Polar Biology

, Volume 39, Issue 12, pp 2207–2225 | Cite as

Heterotrophic bacteria in Antarctic lacustrine and glacial environments

Review

Abstract

Antarctica has the greatest diversity of lakes types on the planet including freshwater, brackish, saline and hypersaline systems, epishelf lakes, ice shelf lakes and lakes and cryoconite holes on glacier surfaces. Beneath the continental ice sheet, there are hundreds of subglacial lakes. These systems are dominated by microbial food webs, with few or no metazoans. They are subject to continuous cold, low annual levels of photosynthetically active radiation and little or no allochthonous nutrient inputs from their catchments. Subglacial lakes function in darkness. Heterotrophic bacteria are a conspicuous and important component of the simple truncated food webs present. Bacterial abundance and production vary between freshwater and saline lakes, the latter being more productive. The bacterioplankton functions throughout the year, even in the darkness of winter when primary production is curtailed. In more extreme glacial habitats, biomass is even lower with low rates of production during the annual melt season. Inter-annual variation appears to be a characteristic of bacterial production in lakes. The factors that control production appear to be phosphorus limitation and grazing by heterotrophic and mixotrophic flagellate protozoa. The evidence suggests high rates of viral infection in bacteria and consequent viral lysis, resulting in significant carbon recycling, which undoubtedly supports bacterial growth in winter. The biodiversity of lacustrine Antarctic heterotrophic bacteria is still relatively poorly researched. However, most of the main phyla are represented and some patterns are beginning to emerge. One of the major problems is that data for heterotrophic bacteria are confined to a few regions served by well-resourced research stations, such as the McMurdo Dry Valleys, the Vestfold Hills and Signy Island. A more holistic multidisciplinary approach is needed to provide a detailed understanding of the functioning, biodiversity and evolution of these communities. This is particularly important as Antarctic lakes are regarded as sentinels of climate change.

Keywords

Antarctica Heterotrophic bacteria Lakes Glaciers Extremophiles 

Notes

Acknowledgments

The work of the authors quoted here was funded by the Natural Environment Research Council (UK) the Levehulme Trust (UK), the National Science Foundation (USA) and the Australian Antarctic Program.

References

  1. Albertsen M, Hugenholtz P, Skarshewski A, Nielsen KL, Tyson GW, Nielsen PH (2013) Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nat Biotechnol 31:533–538PubMedCrossRefGoogle Scholar
  2. Alfreider A, Pernhaler J, Amann R, Sattler B, Glockner F, Wille A, Psenner R (1996) Community analysis of the bacterial assemblages in the winter cover and pelagic layers of a high mountain lake by in situ hybridization. Appl Environ Microbiol 62:2138–2144PubMedPubMedCentralGoogle Scholar
  3. Anesio AM, Sattler B, Foreman C, Hodson AJ, Tranter M, Psenner R (2011) Carbon fluxes through bacterial communities on glacier surfaces. Ann Glaciol 51(56):32–40CrossRefGoogle Scholar
  4. Antoniades D, Crawley C, Douglas MSV, Pienitz R, Andersen D, Foran PT, Hawes I, Pollard W, Vincent WF (2007) Abrupt environmental change in Canada’s northernmost lake inferred from diatom and fossil pigment stratigraphy. Geophys Res Lett 34:L18708. doi: 10.1029/2007Gl030947 CrossRefGoogle Scholar
  5. Bagshaw EA, Tranter M, Wadham JL, Fountain AG, Basagic H (2010) Dynamic behaviour of supraglacial lakes on cold polar glaciers: Canada Glacier, McMurdo Dry Valleys, Antarctica. J Glaciol 56:366–368CrossRefGoogle Scholar
  6. Bayliss P, Ellis-Evans JC, Laybourn-Parry J (1997) Temporal patterns of primary production in a large ultra-oligotrophic Antarctic freshwater lake. Polar Biol 18:363–370CrossRefGoogle Scholar
  7. Bell EM, Laybourn-Parry J (1999) Annual plankton dynamics in an Antarctic saline lake. Freshw Biol 41:507–519CrossRefGoogle Scholar
  8. Bowman JP, McCammon SA, Skerratt JH (1997) Methylosphaera hansonii gen. nov., sp. nov., a psychrophilic, group I methanotroph from Antarctic marine-salinity, meromictic lakes. Microbiology 143:1451–1459PubMedCrossRefGoogle Scholar
  9. Bowman JP, Rea SM, McCammon SA, McMeekin TA (2000) Diversity and community structure within anoxic sediment from marine meromicic lakes and a coastal marine basin, Vestfold Hills, Eastern Antarctica. Environ Microbiol 2:227–237PubMedCrossRefGoogle Scholar
  10. Bowman JP, Nichols CM, Gibson JAE (2003) Algoriphagus ratkowskyi gen.nov., sp. nov., Brumimicrobium glaciale gen. nov., sp. nov., Cryomorpha ignava gen. nov., sp. nov. and Crocinitomix catalasitica gen. nov., sp. nov, novel Flavobacteria isolated from various polar habitats. Int J Syst Evol Microbiol 53:1343PubMedCrossRefGoogle Scholar
