila Andrássy, 2006 and Halomonhystera continentalis Andrássy, 2006, and by a new species described in this report, Hypodontolaimus antarcticus sp. n. Originally marine but now brackish Highway Lake contained a nematode fauna with both freshwater and marine-derived components. The nematode fauna of Antarctica now consists of 54 named species, 22 of which are found in East Antarctica.     

AN ENCYSTMENT STAGE,BEARING A NEW SCALE TYPE,OF THE ANTARCTIC PRASINOPHYTE PYRAMIMONAS GELIDICOLA AND ITS PALEOLIMNOLOGICAL AND TAXONOMIC SIGNIFICANCE1

Cysts of the Antarctic prasinophyte Pyramimonas gelidicola McFadden were found in water samples from a fjord and a saline lake in the Vestfold Hills, Antarctica Unialgal cultures of P. gelidicola from Ace Lake produced cysts. After ca. five weeks, tile cysts settled and adhered to the bottom of the culture flask. The cyst wall was covered by a scale type not seen on the flagellated cells; however, the base of the cyst scale was similar to the box scales of P. gelidicola motile cells. Cyst scales were also found off the continental shelf in Prydz Bay. In a 1.7 m sediment core taken from Ace Lake, both cyst scales and box scales of P. gelidicola occurred at most depths. Differences in the ratio of these two scale types at different depths in the core may indicate past ecological changes in the lake. Upper sediments of the core were dated at 5310 ± 90 yrs B.P., indicating that prasinophyte scales may be recognizably preserved for extended periods. P. gelidicola was widely distributed in saline lakes of the Vestfold Hills with salinities of 3.2–133% and temperatures ranging from – 5.0 to 10.4°C. This is the first report of encystment of P. gelidicola and, to our knowledge, is the first record of a prasinophyte with two distinctly different scale types occurring on cells during different stages of the life history.     

MARINE‐DERIVED DINOFLAGELLATES IN ANTARCTIC SALINE LAKES: COMMUNITY COMPOSITION AND ANNUAL DYNAMICS1*[link]

The saline lakes of the Vestfold Hills in Antarctica offer a remarkable natural laboratory where the adaptation of planktonic protists to a range of evolving physiochemical conditions can be investigated. This study illustrates how an ancestral marine community has undergone radical simplification leaving a small number of well‐adapted species. Our objective was to investigate the species composition and annual dynamics of dinoflagellate communities in three saline Antarctic lakes. We observed that dinoflagellates occur year‐round despite extremely low PAR during the southern winter, which suggests significant mixotrophic or heterotrophic activity. Only a small number of dominant dinoflagellate species were found in each lake, in contrast to the species‐rich Southern Ocean from which the lake communities are believed to be derived. We verified that the lake species were representatives of the marine polar dinoflagellate community, and not freshwater species. Polarella glacialis Montresor, Procaccini et Stoecker, a bipolar marine species, was for the first time described in a lake habitat and was an important phototrophic component in the higher salinity lakes. In the brackish lakes, we found a new sibling species to the brackish‐water species Scrippsiella hangoei (J. Schiller) J. Larsen, previously observed only in the Baltic Sea.     

Biogeochemical study of organic substances in Antarctic lakes

The features of organic constituents in Antarctic lakes and ponds of the McMurdo, Syowa and Vestfold oases are summarised from a biogeochemical viewpoint. Total organic carbon or dissolved organic carbon contents in saline lakewaters are generally extremely high and much higher than those in freshwater lakes. The concentrations and/or compositions of hydrocarbons, fatty acids, sterols, phenolic acids and hydroxy acids in lake and pond waters and sediments vary markedly, probably reflecting differences in biological activity and source organisms. Long-chain alkenes, such as n-C_29:2 (carbon chain length: numbers of unsaturated bonds) are found as the major hydrocarbons in some anoxic lake sediments. Unusually, long-chain n-alkanoic acids are abundant in some Antarctic lake sediments and 24-ethylcholest-5-en-3-ol is the most prominent sterol in most of the lakes studied. It is suggested that some bacteria, and cyanobacteria and algae are important sources of long-chain n-alkanoic acids and 24-ethylcholest-5-en-3-ol, respectively, as previously reported from environments of the mid and lower latitudes. The dominance of p-hydroxybenzoic acid among the phenolic acids found together with the absence of syringic, p-coumaric and ferulic acids in the Antarctic lakes reflects the absence of vascular plants in the areas studied.In three Antarctic saline lakes (Vanda, Fryxell and Ace) the kinds and amounts of organic constituents differ with depth due to the zonation of microorganisms. The maximum fatty acid contents are found at depths just above the anoxic layer, corresponding to the photosynthetic maxima in the lakes, and the depths of maximum phytoplankton populations. In the bottom sediments of the lakes, the composition of organic substances is significantly different from that in the water columns, indicating that the sinking organic substances are degraded rapidly by microorganisms on the lake bottom.     

