Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Microbial ecology of Antarctic aquatic systems

Nature Reviews Microbiology volume 13, pages 691–706 (2015)Cite this article

Subjects

An Erratum to this article was published on 20 October 2015

This article has been updated

Key Points

  • The application of 'omic' approaches (for example, pyrosequencing, metagenomics, metatranscriptomics and metaproteomics) has generated unprecedented insight into Antarctic microorganisms and revealed intriguing properties about communities that can be linked to their Antarctic-specific habitats.

  • Community composition and ecosystem function are controlled by the polar light regime, biotic and abiotic environmental factors, limnological history and seed populations, biogeography and the limits of aeolian and advective dispersal caused by physical barriers and distance between sites, and perturbation caused by ecosystem change.

  • The polar austral summer is characterized by continuous high solar irradiance, which stimulates phototrophic growth and kinetically accelerates growth. Such communities tend to be oriented towards maximizing the effectiveness of light energy while switching to light-independent processes (for example, chemolithoautotrophy, phagotrophy and heterotrophic utilization of storage compounds) to survive the cold, dark winter.

  • Virus–host interactions are particularly important in the Antarctic food web, in which they not only control remineralization and influence community composition but have unanticipated roles in influencing productivity cycles. Discoveries pertaining to viruses have included systems with a high diversity of novel eukaryotic viruses, phage-resistant bacteria, and archaea capable of evading, defending against and adapting to viruses.

  • Unusual biogeochemical cycles have developed as a result of communities evolving in very specific, local environments. The indigenous communities have developed a range of traits, including a hierarchical structure, low complexity, niche adaptation, clonal dominance, mixotrophy and short-circuited nutrient cycles that enhance the use and conservation of resources.

  • Specific taxa have a major influence on overall ecosystem function, with stability of those biomes being reliant on the key, specialized and fit members maintaining function and not being affected by ecosystem perturbation, particularly anthropocentric climate change and the introduction of alien species.

Abstract

The Earth's biosphere is dominated by cold environments, and the cold biosphere is dominated by microorganisms. Microorganisms in cold Southern Ocean waters are recognized for having crucial roles in global biogeochemical cycles, including carbon sequestration, whereas microorganisms in other Antarctic aquatic biomes are not as well understood. In this Review, I consider what has been learned about Antarctic aquatic microbial ecology from 'omic' studies. I assess the factors that shape the biogeography of Antarctic microorganisms, reflect on some of the unusual biogeochemical cycles that they are associated with and discuss the important roles that viruses have in controlling ecosystem function.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Overview of Antarctica.
Figure 2: Vestfold Hills lakes.
Figure 3: McMurdo Dry Valleys lakes.
Figure 4: Unusual Antarctic biogeochemistry.
Figure 5: Overview of Antarctic lake ecology.

Similar content being viewed by others

Change history

  • 20 October 2015

    In the above article, there were two spelling errors. The credit line for Figure 2e should read: "Image of Deep Lake courtesy of M. Milnes, Australian Antarctic Division." The acknowledgments should read: “The author is indebted to ... M. Milnes ... for providing images of Antarctic lakes...” These have now been corrected in the online version of the article. We apologize to the readers for any misunderstanding caused.

References

  1. Wilkins, D. et al. Key microbial drivers in Antarctic aquatic environments. FEMS Microl. Rev. 37, 303–335 (2013). Useful compendium of molecular-based studies of Antarctic aquatic microorganisms.

    Article  CAS  Google Scholar 

  2. Chown, S. L. et al. Challenges to the future conservation of the Antarctic. Science 337, 158–159 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Chown, S. L. et al. The changing form of Antarctic biodiversity. Nature 522, 431–438 (2015).

    Article  CAS  PubMed  Google Scholar 

  4. Joughin, I., Smith, B. E. & Medley, B. Marine ice sheet collapse potentially under way for the Thwaites Glacier Basin, West Antarctica. Science 344, 735–738 (2014).

    Article  CAS  PubMed  Google Scholar 

  5. Wouters, B. et al. Glacier mass loss. Dynamic thinning of glaciers on the Southern Antarctic Peninsula. Science 348, 899–903 (2015).

    Article  CAS  PubMed  Google Scholar 

  6. Sen Gupta, A. et al. Projected changes to the Southern Hemisphere Ocean and sea ice in the IPCC AR4 climate models. J. Climate 22, 3047–3078 (2009).

    Article  Google Scholar 

  7. Capotondi, A., Alexander, M. A., Bond, N. A., Curchitser, E. N. & Scott, J. D. Enhanced upper ocean stratification with climate change in the CMIP3 models. J. Geophys. Res. 117, C04031 (2012).