  11. Brambilla E, Hippe H, Hagelstein A, Tindall BJ, Stackebrandt E (2001) 16S rDNA diversity of cultured and uncultured prokaryotes of a mat sample from Lake Fryxell, McMurdo Dry Valleys, Antarctica. Extremophiles 5:23–33PubMedCrossRefGoogle Scholar
  12. Bulat SA, Alekhina IA, Blot M, Petit J-R, de Angelis M, Wagenbach D, Lipenkov VY, Vasilyena LP, Wloch DM, Raynaud D, Lukin VV (2004) DNA signature of thermophilic bacteria from the aged accretion ice of Lake Vostok, Antarctica; implications for searching for life in extreme icy environments. Int J Astrobiol 3:1–12CrossRefGoogle Scholar
  13. Butler HG (1999) Seasonal dynamics of the planktonic microbial community in a maritime Antarctic lake undergoing eutrophication. J Plankton Res 21:2393–2419CrossRefGoogle Scholar
  14. Butler HG, Edworthy MG, Ellis-Evans JC (2000) Temporal plankton dynamics in an oligotrophic maritime Antarctic lake. Freshw Biol 43:215–230CrossRefGoogle Scholar
  15. Cameron KA, Hodson AJ, Osborn AM (2011) Structure and diversity of bacterial, eukaryotic and archaeal communities in glacial cryoconite holes from the Arctic and the Antarctic. FEMS Microbiol Ecol 82:254–267CrossRefGoogle Scholar
  16. Carneiro AR, Ramos RT, Dall’Agnol H, Pinto AC, de Castro Soares S, Santos AR, Guimarães LC, Almeida SS, Baraúna RA, das Graças DA, Franco LC, Ali A, Hassan SS, Nunes CI, Barbosa MS, Fiaux KK, Aburjaile FF, Barbosa EG, Bakhtiar SM, Vilela D, Nóbrega F, dos Santos AL, Carepo MS, Azevedo V, Schneider MP, Pellizari VH, Silva A (2012) Genome sequence of Exiguobacterium antarcticum B7, isolated from a biofilm in Ginger Lake, King George Island, Antarctica. J Bacteriol 194:6689–6690PubMedPubMedCentralCrossRefGoogle Scholar
  17. Carvalho FR, Nastasi FR, Gamba RC, Foronda AS, Pellizari VH (2008) Occurrence and diversity of Legionellaceae in polar lakes of the Antarctic peninsula. Curr Microbiol 57:294–300PubMedCrossRefGoogle Scholar
  18. Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ Microbiol 3:570–577PubMedCrossRefGoogle Scholar
  19. Christner BC, Kvitko BH, Reeve JN (2003) Molecular identification of bacteria and Eukarya inhabiting an Antarctic cryoconite hole. Extremophiles 7:177–183PubMedGoogle Scholar
  20. Christner BC, Royston-Bishop G, Foreman CM, Arnold BR, Tranter M, Welch KA, Lyons WB, Tsapin AI, Studinger M, Priscu JC (2006) Limnological conditions in subglacial Lake Vostok. Limnol Oceanogr 51:2485–2501CrossRefGoogle Scholar
  21. Christner BC, Priscu JC, Achberger AM, Barbante C, Carter SP et al (2014) Subglacial Lake Whillans: a microbial ecosystem beneath the West Antarctic ice sheet. Nature 512:310–313PubMedCrossRefGoogle Scholar
  22. Clocksin KM, Deborah O, Madigan J, Madigan MT (2007) Cold-active chemoorganotrophic bacteria from permanently ice-covered Lake Hoare, Mcmurdo Dry Valleys, Antarctica. Appl Environ Microbiol 73:3077–3083PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater ecosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10CrossRefGoogle Scholar
  24. Collins MD, Lawson PA, Labrenz M, Tindall BJ, Weiss N, Hirsch P (2002) Nesterenkonia lacusekhoensis sp. nov., isolated from hypersaline Ekho Lake, East Antarctica, and emended description of the genus Nesterenkonia. Int J Syst Evol Microbiol 4:1145–1150Google Scholar
  25. Dolhi JM, Maxwell DP, Morgan-Kiss RM (2013) The Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis. Extremophiles 17:711–722PubMedCrossRefGoogle Scholar
  26. Dorado-Garcia I, Medina-Sánchez JM, Herrera G, Cabrerizo MJ, Carrillo P (2014) Quantification of carbon and phosphorus co-limitation in bacterioplankton: new insights on an old topic. PLoS Biol 9(6):e999288Google Scholar
  27. Doran PT, Fritsen CH, McKay CP, Priscu JC, Adams EE (2003) Formation and character of an ancient 19-m ice cover and underlying trapped brine in an ‘ice-sealed’ east Antarctic lake. Proc Natl Acad Sci U S A 100:26–31PubMedCrossRefGoogle Scholar
  28. Ellis-Evans JC, Laybourn-Parry J, Bayliss P, Perriss SJ (1998) Physical, chemical and microbial community characteristics of lakes of the Larsemann Hills, continental Antarctica. Arch Hydrobiol 141:29–230Google Scholar
  29. Felip M, Sattler B, Psenner R, Catalan J (1995) Highly active microbial communities in the ice and snow cover of high mountain lakes. Appl Environ Microbiol 61:2394–2401PubMedPubMedCentralGoogle Scholar
  30. Ferris JM, Burton HR (1988) The annual cycle of heat content and mechanical stability of hypersaline Deep Lake, Vestfold Hills, Antarctica. Hydrobiologia 165:115–128CrossRefGoogle Scholar
  31. Foong CP, Wong Vui Ling CM, González M (2010) Metagenomic analyses of the dominant bacterial community in the Fildes Peninsula, King George Island (South Shetland Islands). Polar Sci 4:263–273CrossRefGoogle Scholar