Microbial diversity and function in Antarctic freshwater ecosystems

Freshwater lakes occur through much of Antarctica and are characterized by short food chains dominated by microbes. Comparatively few studies have been made of continental freshwater lakes until recently, with the main emphasis being on the less extreme maritime Antarctic lakes. The wide range of trophic status seen at the northern extremes of the maritime Antarctic reduces markedly further south, but a wide range of micro-organisms occur throughout the latitudinal range. Information on seasonal and spatial patterns of microbial activity for freshwater lakes demonstrate rapid changes in community composition at certain times of year despite constant low temperatures. Benthic communities of cyanobacteria and bacteria are a feature of most lakes and are involved in a wide range of geochemical cycling. There is a need for more detailed taxonomic information on most groups and considerable potential for molecular studies.     

Seasonal dynamics of the planktonic community in Lake Druzhby, Princess Elizabeth Land, Eastern Antarctica

1. The temporal abundance and composition of the plankton of a continental Antarctic lake (Lake Druzhby) situated in the Vestfold Hills, Eastern Antarctica was investigated from December 1992 to December 1993. The system was dominated by microbial plankton (cyanobacteria, heterotrophic bacteria and protozoans) with few metazoans. 2. Chlorophyll a concentrations ranged between 0.15 and 1.1 μg l^–1 and showed highest levels from late winter to spring. 3. Heterotrophic bacteria ranged between 75 and 250 × 10⁶ l^–1 with highest abundances in late winter/spring. Mean bacterial biovolumes showed considerable seasonal variation (0.05–0.31 μm³). Largest biovolumes occurred in summer and this was the time of highest community biomass. 4. Heterotrophic nanoflagellates reached highest abundances in late summer (maximum 14 × 10⁵ l^–1). Their mean biovolume also exhibited considerable seasonal variation, ranging between 1.77 and 27.0 μm³, with largest size resulting in community biomass peaking in early summer. Ciliated protozoa were poorly represented and sparse. Phototrophic nanoflagellates were sparse in this lake; instead the phototrophic plankton was dominated by a small rod-shaped cyanobacterium which constituted the largest carbon pool in the system. It was common throughout the year, its biomass peaking in autumn. Its presence is discussed in relation to lake morphometry and light climate. 5. Heterotrophic flagellate grazing rates ranged from 6.78 bacteria cell^–1 day^–1 at 2 °C to 11.8 bacteria cell^–1 day^–1 at 4 °C. They remove around 2% of the bacterial carbon pool per day during summer and winter. 6. Nutrient levels were low and recorded in pulses. Dissolved and particulate organic carbon were also low, usually less than 3 mg l^–1 and 600 μg l^–1, respectively. The carbon pools were derived from autochthonous sources. This lake system is driven by bottom-up forces and lacks top-down control, which fits into the picture currently seen for continental Antarctic lakes.     

Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes

1. Seasonal patterns of grazing and photosynthesis were investigated in two saline Antarctic lakes (Highway and Ace) in the Vestfold Hills (68°S). The phototrophic nanoflagellate (PNAN) community was dominated by Pyramimonas gelidicola and two morphological forms of a cryptophyte species that occurred throughout the year. Both species were mixotrophic on bacteria, and in Highway Lake they also exploited dissolved organic carbon as determined by the uptake of fluorescently labelled dextrans. 2. Clearance rates ranged between 0.02 and 0.21 nL h^?1 cell^?1 in Ace Lake and 0.004–1.05 nL h^?1 cell^?1 in Highway Lake. On occasion cryptophyte grazing equalled that of the heterotrophic nanoflagellates (HNAN). 3. Photosynthetic rates showed similar trends in both lakes, but there were differences in chlorophyll a specific rates and photosynthetic efficiency, probably related to the meromictic characteristic of Ace Lake. Primary production was measurable in winter and peaked in summer following the maxima of mixotroph grazing. 4. The HNAN community of Highway Lake achieved clearance rates of 0.02–1.80 nL h^?1 cell^?1 and removing between 50 and 693 ng bacterial carbon L^?1 day^?1, with highest impact in winter when HNAN were most abundant. The HNAN also ingested fluorescently labelled dextrans showing a preference for 4 and 500 kDa molecules. The more diverse HNAN community of Ace Lake had lower clearance rates (0.04–0.37 nL h^?1 cell^?1) and exerted a lower grazing pressure on bacterioplankton. In Highway Lake, where the HNAN community was dominated by the choanoflagellate Diaphanoeca grandis, there was a significant correlation between mean cell volume and clearance rate. 5. The major feature was that the microbial plankton functioned throughout the year by employing nutritional versatility.     