    Article  Google Scholar 

  8. McNeil, B. I. & Matear, R. J. Southern Ocean acidification: a tipping point at 450-ppm atmospheric CO2 . Proc. Natl Acad. Sci. USA 105, 18860–18864 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Le Quéré, C. et al. Saturation of the Southern Ocean CO2 sink due to recent climate change. Science 136, 1735–1738 (2007).

    Article  CAS  Google Scholar 

  10. Frölicher, T. L. et al. Dominance of the Southern Ocean in anthropogenic carbon and heat uptake in CMIP5 models. J. Climate 28, 862–886 (2015).

    Article  Google Scholar 

  11. Falkowski, P. Ocean science: the power of plankton. Nature 483, S17–S20 (2012).

    Article  CAS  PubMed  Google Scholar 

  12. Cary, S. C., McDonald, I. R., Barrett, J. E. & Cowan, D. A. On the rocks: the microbiology of Antarctic Dry Valley soils. Nat. Rev. Microbiol. 8, 129–138 (2010). Insightful review describing soil and rock microbial communities in the McMurdo Dry Valleys.

    Article  CAS  PubMed  Google Scholar 

  13. Cowan, D. A. & Tow, L. A. Endangered Antarctic environments. Annu. Rev. Microbiol. 58, 649–690 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Murray, A. & Grzymski, J. Diversity and genomics of Antarctic marine microorganisms. Phil. Trans. R. Soc. B 362, 2259–2271 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Laybourn-Parry, J. No place too cold. Science 324, 1521–1522 (2009).

    Article  CAS  PubMed  Google Scholar 

  16. Feller, G. & Gerday, C. Psychrophilic enzymes: hot topics in cold adaptation. Nat. Rev. Microbiol. 1, 200–208 (2003).

    Article  CAS  PubMed  Google Scholar 

  17. Cavicchioli, R. Cold adapted Archaea. Nat. Rev. Microbiol. 4, 331–343 (2006).

    Article  CAS  PubMed  Google Scholar 

  18. Margesin, R. & Miteva, V. Diversity and ecology of psychrophilic microorganisms. Res. Microbiol. 162, 346–361 (2011).

    Article  PubMed  Google Scholar 

  19. Siddiqui, K. S. et al. Psychrophiles. Annu. Rev. Earth Planet. Sci. 41, 87–115 (2013).

    Article  CAS  Google Scholar 

  20. De Maayer, P., Anderson, D., Cary, C. & Cowan, D. A. Some like it cold: understanding the survival strategies of psychrophiles. EMBO Rep. 15, 508–517 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Jansson, J. & Tas, N. The microbial ecology of permafrost. Nat. Rev. Microbiol. 12, 414–425 (2014).

    Article  CAS  PubMed  Google Scholar 

  22. Boetius, A., Anesio, A. M., Deming, J. W., Mikucki, J. & Rapp, J. Z. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat. Rev. Microbiol. 13, 677–690 (2015).

    Article  CAS  PubMed  Google Scholar 

  23. Williams, T. J. et al. The role of planktonic Flavobacteria in processing algal organic matter in coastal East Antarctica revealed using metagenomics and metaproteomics. Environ. Microbiol. 15, 1302–1317 (2013).

    Article  CAS  PubMed  Google Scholar 

  24. Williams, T. J. & Cavicchioli, R. Marine metaproteomics: deciphering the microbial metabolic food web. Trends Microbiol. 22, 248–260 (2014).

    Article  CAS  PubMed  Google Scholar 

  25. Rahmstorf, S. Thermohaline circulation: the current climate. Nature 421, 699 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Matsumoto, K. Radiocarbon-based circulation age of the world oceans. J. Geophys. Res. 112, C09004 (2007).

    Google Scholar 

  27. Zika, J. D., England, M. H. & Sijp, W. P. The ocean circulation in thermohaline coordinates. J. Phys. Oceanogr. 42, 708–724 (2012).

    Article  Google Scholar 

  28. Ballarotta, M., Falahat, S., Brodeau, L. & Döös, K. On the glacial and interglacial thermohaline circulation and the associated transports of heat and freshwater. Ocean Sci. 10, 907–921 (2014).

    Article  Google Scholar 

  29. Ghiglione, J.-F. et al. Pole-to-pole biogeography of surface and deep marine bacterial communities. Proc. Natl Acad. Sci. USA 109, 17633–17638 (2012). Insightful study teasing apart the roles of isolation and ocean connectivity in influencing the distribution of microbial communities in polar ocean waters.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Sul, W. J., Oliver, T. A., Ducklow, H. W., Amaral-Zettler, L. A. & Sogin, M. L. Marine bacteria exhibit a bipolar distribution. Proc. Natl Acad. Sci. USA 110, 2342–2347 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Wilkins, D., van Sebille, E., Rintoul, S. R., Lauro, F. M. & Cavicchioli, R. Advection shapes Southern Ocean microbial assemblages independent of distance and environment effects. Nat. Commun. 4, 2457 (2013). First study to demonstrate that physical transport shapes marine microbial assemblages and should therefore be considered in the ecology and biogeography of marine microorganisms.