  32. Foreman CM, Sattler B, Mikucki JA, Porazinska DL, Priscu JC (2007) Metabolic activity and diversity of cryoconites in the Taylor Valley, Antarctica. J Geophys Res 112:32CrossRefGoogle Scholar
  33. Franzmann PD, Rohde M (1991) An obligately anaerobic, coiled bacterium from Ace Lake, Antarctica. J Gen Microbiol 137:2191–2196CrossRefGoogle Scholar
  34. Franzmann PD, Deprez PP, Buron HR, van den Hoff J (1987) Limnology of Organic Lake, Antarctica, a meromictic lake that contains high concentrations of dimethyl sulfide. Aust J Mar Freshw Res 38:409–417CrossRefGoogle Scholar
  35. Franzmann PD, Skyring GW, Burton HR, Deprez PP (1988) Sulfate reduction rates and some aspects of the limnology of four lakes and a fjord in the Vestfold Hills, Antarctica. Hydrobiologia 165:25–33CrossRefGoogle Scholar
  36. Franzmann PD, Höpfl P, Weiss N, Tindall BJ (1991a) Psychrotrophic, lactic acid-producing bacteria from anoxic waters in Ace Lake, Antarctica; Carnobacterium funditum sp. nov. and Carnobacterium alterfunditum sp. nov. Arch Microbiol 156:255–262PubMedCrossRefGoogle Scholar
  37. Franzmann PD, Roberts NJ, Mancuso CA, Burton HR, McMeekin TA (1991b) Methane production in meromictic Ace lake, Antarctica. Hydrobiologia 210:191–201CrossRefGoogle Scholar
  38. Franzmann PD, Liu Y, Balkwill DL, Aldrich HC, Conway E et al (1997) Methanogenium frigidum sp. Nov., a psychrophilic, H2-using methanogen from Ace Lake. Int J Syst Bacteriol 47:1068–1072PubMedCrossRefGoogle Scholar
  39. Fricker HA, Scambos T, Bindschadler R, Padman L (2007) An active subglacial water system in West Antarctica mapped from space. Science 315:1544–1548PubMedCrossRefGoogle Scholar
  40. Fukui F, Torii T, Okabe S (1985) Vertical distribution of nutrients and DOC in lake waters near Syowa Station, Antarctica. Antarct Rec 86:28–35Google Scholar
  41. Gibson JAE, Andersen DT (2002) Physical structure of the epishelf lakes of the southern Bunger Hills, East Antarctica. Antarct Sci 14:253–261CrossRefGoogle Scholar
  42. Gilbert J, Davies P, Laybourn-Parry J (2005) A hyperactive calcium dependent antifreeze protein in an Antarctic bacterium. FEMS Microbiol Lett 245:67–72PubMedCrossRefGoogle Scholar
  43. Glatz RE, Lepp PW, Ward BB, Francis CA (2006) Planktonic microbial community composition across steep physical/chemical gradients in permanently ice-covered Lake Bonney, Antarctica. Geobiology 4:53–67CrossRefGoogle Scholar
  44. Green WJ, Lyons WB (2009) The saline lakes of the McMurdo Dry Valleys, Antarctica. Aquat Geochem 15:321–348CrossRefGoogle Scholar
  45. Hahn MW, Koll U, Jezberová J (2015) Global phylogeography of pelagic Polynucleobacter bacteria: restricted geographic distribution of subgroups, isolation by distance and influence of climate. Environ Microbiol 17:829–840PubMedCrossRefGoogle Scholar
  46. Hall EK, Dzialowski AR, Stoxen SM, Cotner JB (2009) The effect of temperature on the coupling between phosphorus and growth in lacustrine bacterioplankton communities. Limnol Oceanogr 54:880–889CrossRefGoogle Scholar
  47. Hansson L-A, Hylander H, Dartnall HJG, Lidström S, Svensson J-E (2011) High zooplankton diversity in the extreme environments of the McMurdo Dry Valley lakes, Antarctica. Antarct Sci 24:131–138CrossRefGoogle Scholar
  48. Hawes I, Howard-Williams C, Fountain AG (2008) Ice-based freshwater ecosystems. In: Vincent WF, Laybourn-Parry J (eds) Polar lakes and rivers, limnology of Arctic and Antarctic ecosystems. Oxford University Press, Oxford, pp 103–118CrossRefGoogle Scholar
  49. Heath CW (1988) Annual primary productivity of an Antarctic continental lake: phytoplankton and benthic algal mat production strategies. Hydrobiologia 165:77–87CrossRefGoogle Scholar
  50. Hendy CH (2000) Late quaternary lakes in the McMurdo sound region of Antarctica. Geogr Ann A 82:411–432CrossRefGoogle Scholar
  51. Henshaw T, Laybourn-Parry J (2002) The annual patterns of photosynthesis in two large freshwater, ultra-oligotrophic Antarctic lakes. Polar Biol 25:744–752Google Scholar
  52. Herbei R, Lyons WB, Laybourn-Parry J, Gardner C, Priscu JC, McKnight DM (2010) Physiochemical properties influencing biomass abundance and primary production in Lake Hoare, Antarctica. Ecol Model 221:1184–1193CrossRefGoogle Scholar
  53. Hobbie JE, Laybourn-Parry J (2008) Heterotrophic microbial processes in polar lakes. In: Vincent WF, Laybourn-Parry J (eds) Polar lakes and rivers, limnology of Arctic and Antarctic ecosystems. Oxford University Press, Oxford, pp 197–212CrossRefGoogle Scholar
  54. Hodgson DA, Johnston NM, Caulkett AP, Jones VJ (1998) Palaeolimnology of Antarctic fur seal Arctocephalus gazelle populations and implications for Antarctic management. Biol Conserv 83:145–154CrossRefGoogle Scholar
  55. Hodson AJ, Anesio AM, Tranter M, Fountain AG, Osborn M, Priscu JC, Laybourn-Parry J, Sattler B (2008) Glacial ecosystems. Ecol Monogr 78:41–67CrossRefGoogle Scholar