Daphniopsis studeri (Crustacea: Cladocera) in lakes of the Vestfold Hills,Antarctica

Summary The adult sizes and reproductive capabilities of populations of the cladoceran Daphniopsis studeri Rühe from freshwater and slightly saline lakes in the Vestfold Hills, Princess Elizabeth Land were monitored during December, 1990. The population of Crooked Lake was studied in detail from July 1990–March 1991. Limited samples were also obtained from Heard Island (sub Antarctic). Obligate parthenogenesis involving the production of subitaneous eggs appears to be the case. No males occurred. The overwintering populations of continental Antarctica consist mainly of adult females containing extensive fat reserves. The main reproductive effort occurs in spring. some females produce a smaller second brood during the summer. Reproductive output increases with adult size which is related to the nutrient status of the lake and its productivity. The Heard Island populations have a higher weight to length ratio than the Vestfold populations and have a much greater reproductive output.     

Detection of a novel ecotype of <Emphasis Type="Italic">Pfiesteria piscicida</Emphasis> (Dinophyceae) in an Antarctic saline lake by real-time PCR

The heterotrophic dinoflagellate Pfiesteria piscicida was detected in Ace Lake in the Vestfold Hills, eastern Antarctica by using real-time PCR based on 18S rDNA sequences. Antarctic water samples collected in 2004 were tested by species-specific real-time PCR assays for the identification of P. piscicida and P. shumwayae. Positive results were shown with P. piscicida-specific real-time PCR, and PCR products were examined by sequence analysis for confirmation. A phylogenetic tree made from partial 18S rDNA sequences showed that the Antarctic clone clustered with P. piscicida. This result suggests that P. piscicida is present in the extreme conditions of an Antarctic saline lake which has not contained fish for thousands of years.     

Diversity of 746 heterotrophic bacteria isolated from microbial mats from ten Antarctic lakes

Microbial mats, growing in Antarctic lakes constitute unique and very diverse habitats. In these mats microorganisms are confronted with extreme life conditions. We isolated 746 bacterial strains from mats collected from ten lakes in the Dry Valleys (lakes Hoare and Fryxell), the Vestfold Hills (lakes Ace, Druzhby, Grace, Highway, Pendant, Organic and Watts) and the Larsemann Hills (lake Reid), using heterotrophic growth conditions. These strains were investigated by fatty acid analysis, and by numerical analysis, 41 clusters, containing 2 to 77 strains, could be delineated, whereas 31 strains formed single branches. Several fatty acid groups consisted of strains from different lakes from the same region, or from different regions. The 16S rRNA genes from 40 strains, representing 35 different fatty acid groups were sequenced. The strains belonged to the alpha, beta and gamma subclasses of the Proteobacteria, the high and low percent G+C Gram-positives, and to the Cytophaga-Flavobacterium-Bacteroides branch. For strains representing 16 fatty acid clusters, validly named nearest phylogenetic neighbours showed pairwise sequence similarities of less than 97%. This indicates that the clusters they represent, belong to taxa that have not been sequenced yet or as yet unnamed new taxa, related to Alteromonas, Bacillus, Clavibacter, Cyclobacterium, Flavobacterium, Marinobacter, Mesorhizobium, Microbacterium, Pseudomonas, Saligentibacter, Sphingomonas and Sulfitobacter.     

Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes

For the first time, the cyanobacterial diversity from microbial mats in lakes of Eastern Antarctica was investigated using microscopic and molecular approaches. The present study assessed the biogeographical distribution of cyanobacteria in Antarctica. Five samples were taken from four lakes spanning a range of different ecological environments in Larsemann Hills, Vestfold Hills and Rauer Islands to evaluate the influence of lake characteristics on the cyanobacterial diversity. Seventeen morphospecies and 28 16S rRNA gene-based operational taxonomic units belonging to the Oscillatoriales, Nostocales and Chroococcales were identified. The internal transcribed spacer was evaluated to complement the 16S rRNA gene data and showed similar but more clear-cut tendencies. The molecular approach suggested that potential Antarctic endemic species, including a previously undiscovered diversity, are more abundant than has been estimated by morphological methods. Moreover, operational taxonomic units, also found outside Antarctica, were more widespread over the continent than potential endemics. The cyanobacterial diversity of the most saline lakes was found to differ from the others, and correlations between the sampling depth and the cyanobacterial communities can also be drawn. Comparison with database sequences illustrated the ubiquity of several cyanobacterial operational taxonomic units and their remarkable range of tolerance to harsh environmental conditions.