    Article  PubMed  CAS  Google Scholar 

  32. Fuhrman, J. A. et al. A latitudinal diversity gradient in planktonic marine bacteria. Proc. Natl Acad. Sci. USA 105, 7774–7778 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Galand, P. E., Potvin, M., Casamayor, E. O. & Lovejoy, C. Hydrography shapes bacterial biogeography of the deep Arctic Ocean. Nature 4, 564–576 (2009).

    Google Scholar 

  34. Lauro, F. M., Chastain, R. A., Blankenship, L. E., Yayanos, A. A. & Bartlett, D. H. The unique 16S rRNA genes of piezophiles reflect both phylogeny and adaptation. Appl. Env. Microbiol. 73, 838–845 (2007).

    Article  CAS  Google Scholar 

  35. Giebel, H.-A., Brinkhoff, T., Zwisler, W., Selje, N. & Simon, M. Distribution of Roseobacter RCA and SAR11 lineages and distinct bacterial communities from the subtropics to the Southern Ocean. Environ. Microbiol. 11, 2164–2178 (2009).

    Article  CAS  PubMed  Google Scholar 

  36. Sabine, C. L. et al. The oceanic sink for anthropogenic CO2 . Science 305, 367–371 (2004).

    Article  CAS  PubMed  Google Scholar 

  37. Mikaloff Fletcher, S. E. et al. Inverse estimates of anthropogenic CO2 uptake, transport, and storage by the ocean. Global Biogeochem. Cy. 20, GB2002 (2006).

    Article  CAS  Google Scholar 

  38. Gruber, N. et al. Oceanic sources, sinks, and transport of atmospheric CO2 . Global Biogeochem. Cy. 23, GB1005 (2009).

    Article  CAS  Google Scholar 

  39. Thomalla, S. J. et al. Phytoplankton distribution and nitrogen dynamics in the southwest Indian subtropical gyre and Southern Ocean waters. Ocean Sci. 7, 113–127 (2011).

    Article  CAS  Google Scholar 

  40. Wilkins, D. et al. Biogeographic partitioning of Southern Ocean microorganisms revealed by metagenomics. Environ. Microbiol. 15, 1318–1333 (2013).

    Article  CAS  PubMed  Google Scholar 

  41. Brown, M. V. et al. Global biogeography of SAR11 marine bacteria. Mol. Syst. Biol. 8, 595 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Selje, N., Simon, M. & Brinkhoff, T. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427, 445–448 (2004).

    Article  CAS  PubMed  Google Scholar 

  43. Gianoulis, T. A. et al. Quantifying environmental adaptation of metabolic pathways in metagenomics. Proc. Natl Acad. Sci. USA 106, 1374–1379 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Barton, A. D., Dutkiewicz, S., Flierl, G., Bragg, J. & Follows, M. J. Patterns of diversity in marine phytoplankton. Science 327, 1509–1511 (2010).

    Article  CAS  PubMed  Google Scholar 

  45. Jiang, X. et al. Functional biogeography of ocean microbes revealed through non-negative matrix factorization. PLoS ONE 7, e43866 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Thomas, M. K., Kremer, C. T., Klausmeier, C. A. & Litchman, E. A global pattern of thermal adaptation in marine phytoplankton. Science 338, 1085–1088 (2012).

    Article  CAS  PubMed  Google Scholar 

  47. Swan, B. K. et al. Prevalent genome streamlining and latitudinal divergence of surface ocean bacterioplankton. Proc. Natl Acad. Sci. USA 110, 11463–11468 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Womack, A. M., Bohannan, B. J. & Green, J. L. Biodiversity and biogeography of the atmosphere. Phil. Trans. R. Soc. B 365, 3645–3653 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Baas Becking, L. G. M. Geobiologie Of Inleiding Tot De Milieukunde (W. P. Van Stockum & Zoon, 1934) (in Dutch).

    Google Scholar 

  50. Wynn-Williams, D. D. Aerobiology and colonization in Antarctica — the BIOTAS Programme. Grana 30, 380–393 (1991).

    Article  Google Scholar 

  51. de Wit, R. & Bouvier, T. 'Everything is everywhere, but, the environment selects'; what did Baas Becking and Beijerinck really say? Environ. Microbiol. 8, 755–758 (2006).

    Article  PubMed  Google Scholar 

  52. Martiny, J. B. H. et al. Microbial biogeography: putting microorganisms on the map. Nat. Rev. Microbiol. 4, 102–112 (2006).

    Article  CAS  PubMed  Google Scholar 

  53. Hanson, C. A., Fuhrman, J. A., Horner-Devine, M. C. & Martiny, J. B. H. Beyond biogeographic patterns: processes shaping the microbial landscape. Nat. Rev. Microbiol. 10, 497–506 (2012). Excellent description of the mechanisms involved in shaping the biogeography of microbial communities.