  56. Hodson AJ, Paterson H, Westwood K, Cameron K, Laybourn-Parry J (2013) A blue ice ecosystem on the margins of the East Antarctic ice sheet. J Glaciol. doi: 10.3189/2013JoG12J052 Google Scholar
  57. Hofer JS, Sommaruga R (2001) Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat Microb Ecol 26:1–11CrossRefGoogle Scholar
  58. Hosoi-Tanabe S, Zhang H, Zhu D, Nagata S, Ban S, Imura S (2010) Comprehensive analysis of an antarctic bacterial community with the adaptability of growth at higher temperatures than those in Antarctica. Biocontrol Sci 15:57–62PubMedCrossRefGoogle Scholar
  59. Huang JP, Hoover RB, Swain A, Murdock C, Bej AK (2010) Comparison of the microbial diversity and abundance between the freshwater land-locked lakes of the Schirmacher Oasis and the perennially ice-covered Lake Untersee in East Antarctica. NASA Technical Report: ntrs.nasa.gov/archive/nasa/casi,ntrs.gov/20100040620
  60. Huang JP, Swain AK, Anderson DT, Bej AK (2014) Bacterial diversity within five unexplored freshwater lakes interconnected by surface channels in East Antarctica dronning maud land (Schirmacher Oasis) using amplicon pyrosequencing. Polar Biol 37:359–366CrossRefGoogle Scholar
  61. Izaguirre I, Allende L, Marinone MC (2003) Comparative study of the planktonic communities of three lakes of contrasting trophic status at Hope Bay (Antarctic Peninsula). J Plankton Res 25:1079–1097CrossRefGoogle Scholar
  62. Jacquet S, Domaizon I, Chardon C, Personnic S (2013) Are small grazers and/or viruses a structuring factor of free-living bacterial community in Lake Geneva? Adv Microbiol 3:233–248CrossRefGoogle Scholar
  63. James SR, Burton HR, McMeekin TA, Mancus CA (1994) Seasonal abundance of Halomonas meridian, Halomonas subglaciescola, Flavobacerium gondwanense and Flavobacterium salegens in four Antarctic lakes. Antarct Sci 6:325–332CrossRefGoogle Scholar
  64. James MR, Pridmore RD, Cummings VJ (1995) Planktonic communities of melt ponds on the McMurdo Ice Shelf, Antarctica. Polar Biol 15:555–567CrossRefGoogle Scholar
  65. Jansson M, Bergström A-K, Lymer D, Vrede K, Karlsson J (2006) Bacterioplankton and nutrient use efficiencies under variable organic carbon and inorganic phosphorus ratios. Microb Ecol 52:358–364PubMedCrossRefGoogle Scholar
  66. Karr EA, Sattley WM, Rice MR, Jung DO, Madigan MT, Achenbach LA (2005) Diversity and distribution of sulfate-reducing bacteria in permanently frozen Lake Fryxell, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 71:6353–6359PubMedPubMedCentralCrossRefGoogle Scholar
  67. Karr EA, Ng JM, Belchik SM, Sattley WM, Madigan MT, Achenbach LA (2006) Biodiversity of methanogenic and other Archaea in the permanently frozen Lake Fryxell, Antarctica. Appl Environ Microbiol 72:1663–1666PubMedPubMedCentralCrossRefGoogle Scholar
  68. Kurosawa N, Sato S, Kawarabayasi Y, Imura S, Naganuma T (2010) Archaeal and bacterial community structures in the anoxic sediment of Antarctic meromictic lake Nurume-Ike. Polar Sci 4:421–429CrossRefGoogle Scholar
  69. Labrenz M, Collins MD, Lawson PA, Tindall BJ, Braker G, Hirsch P (1998) Antarctobacter heliothermus gen. nov., sp. nov., a budding bacterium from hypersaline and heliothermal Ekho Lake. Int J Syst Bacteriol 48:1363–1372PubMedCrossRefGoogle Scholar
  70. Lanoil BD, Ciuffetti LM, Giovannoni SJ (1996) The marine bacterium Pseudoalteromonas haloplanktis has a complex genome structure composed of two separate genetic units. Genome Res 6(12):1160–1169PubMedCrossRefGoogle Scholar
  71. Lauro FM, DeMaere MZ, Yau S, Brown MV, Ng C, Wilkins D, Raftery MJ, Gibson JAE, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Thomas T, Cavicchioli R (2011) An interactive study of a meromictic lake ecosystem in Antarctica. ISME J 5:879–895PubMedCrossRefGoogle Scholar
  72. Lawson PA, Collins MD, Schumann P, Tindall BJ, Hirsch P, Labrenz M (2000) New LL-diaminopimelic acid-containing actinomycetes from hypersaline, heliothermal and meromictic Antarctic Ekho Lake: Nocardioides aquaticus sp. nov. and Friedmanniella [correction of Friedmannielly] lacustris sp. nov. Syst Appl Microbiol 23:219–229PubMedCrossRefGoogle Scholar
  73. Laybourn-Parry J, Bayliss B (1996) Seasonal dynamics of the planktonic community of Lake Druzhby, Princess Elizabeth Land, Eastern Antarctica. Freshw Biol 35:57–67CrossRefGoogle Scholar
  74. Laybourn-Parry J, Walton M (1998) Seasonal heterotrophic flagellate and bacterial plankton dynamics in a large oligotrophic lake—Loch Ness. Freshw Biol 39:1–8CrossRefGoogle Scholar
  75. Laybourn-Parry J, Pearce DA (2007) The biodiversity and ecology of Antarctic lakes—models for evolution. Philos Trans R Soc Lond B 362:2273–2289CrossRefGoogle Scholar
  76. Laybourn-Parry J, Bell EM (2014) Ace Lake: three decades of research on a meromictic, Antarctic lake. Polar Biol 37:1685–1699CrossRefGoogle Scholar
  77. Laybourn-Parry J, Wadham JL (2014) Antarctic lakes. Oxford University Press, OxfordCrossRefGoogle Scholar
  78. Laybourn-Parry J, Walton M, Young J, Jones RI, Shine A (1994) Protozooplankton and bacterioplankton in a large oligotrophic lake—Loch Ness, Scotland. J Plankton Res 16:1655–1670CrossRefGoogle Scholar
  79. Laybourn-Parry J, Bayliss P, Ellis-Evans JC (1995) The dynamics of heterotrophic nanoflagellates and bacterioplankton in a large ultra-oligotrophic Antarctic lake. J Plankton Res 17:1835–1850CrossRefGoogle Scholar
  80. Laybourn-Parry J, Quayle W, Henshaw T (2002) The biology and evolution of Antarctic saline lakes in relation to salinity and trophy. Polar Biol 25:542–552CrossRefGoogle Scholar
  81. Laybourn-Parry J, Henshaw T, Jones DJ, Quayle W (2004) Bacterioplankton production in freshwater Antarctic lakes. Freshw Biol 49:735–744CrossRefGoogle Scholar
  82. Laybourn-Parry J, Marshall WA, Marchant HJ (2005) Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes. Freshw Biol 50:830–838CrossRefGoogle Scholar
  83. Laybourn-Parry J, Madan NJ, Marshall WA, Marchant HJ, Wright SW (2006) Carbon dynamics in an ultra-oligotrophic epishelf lake (Beaver Lake, Antarctica) in summer. Freshw Biol 51:1116–1130CrossRefGoogle Scholar
  84. Laybourn-Parry J, Marshall WJ, Madan NJ (2007) Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol 30:351–358CrossRefGoogle Scholar
  85. Laybourn-Parry J, Tranter M, Hodson AJ (2010) The ecology of snow and ice environments. Oxford University Press, OxfordGoogle Scholar
  86. Lisle JT, Priscu JC (2004) The occurrence of lysogenic bacteria and microbial aggregates in the lakes of the McMurdo Dry Valleys, Antarctica. Microb Ecol 47:427–439PubMedCrossRefGoogle Scholar
  87. Logares R, Lindström ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S (2012) Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J 7:937–948PubMedPubMedCentralCrossRefGoogle Scholar
  88. Lymer DJB, Logue CPD, Brussard A-C, Baudoux K, Vrede K, Lindström ES (2008) Temporal variation in freshwater viral and bacterial community composition. Freshw Biol 53:1163–1175CrossRefGoogle Scholar
  89. Madan NJ, Marshall WA, Laybourn-Parry J (2005) Virus and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshw Biol 50:1291–1300CrossRefGoogle Scholar
  90. Mancuso CA, Franzmann PD, Burton HR, Nichols PD (1990) Microbial community structure and biomass estimates of a methanogenic Antarctic lake ecosystem as determined by phospholipid analysis. Microb Ecol 19:73–95PubMedCrossRefGoogle Scholar
  91. Marshall WA (1996) Biological particles over Antarctica. Nature 383:680CrossRefGoogle Scholar
  92. Marshall WA, Laybourn-Parry J (2002) The balance between photosynthesis and grazing in Antarctic mixotrophic cryptophytes during summer. Freshw Biol 47:2060–2070CrossRefGoogle Scholar
  93. Matsumoto GI (1989) Biogeochemical study of organic-substances in Antarctic lakes. Hydrobiologia 172:265–289CrossRefGoogle Scholar
  94. McCammon SA, Bowman JP (2000) Taxonomy of Antarctic Flavobacterium species: description of Flavobacterium gillisiae sp. nov., Flavobacterium tegetincola sp. nov. and Flavobacterium xanthum sp.nov. review and reclassification of (Flavobacterium) salegans as Salegentibacter salegens gen. nov., comb. nov. Int J Syst Evol Microbiol 50:1055–1063PubMedCrossRefGoogle Scholar
  95. McCammon SA, Innes BH, Bowman JP, Franzmann PD, Dobson SJ, Holloway PE, Skerratt JH, Nicols PD, Rankin JL (1998) Flavobacterium hibernum sp. nov. a lacose utilizing bacterium from a freshwater Antarctic lake. Int J Syst Evol Microbiol 48:1405–1412Google Scholar
  96. McKnight DM, Aiken GR, Smith RL (1991) Aquatic fulvic-acids in microbially based ecosystems—results from two desert lakes in Antarctica. Limnol Oceanogr 36:998–1006CrossRefGoogle Scholar
  97. McMeekin TA, Franzmann PD (1988) Effect of temperature on the growth rates of halotolerant and halophilic bacteria isolated from Antarctic saline lakes. Polar Biol 8:281–285CrossRefGoogle Scholar
  98. Michaud L, Caruso C, Mangano S, Interdonato F, Bruni V, Lo Giudice A (2012) Predominance of Flavobacterium, Pseudomonas, and Polaromonas within the prokaryotic community of freshwater shallow lakes in the northern Victoria Land, East Antarctica. FEMS Microbiol Ecol 82:391–404PubMedCrossRefGoogle Scholar
  99. Mondino LJ, Asao M, Madigan MT (2009) Cold-active halophilic bacteria from halophytic bacteria from the ice-sealed Lake Vida, Antarctica. Arch Microbiol 191:785–790PubMedCrossRefGoogle Scholar
  100. Murray AE, Kenig F, Fritsen CH, McKay CP, Cawley KM, Edwards R, Kuhn E, McKnight DM, Ostrom NE, Peng V, Ponce A, Priscu JC, Samarkin V, Townsend AT, Wagh P, Young SA, Yungg PT, Doran PT (2012) Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake. PNAS 109:20626–20631PubMedPubMedCentralCrossRefGoogle Scholar
  101. Naganuma T, Hua PN, Okamoto T, Ban S, Imura S, Kanda H (2005) Depth distribution of euryhaline bacteria in Suribati Ike, a meromictic lke in East Antarctica. Polar Biol 12:964–970CrossRefGoogle Scholar