    Article  CAS  PubMed  Google Scholar 

  54. Herbold, C. W., Lee, C. K., McDonald, I. R. & Cary, S. C. Evidence of global-scale aeolian dispersal and endemism in isolated geothermal microbial communities of Antarctica. Nat. Commun. 5, 3875 (2014).

    Article  CAS  PubMed  Google Scholar 

  55. Knowlton, C., Veerapaneni, R., D'Elia, T. & Rogers, S. O. Microbial analyses of ancient ice core sections from Greenland and Antarctica. Biology (Basel) 2, 206–232 (2013).

    CAS  PubMed Central  Google Scholar 

  56. Morgan-Kiss, R. M., Priscu, J. C., Pocock, T., Gudynaite-Savitch, L. & Huner, N. P. Adaptation and acclimation of photosynthetic microorganisms to permanently cold environments. Microbiol. Mol. Biol. Rev. 70, 222–252 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Jungblut, A. D., Lovejoy, C. & Vincent, W. F. Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J. 4, 191–202 (2010). Interesting study rationalizing the dispersal and selection of polar-distributed cyanobacteria, which formed the foundation for subsequent metagenomic studies.

    Article  CAS  PubMed  Google Scholar 

  58. Varin, T., Lovejoy, C., Jungblut, A. D., Vincent, W. F. & Corbeil, J. Metagenomic analysis of stress genes in microbial mat communities from Antarctica and the High Arctic. Appl. Environ. Microbiol. 78, 549–559 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Gibson, J. A. E. The meromictic lakes and stratified marine basins of the Vestfold Hills, East Antarctica. Antarct. Sci. 11, 175–192 (1999).

    Article  Google Scholar 

  60. Ng, C. et al. Metaproteogenomic analysis of a dominant green sulfur bacterium from Ace Lake, Antarctica. ISME J. 4, 1002–1019 (2010). First Antarctic metaproteomics study describing an almost complete metagenome-derived genome sequence and high metaproteome coverage of an ecologically important lake microorganism.

    Article  CAS  PubMed  Google Scholar 

  61. Lauro, F. M. et al. An integrative study of a meromictic lake ecosystem in Antarctica. ISME J. 5, 879–895 (2011). First shotgun metagenomics and metaproteomics study describing the identity and functional capacity of microbial populations throughout an entire lake, including a mathematical model describing the effects of environmental parameters on key populations.

    Article  CAS  PubMed  Google Scholar 

  62. Rankin, L. M., Gibson, J. A. E., Franzmann, P. D. & Burton, H. R. The chemical stratification and microbial communities of Ace Lake, Antarctica: a review of the characteristics of a marine-derived meromictic lake. Polarforschung 66, 35–52 (1999).

    Google Scholar 

  63. Sowell, S. M. et al. Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J. 3, 93–105 (2009).

    Article  CAS  PubMed  Google Scholar 

  64. Powell, L. M. et al. Ecology of a novel Synechococcus clade occurring in dense populations in saline Antarctic lakes. Mar. Ecol. Prog. Ser. 291, 65–80 (2005).

    Article  CAS  Google Scholar 

  65. Burke, C. M. & Burton, H. R. Photosynthetic bacteria in meromictic lakes and stratified fjords of the Vestfold Hills, Antarctica. Hydrobiologia 165, 13–23 (1988).

    Article  CAS  Google Scholar 

  66. Karr, E. A., Sattley, W. M., Jung, D. O., Madigan, M. T. & Achenbach, L. A. Remarkable diversity of phototrophic purple bacteria in a permanently frozen Antarctic lake. Appl. Environ. Microbiol. 69, 4910–4914 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Sattley, W. M. & Madigan, M. T. Isolation, characterization, and ecology of cold-active, chemolithotrophic, sulfur-oxidizing bacteria from perennially ice-covered Lake Fryxell, Antarctica. Appl. Environ. Microbiol. 72, 5562–5568 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. DeMaere, M. Z. et al. High level of inter-genera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc. Natl Acad. Sci. USA 110, 16939–16944 (2013). Study demonstrating the interplay between promiscuous gene exchange and niche adaptation in shaping Antarctic microbial communities and generating a low-complexity, hierarchically structured ecosystem.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Campbell, P. J. Primary productivity of a hypersaline Antarctic lake. Mar. Freshwater Res. 29, 717–724 (1978).

    Article  CAS  Google Scholar 

  70. Ferris, J. M. & Burton, H. R. The annual cycle of heat content and mechanical stability of hypersaline Deep Lake, Vestfold Hills, Antarctica. Hydrobiologia 165, 115–128 (1988).