  102. Ng C, Demaere MZ, Williams TJ, Lauro FM, Raftery M, Gibson JAE, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Thomas T, Cavicchioli R (2010) Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake, Antarctica. ISME J 4:1002–1019PubMedCrossRefGoogle Scholar
  103. O’Brien WJ, Bahr M, Hershey AE, Hobbie JE, Kipphut GW, Kling GW, Kling H, McDonald M, Miller MC, Rublee P, Vestal JR (1997) The limnology of Toolik Lake. In: Milner AM, Oswood MW (eds) Freshwaters of Alaska. Springer, New York, pp 61–106CrossRefGoogle Scholar
  104. Oswald GKA, Robin GQ (1973) Lakes beneath the Antarctic ice sheet. Nature 245:251–254CrossRefGoogle Scholar
  105. Overmann J, Beatty JT, Hall KJ (1996) Purple sulfur bacterial control the growth of aerobic heterotrophic bacterioplankton in a meromictic salt lake. Appl Environ Microbiol 62:3251–3258PubMedPubMedCentralGoogle Scholar
  106. Panzenböck M, Möbes-Hansen B, Albert R, Herndl GJ (2000) Dynamics of phyto- and bacterioplankton in a high Arctic lake on Franz Joseph Land archipelago. Aquat Microb Ecol 21:265–273CrossRefGoogle Scholar
  107. Pearce DA (2003) Bacterioplankton community structure in a maritime Antarctic oligotrophic lake during a period of holomixis, as determined by denaturing gradient gel electrophoresis (DGGE) and fluorescence in situ hybridisation (FISH). Microb Ecol 46(1):92–105PubMedCrossRefGoogle Scholar
  108. Pearce DA (2005) The structure and stability of the bacterioplankton community in Antarctic freshwater lakes, subject to extremely rapid environmental change. FEMS Microbiol Ecol 53:61–72PubMedCrossRefGoogle Scholar
  109. Pearce DA, van der Gast C, Lawley B, Ellis-Evans JC (2003) Bacterioplankton community diversity in a maritime Antarctic lake, as determined by culture dependent and culture independent techniques. FEMS Microbiol Ecol 45:59–70PubMedCrossRefGoogle Scholar
  110. Pearce DA, van der Gast CJ, Woodward K, Newsham KK (2005) Significant changes in the bacterioplankton community structure of a maritime Antarctic freshwater lake following nutrient enrichment. Microbiology 151:3237–3248PubMedCrossRefGoogle Scholar
  111. Peeters K, Hodgson DA, Convey P, Willems A (2011) Culturable diversity of heterotrophic bacteria in Forlidas Pond (Pensacola Mountains) and Lundström Lake (Shackleton Range), Antarctica. Microb Ecol 62:399–413PubMedCrossRefGoogle Scholar
  112. Peeters K, Verleyen E, Hodgson DA, Convey P, Ertz D, Vyverman W, Willems A (2012) Heterotrophic bacterial diversity in aquatic microbial mat communities from Antarctica. Polar Biol 35:543–554CrossRefGoogle Scholar
  113. Pick FR, Caron DA (1987) Picoplankton and nanoplankton biomass in Lake Ontario: relative contribution of phototrophic and heterotrophic communities. Can J Fish Aquat Sci 44:2164–2172CrossRefGoogle Scholar
  114. Porazinska DL, Fountain AG, Nylen TH, Tranter M, Virginia RA, Wall DH (2004) The biodiversity and biogeochemistry of cryoconite holes from McMurdo Dry Valley glaciers, Antarctica. Arct Antarct Alp Res 36:84–91CrossRefGoogle Scholar
  115. Priscu JC, Priscu LR, Vincent WF, Howard-Williams C (1987) Photosynthate distribution by microplankton in permanently ice-covered Antarctic desert lakes. Limnol Oceanogr 32:260–270CrossRefGoogle Scholar
  116. Priscu JC, Fritsen CH, Adams EE, Giovannoni SJ, Paerl HW, McKay CP, Doran PT, Gordon DA, Lanoil BD, Pinckney JL (1998) Perennial Antarctic lake ice: an oasis for life in a polar desert. Science 280:2095–2098PubMedCrossRefGoogle Scholar
  117. Priscu JC, Adams EE, Lyons WB, Voytek MA, Mogk DW, Brown RL, McKay CP, Takacs CD, Welch KA, Wolf CF, Kirshtein CD, Avci R (1999) Geomicrobiology of subglacial ice above Lake Vostok, Antarctica. Science 286:2141–2144PubMedCrossRefGoogle Scholar
  118. Quayle WC, Peck LS, Peat H, Ellis-Evans JC, Harrigan PR (2002) Extreme responses to climate change in Antarctic lakes. Science 295:645PubMedCrossRefGoogle Scholar
  119. Rankin LM, Gibson JAE, Franzmann PD, Burton HR (1999) The chemical stratification and microbial communities of Ace Lake, Antarctica: a review of the characteristics of a marine-derived meromictic lake. Polarforschung 66:33–52Google Scholar
  120. Riemann B, Bell RT (1990) Advances in estimating bacterial biomass and growth in aquatic systems. Arch Hydrobiol 118:385–402Google Scholar
  121. Roberts EC, Laybourn-Parry J (1999) Mixotrophic cryptophytes and their predators in the Dry Valley lakes of Antarctica. Freshw Biol 41:737–746CrossRefGoogle Scholar
  122. Roberts EC, Priscu JC, Laybourn-Parry J (2004) Microplankton dynamics in a perennially ice-covered Antarctic lake—Lake Hoare. Freshw Biol 49:853–869CrossRefGoogle Scholar
  123. Rodrigues DF, de Jesus E, Ayala-del-Río HL, Pellizari VH, Gilichinsky D, Sepulveda-Torres L, Tiedje JM (2009) Biogeography of two cold-adapted genera: Psychrobacter and Exiguobacterium. ISME J 3:658–665PubMedCrossRefGoogle Scholar
  124. Romina Schiaffino M, Unrein F, Gasol JM, Massana R, Balagué V, Izaguirre I (2011) Bacterial community structure in a latitudinal gradient of lakes: the roles of spatial versus environmental factors. Freshw Biol 56:1973–1991CrossRefGoogle Scholar
  125. Sattley WM, Madigan MT (2006) Isolation, characterization, and ecology of cold-active, chemolithotrophic, sulfur-oxidizing bacteria from perennially ice-covered Lake Fryxell, Antarctica. Appl Environ Microbiol 72:5562–5568PubMedPubMedCentralCrossRefGoogle Scholar
  126. Saunders NF, Thomas T, Curmi PM, Mattick JS, Kuczek E, Slade R, Davis J, Franzmann PD, Boone D, Rusterholtz K, Feldman R, Gates C, Bench S, Sowers K, Kadner K, Aerts A, Dehal P, Detter C, Glavina T, Lucas S, Richardson P, Larimer F, Hauser L, Cavicchioli R (2003) Mechanisms of thermal adaptation revealed from the genomes of the Antarctic Archaea Methanogenium frigidum and Methanococcoides burtonii. Genome Res 13:1580–1588PubMedPubMedCentralCrossRefGoogle Scholar
  127. Säwström C, Anesio AM, Granéli W, Laybourn-Parry J (2007a) Seasonal viral loop dynamics in two large ultra-oligotrophic Antarctic freshwater lakes. Microb Ecol 53:1–11PubMedCrossRefGoogle Scholar
  128. Säwström C, Granéli W, Laybourn-Parry J, Anesio AM (2007b) High viral infection rates in Antarctic and Arctic bacterioplankton. Environ Microbiol 9:250–255PubMedCrossRefGoogle Scholar
  129. Säwström C, Laybourn-Parry J, Anesio AM, Priscu JC, Lisle J (2008) Bacteriophage in polar inland waters. Extremophiles 12:167–175PubMedCrossRefGoogle Scholar
  130. Säwström C, Karlson J, Laybourn-Parry J, Granéli W (2009) Zooplankton feeding on algae and bacteria under ice in Lake Druzhby, East Antarctica. Polar Biol 32:1195–1202CrossRefGoogle Scholar
  131. Scavia D, Laird GA, Fahnenstiel GL (1986) Production of planktonic bacteria in Lake Michigan. Limnol Oceanogr 31:612–626CrossRefGoogle Scholar
  132. Schiaffino MR, Unrein F, Gasol JM, Farias ME, Estevez C, Balagué V, Izaguirre I (2009) Comparative analysis of bacterioplankton assemblages from maritime Antarctic freshwater lakes with contrasting trophic status. Polar Biol 32:923–936CrossRefGoogle Scholar
  133. Siegert MJ, Ross N, Le Brocq AM (2016) Recent advances in understanding Antarctic subglacial lakes and hydrology. Philos Trans R Soc A 374:20140306. doi: 10.1098/rsta.2014.0306 CrossRefGoogle Scholar
  134. Simek K, Horñák K, Jezbera J, Nedoma J, Vrba J, Straskrábová V, Macek M, Dolan JR, Hahn WH (2006) Maximum growth rates and possible life strategies of different bacterioplankton groups in relation to phosphorus availability in a freshwater reservoir. Environ Microbiol 8:1613–1624PubMedCrossRefGoogle Scholar
  135. Smith RIL (1988) Destruction of Antarctic terrestrial ecosystems by a rapidly increasing fur seal population. Biol Conserv 45:55–72CrossRefGoogle Scholar
  136. Smith JA, Hodgson DA, Bentle MJ, Verleyen E, Leng MJ, Roberts SJ (2006) Limnology of two Antarctic epishelf lakes and their potential to record periods of ice shelf loss. J Paleolimnol 35:373–394CrossRefGoogle Scholar
  137. Smith BE, Fricker HA, Joughin IR, Tulaczyk S (2009) An inventory of active subglacial lakes in Antarctica detected by Icesat (2003–2008). J Glaciol 55:573–595CrossRefGoogle Scholar
  138. Snauwaert I, Hoste B, De Bruyne K, Peeters K, De Vuyst L, Willems A, Vandamme P (2013) Carnobacterium iners sp. nov., a psychrophilic, lactic acid-producing bacterium from the littoral zone of an Antarctic pond. Int J Syst Evol Microbiol 63:1370–1375PubMedCrossRefGoogle Scholar
  139. Stingl U, Foo W, Vergin KL, Lanoil B, Giovannoni SJ (2008) Dilution-top-extinction culturing of psychrotolerant planktonic bacteria from permanently ice-covered lakes in the McMurdo Dry Valleys, Antarctica. Microb Ecol 55:395–405PubMedCrossRefGoogle Scholar
  140. Sundh I, Bell RT (1992) Extracellular dissolved organic carbon released from phytoplankton as a source of carbon for heterotrophic bacteria in lakes of different humic content. Hydrobiologia 229:93–106CrossRefGoogle Scholar
  141. Takacs CD, Priscu JC (1998) Bacterioplankton dynamics in the McMurdo Dry Valley lakes, Antarctica: production and biomass over four seasons. Microb Ecol 36:239–250PubMedCrossRefGoogle Scholar
  142. Takacs CD, Priscu JC, McKnight DM (2001) Bacterial dissolved organic carbon demand in McMurdo Dry valley lakes, Antarctica. Limnol Oceanogr 46:1189–1194CrossRefGoogle Scholar
  143. Tang C, Madigan MT, Lanoil B (2013) Bacterial and archaeal diversity in sediments of west Lake Bonney, McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 79:1034–1038PubMedPubMedCentralCrossRefGoogle Scholar