    Article  CAS  Google Scholar 

  71. Rodriguez-Valera, F., Ruiz-Berraquero, F. & Ramos-Cormenzana, A. Isolation of extreme halophiles from seawater. Appl. Environ. Microbiol. 38, 164–165 (1979).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Munson, M. A., Nedwell, D. B. & Embley, T. M. Phylogenetic diversity of archaea in sediment samples from a coastal salt marsh. Appl. Environ. Microbiol. 63, 4729–4733 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Purdy, K. J. et al. Isolation of haloarchaea that grow at low salinities. Environ. Microbiol. 6, 591–595 (2004).

    Article  CAS  PubMed  Google Scholar 

  74. Bolhuis, H. & Stal, L. J. Analysis of bacterial and archaeal diversity in coastal microbial mats using massive parallel 16S rRNA gene tag sequencing. ISME J. 5, 1701–1712 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Williams, T. J. et al. Microbial ecology of an Antarctic hypersaline lake: genomic assessment of ecophysiology amongst dominant haloarchaea. ISME J. 8, 1645–1658 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Murray, A. E. et al. Microbial life at −13 °C in the brine of an ice-sealed Antarctic lake. Proc. Natl Acad. Sci. USA 109, 20626–20631 (2012). Careful consideration of the role of geochemical and biological processes occurring in an unusual ice-covered lake.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Doran, P. T., Fritsen, C. H., McKay, C. P., Priscu, J. C. & Adams, E. E. 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. USA 100, 26–31 (2003).

    Article  CAS  PubMed  Google Scholar 

  78. Yau, S. et al. Metagenomic insights into strategies of carbon conservation and unusual sulfur biogeochemistry in a hypersaline Antarctic lake. ISME J. 7, 1944–1961 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Yau, S. et al. Virophage control of Antarctic algal host–virus dynamics. Proc. Natl Acad. Sci. USA 108, 6163–6168 (2011). First paper to describe an ecological role for virophages, indicating that virophages regulate host–virus interactions, influence overall carbon flux and have previously unrecognized roles in diverse aquatic ecosystems.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Mikucki, J. A. & Priscu, J. C. Bacterial diversity associated with Blood Falls, a subglacial outflow from the Taylor Glacier, Antarctica. Appl. Environ. Microbiol. 73, 4029–4039. (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Mikucki, J. A. et al. A contemporary microbially maintained subglacial ferrous “ocean”. Science 324, 397–400 (2009). Colourful description of a fascinating subglacial system gleaned from the analysis of a spectacular glacier outflow.

    Article  CAS  PubMed  Google Scholar 

  82. Grzymski, J. J. et al. A metagenomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters. ISME J. 6, 1901–1915 (2012). First study using metagenomics to identify seasonal shifts in Southern Ocean communities, highlighting the role of chemolithoautotrophic microorganisms in fixing CO 2 in winter.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Williams, T. J. et al. A metaproteomic assessment of winter and summer bacterioplankton from Antarctic Peninsula coastal surface waters. ISME J. 6, 1883–1900 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ghiglione, J. F. & Murray, A. E. Pronounced summer to winter differences and higher wintertime richness in coastal sub-Antarctic and Antarctic marine bacterioplankton. Environ. Microbiol. 14, 617–629 (2012).

    Article  CAS  PubMed  Google Scholar 

  85. Vick, T. J. & Priscu, J. C. Bacterioplankton productivity in lakes of the Taylor Valley, Antarctica, during the polar night transition. Aquat. Microb. Ecol. 68, 77–90 (2012).

    Article  Google Scholar 

  86. Vick-Majors, T. J., Priscu, J. C. & Amaral-Zettler, L. A. Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. ISME J. 8, 778–789 (2014). First pyrosequencing study to identify shifts in lake communities during the transition to polar darkness and identifying the potentially important role of chemolithoautotrophic carbon fixation.

    Article  CAS  PubMed  Google Scholar 

  87. Bielewicz, S. et al. Protist diversity in a permanently ice-covered Antarctic lake during the polar night transition. ISME J. 5, 1559–1564 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  88. Thurman, J. et al. Microbial dynamics and flagellate grazing during transition to winter in Lakes Hoare and Bonney, Antarctica. FEMS Microbiol. Ecol. 82, 449–458 (2012).

    Article  CAS  PubMed  Google Scholar 

  89. Laybourn-Parry, J., Marshall, W. A. & Marchant, H. J. Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes. Freshwater Biol. 50, 830–838 (2005).

    Article  Google Scholar 

  90. Kepner, R. L., Wharton, R. A. & Suttle, C. A. Viruses in Antarctic lakes. Limnol. Oceanogr. 43, 1754–1761 (1998).

    Article  PubMed  Google Scholar 

  91. López-Bueno, A. et al. High diversity of the viral community from an Antarctic lake. Science 326, 858–861 (2009). First metagenome study of an Antarctic environment, identifying a high level of new unique viruses and illustrating virus dynamics associated with physical changes occurring in the lake.