  144. Telling J, Anesio AM, Tranter M, Fountain AG, Nylen T, Hawkings J, Singh VB, Kaur P, Wadham GL (2014) Spring thaw ionic pulses boost nutrient availability and microbial growth in entombed Antarctic Dry Valley cryoconite holes. Front Microbiol. doi: 10.3389/fmicb.2014.00694 PubMedPubMedCentralGoogle Scholar
  145. Thurman J, Parry J, Hill PJ, Laybourn-Parry J (2010) The filer-feeding ciliates Colpidium striatum and Tetrahymena pyriformis display selective feeding behaviours in the presence of mixed, equally sized, bacterial prey. Protist 161:577–588PubMedCrossRefGoogle Scholar
  146. Thurman J, Parry J, Hill PJ, Priscu JC, Vick TJ, Chiuchiolo A, Laybourn-Parry J (2012) Microbial dynamics and flagellate grazing rates during transition to winter in Lakes Hoare and Bonney, Antarctica. FEMS Microbiol Ecol 82:449–458PubMedCrossRefGoogle Scholar
  147. Tindall BJ, Brambilla E, Steffan M, Neumann R, Pukall R, Kroppenstedt RM, Stackebrandt E (2000) Cultivatable microbial biodiversity: gnawing at the Gordian knot. Environ Microbiol 2:310–318PubMedCrossRefGoogle Scholar
  148. Tominaga H, Fukui F (1981) Saline lakes at Syowa Oasis, Antarctica. Hydrobiologia 82:375–389CrossRefGoogle Scholar
  149. Toolan T, Wehr JD, Findlay S (1991) Inorganic phosphorus stimulation of bacterioplankton production in a meso-eutrophic lake. Appl Environ Microbiol 57:2074–2078PubMedPubMedCentralGoogle Scholar
  150. Van Trappen S, Mergaert J, Van Eygen S, Dawyndt P, Cnockaert MC, Swings J (2002) Diversity of 746 heterotrophic bacteria isolated from microbial mats from ten Antarctic lakes. Syst Appl Microbiol 25:603–610PubMedCrossRefGoogle Scholar
  151. Van Trappen S, Vandecandelaere I, Mergaert J, Swings J (2004) Flavobacterium degerlachei sp. nov., Flavobacterium frigoris sp. nov. and Flavobacterium micromati sp. nov., novel psychrophilic bacteria isolated from microbial mats in Antarctic lakes. Int J Syst Evol Microbiol 54:85–92PubMedCrossRefGoogle Scholar
  152. Vander Schaaf NA, Cunningham AMG, Cluff BP, Kraemer CK, Reeves CL, Riester CJ, Slater LK, Madigan MT, Sattley WM (2015) Cold-adapted, heterotrophic bacteria from the highly oligotrophic waters of Lake Vanda, Antarctica. Microorganisms 3:391–406PubMedPubMedCentralCrossRefGoogle Scholar
  153. Vaqué D, Pace ML (1992) Grazing on bacteria by flagellates and cladocerans in lakes of contrasting food web structure. J Plankton Res 14:307–321CrossRefGoogle Scholar
  154. Villaescusa JA, Casamayor EO, Rochera C, Velázquez D, Chicote Á, Quesada A, Camacho A (2010) A close link between bacterial community composition and environmental heterogeneity in maritime Antarctic lakes. Int Microbiol 13:67–77PubMedGoogle Scholar
  155. Vincent WF (1981) Production strategies in Antarctic inland waters: phytoplankton ecophysiology in a permanently ice-covered lake. Ecology 62:1215–1224CrossRefGoogle Scholar
  156. Vincent WF, Hobbie JE, Laybourn-Parry J (2008) Introduction to the limnology of high-latitude lake and river ecosystems. In: Vincent WF, Laybourn-Parry J (eds) Polar lakes and rivers, limnology of Arctic and Antarcyic aquatic ecosystems. Oxford University Press, Oxford, pp 1–18CrossRefGoogle Scholar
  157. Vrede K (2005) Nutrient and temperature limitation of bacterioplankton growth in temperate lakes. Microb Ecol 49:245–256PubMedCrossRefGoogle Scholar
  158. Vrede K, Vrede T, Isaksson A, Karlsson A (1999) Effects of nutrient (phosphorus, nitrogen and carbon) and zooplankton on bacterioplankton and phytoplankton—a seasonal study. Limnol Oceanogr 44:1616–1624CrossRefGoogle Scholar
  159. Ward BB, Granger J, Maldonado MT, Wells ML (2003) What limits bacterial production in the suboxic region of permanently ice-covered Lake Bonney, Antarctica? Aquat Microb Ecol 31:33–47CrossRefGoogle Scholar
  160. Webster-Brown J, Gall M, Gibson J, Wood S, Hawes I (2010) The biogeochemistry of meltwater habitats in the Darwin Glacier region (80°S). Victoria Land, Antarctica. Antarct Sci 22:646–661CrossRefGoogle Scholar
  161. Weinbauer MG, Höfle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl Environ Microbiol 64:431–438PubMedPubMedCentralGoogle Scholar
  162. Xiao X, Yin X, Lin L, Sun L, You Z, Wang P, Wang F (2005) Chitinase genes in lake sediments of Ardley Island, Antarctica. Appl Environ Microbiol 71:7904–7909PubMedPubMedCentralCrossRefGoogle Scholar
  163. Yau S, Lauro FM, Williams TJ, DeMaere MZ, Brown MV, Rich J, Gibson JAE, Cavicchioli R (2013) Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake. ISME J 7:1944–1961PubMedPubMedCentralCrossRefGoogle Scholar
  164. Zwart D, Bird M, Stone J, Lambeck K (1998) Holocene sea-level change and ice-sheet history in the Vestfold Hills, East Antarctica. Earth Planet Sci Lett 155:131–145CrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Bristol Glaciology Centre, School of Geographical SciencesUniversity of BristolBristolUK
  2. 2.School of Applied ScienceUniversity of NorthumbriaNewcastle-upon-TyneUK

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