    Article  PubMed  CAS  Google Scholar 

  92. Anesio, A. M. & Bellas, C. M. Are low temperature habitats hot spots of microbial evolution driven by viruses? Trends Microbiol. 19, 52–57 (2011).

    Article  CAS  PubMed  Google Scholar 

  93. Tschitschko, B. et al. Antarctic archaea-virus interactions: metaproteome-led analysis of invasion, evasion and adaptation. ISME J. 9, 2094–2107 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Hopkins, M. et al. Diversity of environmental single-stranded DNA phages revealed by PCR amplification of the partial major capsid protein. ISME J. 8, 2093–2103 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. López-Bueno, A., Rastrojo, A., Peiró, R., Arenas, M. & Alcamí, A. Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Mol. Ecol. 24, 4812–4825 (2015). First study describing RNA viruses in an Antarctic lake, identifying the important but uncharacterized roles that RNA viruses have in Antarctic aquatic systems.

    Article  PubMed  CAS  Google Scholar 

  96. Aguirre de Cárcer, D., López-Bueno, A., Pearce, D. A. & Alcamí, A. Biodiversity and distribution of polar freshwater DNA viruses. Sci. Adv. 1, e1400127 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Cavicchioli, R. & Erdmann, S. The discovery of Antarctic RNA viruses: a new game changer. Mol. Ecol. 24, 4809–4811 (2015).

    Article  PubMed  Google Scholar 

  98. Rodriguez-Brito, B. et al. Viral and microbial community dynamics in four aquatic environments. ISME J. 4, 739–751 (2010).

    Article  PubMed  Google Scholar 

  99. Culley, A. I., Lang, A. S. & Suttle, C. A. Metagenomic analysis of coastal RNA virus communities. Science 312, 1795–1798 (2006).

    Article  CAS  PubMed  Google Scholar 

  100. Doming, E. & Holland, J. J. RNA virus mutations and fitness for survival. Annu. Rev. Microbiol. 51, 151–158 (1997).

    Article  Google Scholar 

  101. Williams, T. J. et al. Defining the response of a microorganism to growth temperature that spans its full growth temperature range (-2 °C to 28 °C) using multiplex quantitative proteomics. Environ. Microbiol. 13, 2186–2203 (2011).

    Article  CAS  PubMed  Google Scholar 

  102. Cavicchioli, R. On the concept of a psychrophile. ISME J. http://dx.doi.org/10.1038/ismej.2015.160, (2015).

  103. Jansson, J. K. & Prosser, J. I. Microbiology: the life beneath our feet. Nature 494, 40–41 (2013).

    Article  CAS  PubMed  Google Scholar 

  104. Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).

    Article  CAS  PubMed  Google Scholar 

  105. Liu, J. & Curry, J. A. Accelerated warming of the Southern Ocean and its impacts on the hydrological cycle and sea ice. Proc. Natl Acad. Sci. USA 107, 14987–14992 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Parkinson, C. L. Global sea ice coverage from satellite data: annual cycle and 35-yr trends. J. Climate 27, 9377–9382 (2014).

    Article  Google Scholar 

  107. Böning, C. W., Dispert, A., Visbeck, M., Rintoul, S. R. & Schwarzkopf, F. U. The response of the Antarctic Circumpolar Current to recent climate change. Nat. Geo. 1, 864–869 (2008).

    Article  CAS  Google Scholar 

  108. Fyfe, J. C. & Saenko, O. A. Human-induced change in the Antarctic Circumpolar Current. J. Climate 18, 3068–3073 (2005).

    Article  Google Scholar 

  109. Biastoch, A., Böning, C. W., Schwarzkopf, F. U. & Lutjeharms, J. R. E. Increase in Agulhas leakage due to poleward shift of Southern Hemisphere westerlies. Nature 462, 495–498 (2009).

    Article  CAS  PubMed  Google Scholar 

  110. Meijers, A. J. S. The Southern Ocean in the Coupled Model Intercomparison Project phase 5. Phil. Trans. R. Soc. A 372, 20130296 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Weber, T. S. & Deutsch, C. Ocean nutrient ratios governed by plankton biogeography. Nature 467, 550–554 (2010).

    Article  CAS  PubMed  Google Scholar 

  112. Murphy, E. J. et al. Developing integrated models of Southern Ocean food webs: Including ecological complexity, accounting for uncertainty and the importance of scale. Prog. Oceanogr. 102, 74–92 (2012).

    Article  Google Scholar 

  113. Wright, A. & Siegert, M. A fourth inventory of Antarctic subglacial lakes. Antarct. Sci. 24, 659–664 (2012).

    Article  Google Scholar 

  114. Inman, M. Antarctic drilling — the plan to unlock Lake Vostok. Science 310, 611–612 (2005).

    Article  CAS  PubMed  Google Scholar 

  115. Fox, D. Lakes under the ice: Antarctica's secret garden. Nature 512, 244–246 (2014).

    Article  CAS  PubMed  Google Scholar 

  116. Schiermeier, Q. Polar drilling problems revealed. Nature 505, 463 (2014).

    Article  CAS  PubMed  Google Scholar 

  117. Rogers, S. O. et al. Ecology of subglacial Lake Vostok (Antarctica), based on metagenomic/metatranscriptomic analyses of accretion ice. Biology (Basel) 2, 629–650 (2013).

    Google Scholar 

  118. Shtarkman, Y. M. et al. Subglacial Lake Vostok (Antarctica) accretion ice contains a diverse set of sequences from aquatic, marine and sediment-inhabiting bacteria and eukarya. PLoS ONE 8, e67221 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Siegert, M. J., Makinson, K., Blake, D., Mowlem, M. & Ross, N. An assessment of deep hot-water drilling as a means to undertake direct measurement and sampling of Antarctic subglacial lakes: experience and lessons learned from the Lake Ellsworth field season 2012/13. Ann. Glaciol. 55, 59–73 (2014).

    Article  Google Scholar 

  120. Christner, B. C. et al. A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512, 310–313 (2014). First successful deep subglacial lake exploration to identify the presence and function of lake microbial communities.

    Article  CAS  PubMed  Google Scholar 

  121. Tranter, M. Biogeochemistry: microbes eat rock under ice. Nature 512, 256–257 (2014).

    Article  CAS  PubMed  Google Scholar 

  122. Priscu, J. C. et al. A microbiologically clean strategy for access to the Whillans Ice Stream subglacial environment. Antarct. Sci. 25, 637–647 (2013).

    Article  Google Scholar 

  123. Richter, A. et al. Subglacial Lake Vostok not expected to discharge water. Geophys. Res. Lett. 41, 6772–6778 (2014).

    Article  Google Scholar 

  124. Bell, R. E. et al. Origin and fate of Lake Vostok water frozen to the base of the East Antarctic ice sheet. Nature 416, 307–310 (2002).

    Article  CAS  PubMed  Google Scholar 

  125. Fricker, H. A., Scambos, T., Bindschadler, R. & Padman, L. An active subglacial water system in West Antarctica mapped from space. Science 315, 1544–1548 (2007).

    Article  CAS  PubMed  Google Scholar 

  126. Fisher, A. T. et al. High geothermal heat flux measured below the West Antarctic Ice Sheet. Sci. Adv. 1, e1500093 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  127. Wingham, D. J., Siegert, M. J., Shepherd, A. & Muir, A. S. Rapid discharge connects Antarctic subglacial lakes. Nature 440, 1033–1036 (2006).

    Article  CAS  PubMed  Google Scholar 

  128. Pattyn, F. Antarctic subglacial conditions inferred from a hybrid ice sheet/ice stream model. Earth Planet. Sci. Lett. 295, 451–461 (2010).

    Article  CAS  Google Scholar 

  129. Wadham, J. L. et al. Potential methane reservoirs beneath Antarctica. Nature 488, 633–637 (2012). Important study highlighting the potential scale of the role that subglacial Antarctic microorganisms may have in global nutrient cycles.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The author is indebted to J. Berengut and D. Smith who crafted figures, A. Hull, M. Milnes, H. Dugan and J. Mikucki for providing images of Antarctic lakes, the Landsat Image Mosaic of Antarctica (LIMA) project for making satellite images available, D. Velázquez for discussions about Antarctic viruses, and T. Kolesnikow and T. J. Williams for insightful comments on manuscript drafts. The author's Antarctic research has been supported by the Australian Research Council, the Australian Antarctic Science Program, the Gordon and Betty Moore Foundation for DNA sequencing at the J. Craig Venter Institute and the US Department of Energy for DNA sequencing at the Joint Genome Institute.

Author information

Authors and Affiliations

  1. School of Biotechnology and Biomolecular Sciences, The University of New South Wales, Sydney, 2052, New South Wales, Australia

    Ricardo Cavicchioli

Authors
  1. Ricardo Cavicchioli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ricardo Cavicchioli.

Ethics declarations

Competing interests

The author declares no competing financial interests.

PowerPoint slides

Glossary

Antarctic thermohaline circulation

Antarctic thermohaline circulation (part of 'the global conveyer belt') arises from katabatic winds — which cause water movement that cools Southern Ocean water, which sinks because of its increased density — and from sea ice formation, which results in salt exclusion, causing the sinking of dense briny water.

Antarctic ice sheet

The Antarctic continent comprises the Antarctic Peninsula Ice Sheet, the West Antarctic Ice Sheet and the East Antarctic Ice Sheet, which collectively comprise more than 500 individual glaciers.

Stratification

The difference in the density of water between the surface and deeper waters (for example, upper ocean stratification from the surface to a depth of ∼200 m); stratification is increasing owing to the warming of surface waters and to an increase in freshwater content in high-latitude regions.

Endemicity

The extent to which isolation and natural selection affect speciation of microorganisms in a given region (in this case, within Antarctica).

Pelagic

Pelagic microorganisms inhabit the open ocean, in contrast to sea-ice microorganisms, which inhabit sea ice.

Krill

Crustaceans (euphausiids) that live in the open ocean, feed on phytoplankton and to some extent zooplankton, and represent an important component in the food web bridging microorganisms (for example, primary producers) and higher trophic organisms (for example, fish, whales, seals and seabirds) that depend on them for survival.

Pyrosequencing

Targeted DNA sequencing of specific gene amplicons, typically regions of small subunit rRNA (SSU rRNA) genes that can subsequently be used for generating diversity estimates and phylogenetic reconstruction of microbial community composition.

Metagenomics

The study of the total DNA sequences obtained from DNA extracted from an environmental sample, with random 'shotgun' sequencing providing an inventory of genes representing the organisms present within the sample.

Metatranscriptomics

The study of RNA species expressed by a microbial community present within an environmental sample determined by DNA sequencing of reverse transcribed cDNA generated from the RNA.

Metaproteomics

The study of the proteins represented by a community of microorganisms present in an environmental sample, with protein identifications obtained using mass spectrometry to determine the mass of peptides derived from extracted proteins.

Microbial communities

All individual microbial taxa within a defined habitat.

Advection

Physical transport of components (for example, biotic and abiotic matter and heat) by ocean currents.

Biogeography

Distribution of biodiversity over space and time.

SAR11 bacterial clade

Members of the Bacteria comprising a distinct family within the Alphaproteobacteria that are abundant and ubiquitous in marine environments, and have important roles as oligotrophic heterotrophs.

Mosaic genomes

Genomes assembled from metagenome data that are typically incomplete, in comparison to closed or draft genomes of individual cultivated laboratory-grown isolates.

Phylotypes

Genetic variants of a specific lineage, often used to describe subtypes of a species: for example, an operationally defined measure of phylogenetic clustering of small subunit rRNA (SSU rRNA) gene sequences or internal transcribed spacer sequences of SSU rRNA genes.

Aeolian dispersal

Movement and successful establishment of organisms (in this case, microorganisms) from one location to another mediated by the wind.

Meromictic

A stratified lake that contains an upper mixed layer (mixolimnion) that does not mix with the bottom stagnant anoxic layer (monimolimnion) owing to a steep density gradient (for example, pycnocline, oxycline and chemocline) separating the two layers. By contrast, in a monomictic lake, water throughout the lake (top to bottom) mixes once per year.

Microbial populations

The total contingent of one taxon (for example, species) within a microbial community.

Green sulfur bacteria

(GSB). GSB (Chlorobiaceae) are phototrophic primary producers that fix CO2 at low sunlight intensities and have important roles in sulfur cycling by oxidizing reduced forms of sulfur that are often made available in the system by sulfate-reducing bacteria.

Anoxic

An anoxic environment lacks oxygen, such as the bottom waters of a meromictic lake, where oxygen has been depleted and only anaerobic processes occur (for example, methanogenesis).

Biogeochemical cycles

The influences of both biotic and abiotic processes on the inter-conversion of chemical substances, typically cycling chemicals through oxidized and reduced forms.

Haloarchaea

Heterotrophic members of the domain Archaea that require hypersaline conditions for growth.

Benthic

Benthic organisms live at the bottom of a water body (for example, a lake or an ocean); these include microorganisms growing in mats on the sediment surface and within the shallow subsurface.

Ecotype

A phylotype where the genetic variation manifests in a phenotypic distinction that enables colonization of a specific ecological niche.

Sympatric speciation

The process leading to the evolution of new species from a single ancestral species while inhabiting the same geographic location.

Limnology

The study of inland aquatic (freshwater or saline) systems, including their physical, geological, chemical and biological characteristics.

Virophages

Small viruses that are deleterious to other larger viruses, but also require the larger viruses for their own propagation (for example, by gaining entry to a host cell).

Open discovery

As opposed to the testing of a specific hypothesis, open discovery involves learning something new from data acquired by observation and analysis (for example, metagenome data) that is essentially unforeseeable and is often serendipitous, akin to turning over a rock to discover what lies beneath it, opening an ancient tomb to learn what secrets it holds or viewing a new world for the first time.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cavicchioli, R. Microbial ecology of Antarctic aquatic systems. Nat Rev Microbiol 13, 691–706 (2015). https://doi.org/10.1038/nrmicro3549

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro3549

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing