Review Article | Published:

Microbial ecology of the cryosphere: sea ice and glacial habitats

Nature Reviews Microbiology volume 13, pages 677690 (2015) | Download Citation

Abstract

The Earth's cryosphere comprises those regions that are cold enough for water to turn into ice. Recent findings show that the icy realms of polar oceans, glaciers and ice sheets are inhabited by microorganisms of all three domains of life, and that temperatures below 0 °C are an integral force in the diversification of microbial life. Cold-adapted microorganisms maintain key ecological functions in icy habitats: where sunlight penetrates the ice, photoautotrophy is the basis for complex food webs, whereas in dark subglacial habitats, chemoautotrophy reigns. This Review summarizes current knowledge of the microbial ecology of frozen waters, including the diversity of niches, the composition of microbial communities at these sites and their biogeochemical activities.

Key points

  • Active, diverse microorganisms have been detected in all cryospheric habitats on Earth, and they are as abundant as those living in freshwater habitats.

  • Numerous intracellular and extracellular adaptations enable microorganisms to thrive at temperatures below 0 °C, and thus to survive and grow in liquid inclusions within porous ice matrices.

  • The many different types of cryospheric habitats pose distinct habitability challenges to resident microorganisms. Communities specialized to each type of ice environment use different strategies to fulfil their energy and growth requirements, using either sunlight, or inorganic or organic compounds as energy sources.

  • Today, the use of next-generation sequencing approaches enables more detailed insights into microbial community composition and function, and allows the tracking of structural and functional differences and changes at a high resolution.

  • Climate change is altering the cryosphere; it is expected that this will lead to shifts in the distribution, composition and activity of cold-adapted microorganisms.

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References

  1. 1.

    & The snowball Earth hypothesis: testing the limits of global change. Terra Nov. 14, 129–155 (2002).

  2. 2.

    et al. The disappearing cryosphere: impacts and ecosystem responses to rapid cryosphere loss. Bioscience 62, 405–415 (2012).

  3. 3.

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

  4. 4.

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

  5. 5.

    , & Exopolymer alteration of physical properties of sea ice and implications for ice habitability and biogeochemistry in a warmer Arctic. Proc. Natl Acad. Sci. USA 108, 3653–3658 (2011). Quantitative image and chemical analyses of natural and laboratory-grown sea ice shows that EPS produced by diatoms alters the physical complexity of ice pores, increasing the habitable liquid-filled space within the ice and the potential for primary productivity.

  6. 6.

    , , , & Prokaryotic diversity in sediments beneath two polar glaciers with contrasting organic carbon substrates. Extremophiles 16, 255–265 (2012).

  7. 7.

    , , , & High microbial activity on glaciers: importance to the global carbon cycle. Glob. Chang. Biol. 15, 955–960 (2009).

  8. 8.

    et al. Microbial cell budgets of an Arctic glacier surface quantified using flow cytometry. Environ. Microbiol. 14, 2998–3012 (2012).

  9. 9.

    et al. Floating ice-algal aggregates below melting Arctic sea ice. PLoS ONE 8, e76599 (2013).

  10. 10.

    , , , & Biological- and physical-induced oxygen dynamics in melting sea ice of the Fram Strait. Limnol. Oceanogr. 59, 1097–1111 (2014).

  11. 11.

    et al. Composition, buoyancy regulation and fate of ice algal aggregates in the central Arctic Ocean. PLoS ONE 9, e107452 (2014).

  12. 12.

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

  13. 13.

    & in Microbial Diversity and Bioprospecting (ed. Bull, A.) 130–145 (ASM Press, 2004). This chapter discusses the microbial ecology of icy habitats and contends that microorganisms in frozen environments are numerous and are an unaccounted contribution to global carbon budgets.

  14. 14.

    , , , & Bacterial community structure in high-arctic snow and freshwater as revealed by pyrosequencing of 16S rRNA genes and cultivation. Polar Res. 32, 17390 (2013).

  15. 15.

    , & Microbial nitrogen cycling in Arctic snowpacks. Environ. Res. Lett. 8, 035004 (2013).

  16. 16.

    et al. Bacterial diversity in snow on North Pole ice floes. Extremophiles 18, 945–951 (2014).

  17. 17.

    , & Potential drivers of microbial community structure and function in Arctic spring snow. Front. Microbiol. 5, 413 (2014).

  18. 18.

    , , , & Stable microbial community composition on the Greenland Ice Sheet. Front. Microbiol. 6, 193 (2015).

  19. 19.

    , , , & Metabolic activity and diversity of cryoconites in the Taylor Valley, Antarctica. J. Geophys. Res. 112, G04S32 (2007).

  20. 20.

    , , & Temporal variations in physical and chemical features of cryoconite holes on Canada Glacier, McMurdo Dry Valleys, Antarctica. J. Geophys. Res. 113, G01S92 (2008).

  21. 21.

    et al. Glacial ecosystems. Ecol. Monogr. 78, 41–67 (2008).

  22. 22.

    & Glaciers and ice sheets as a biome. Trends Ecol. Evol. 27, 219–225 (2012). This review provides an introduction to glaciated environments that serve as microbial habitats.

  23. 23.

    et al. Limnological conditions in subglacial Lake Vostok, Antarctica. Limnol. Oceanogr. 51, 2485–2501 (2006).

  24. 24.

    , & Novel ultramicrobacterial isolates from a deep Greenland ice core represent a proposed new species, Chryseobacterium greenlandense sp. nov. Extremophiles 14, 61–69 (2010).

  25. 25.

    , , & Comparison of the microbial diversity at different depths of the GISP2 Greenland ice core in relationship to deposition climates. Environ. Microbiol. 11, 640–656 (2009).

  26. 26.

    Chemical models of solute acquisition in glacial melt waters. J. Glaciol. 30, 49–57 (1984).

  27. 27.

    , & Microbial life beneath a High Arctic glacier. Appl. Environ. Microbiol. 66, 3214–3220 (2000).

  28. 28.

    et al. Widespread bacterial populations at glacier beds and their relationship to rock weathering and carbon cycling. Geology 27, 107–110 (1999).

  29. 29.

    & Water flow through temperate glaciers. Rev. Geophys. 36, 299 (1998).

  30. 30.

    Glaciers (Routledge, 1999).

  31. 31.

    et al. Bacteria beneath the West Antarctic ice sheet. Environ. Microbiol. 11, 609–615 (2009).

  32. 32.

    , & The Ecology of Snow and Ice Environments (Oxford Univ. Press, 2012).

  33. 33.

    & in Planets and Life: The Emerging Science of Astrobiology (eds Sullivan, W. T. & Baross, J. A.) 292–312 (Cambridge Univ. Press, 2007).

  34. 34.

    Sea ice ecosystems. Ann. Rev. Mar. Sci. 6, 439–467 (2014).

  35. 35.

    & Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ. Microbiol. 8, 1115–1121 (2006).

  36. 36.

    , & A physical mechanism for establishing algal populations in frazil ice. Nature 306, 363–365 (1983).

  37. 37.

    et al. Massive phytoplankton blooms under Arctic sea ice. Science 336, 1408 (2012).

  38. 38.

    , & Diatom vertical migration within land-fast Arctic sea ice. J. Mar. Syst. 139, 496–504 (2014).

  39. 39.

    , & Motility of Colwellia psychrerythraea strain 34H at subzero temperatures. Appl. Environ. Microbiol. 69, 4282–4284 (2003).

  40. 40.

    & Elevated bacterial abundance and exopolymers in saline frost flowers and implications for atmospheric chemistry and microbial dispersal. Geophys. Res. Lett. 37, L13501 (2010).

  41. 41.

    et al. Frost flowers on young Arctic sea ice: the climatic, chemical, and microbial significance of an emerging ice type. J. Geophys. Res. Atmos. 119, 593–612 (2014).

  42. 42.

    , , & Predominance of ß-proteobacteria in summer melt pools on Arctic pack ice. Limnol. Oceanogr. 49, 1013–1021 (2004).

  43. 43.

    , & Spatial heterogeneity and temporal dynamics of particles, bacteria, and pEPS in Arctic winter sea ice. J. Mar. Syst. 74, 902–917 (2008).

  44. 44.

    & Bacterial responses to fluctuations and extremes in temperature and brine salinity at the surface of Arctic winter sea ice. FEMS Microbiol. Ecol. 89, 476–489 (2014). This study of two Arctic bacterial isolates subjected to fluctuating and extreme freezing conditions, as encountered in Arctic sea ice during winter, revealed different survival strategies: use of osmoprotectant compounds to reduce cell losses; and an increase in population size via cell miniaturization and fragmentation, which enhances cell dispersal.

  45. 45.

    , & Bacterial activity at −2 to −20 degrees C in Arctic wintertime sea ice. Appl. Environ. Microbiol. 70, 550–557 (2004).

  46. 46.

    Adaptation of Arctic and Antarctic ice metazoa to their habitat. Zoology 104, 339–345 (2001).

  47. 47.

    & Antarctic sea ice — a habitat for extremophiles. Science 295, 641–644 (2002).

  48. 48.

    et al. Broad-scale predictability of carbohydrates and exopolymers in Antarctic and Arctic sea ice. Proc. Natl Acad. Sci. USA 110, 15734–15739 (2013).

  49. 49.

    et al. Export of algal biomass from the melting Arctic sea ice. Science 339, 1430–1432 (2013).

  50. 50.

    Primary production in Antarctic sea ice. Science 276, 394–397 (1997).

  51. 51.

    , , , & New measurements of phytoplankton and ice algal production in the Arctic Ocean. Deep. Res. Part II Top. Stud. Oceanogr. 44, 1623–1644 (1997).

  52. 52.

    & Bacterial standing stock, activity, and carbon production during formation and growth of sea ice in the Weddell Sea, Antarctica. Appl. Environ. Microbiol. 60, 2746–2753 (1994).

  53. 53.

    & Bacteria in sea ice and underlying water of the eastern Weddell Sea in midwinter. Mar. Ecol. Prog. Ser. 117, 269–288 (1995).

  54. 54.

    , , & Recent advances and future perspectives in microbial phototrophy in Antarctic sea ice. Biol. (Basel). 1, 542–556 (2012).

  55. 55.

    & Genetic analysis of sea-ice bacterial communities of the Western Baltic Sea using an improved double gradient method. Polar Biol. 24, 252–257 (2014).

  56. 56.

    , & Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environ. Microbiol. 12, 1828–1841 (2010).

  57. 57.

    , & Archaeal diversity revealed in Antarctic sea ice. Antarct. Sci. 23, 531–536 (2011).

  58. 58.

    et al. Microbial community structure of Arctic multiyear sea ice and surface seawater by 454 sequencing of the 16S RNA gene. ISME J. 6, 11–20 (2012).

  59. 59.

    et al. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Appl. Environ. Microbiol. 69, 6610–6619 (2003). This study provides a thorough comparison of the composition of bacterial communities in sea ice at both poles.

  60. 60.

    , , & Antarctic sea-ice microbial communities show distinct patterns of zonation in response to algal-derived substrates. Aquat. Microb. Ecol. 73, 123–134 (2014).

  61. 61.

    et al. Bacterial communities of surface mixed layer in the pacific sector of the western Arctic Ocean during sea-ice melting. PLoS ONE 9, e86887 (2014).

  62. 62.

    , , & Production and characterization of the intra- and extracellular carbohydrates and polymeric substances (EPS) of three sea-ice diatom species, and evidence for a cryoprotective role for EPS. J. Phycol. 48, 1494–1509 (2012).

  63. 63.

    & Poles apart: biodiversity and biogeography of sea ice bacteria. 53, 189–215 (1999).

  64. 64.

    et al. Colwellia demingiae sp. nov., Colwellia hornerae sp. nov., Colwellia rossensis sp. nov. and Colwellia psychrotropica sp. nov.: psychrophilic Antarctic species with the ability to synthesize docosahexaenoic acid (22:ω63). Int. J. Syst. Bacteriol. 48, 1171–1180 (1998).

  65. 65.

    & Diversity and genomics of Antarctic marine micro-organisms. Phil. Trans. R. Soc. 362, 2259–2271 (2007).

  66. 66.

    , , & Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice. Extremophiles 7, 377–384 (2003).

  67. 67.

    & A molecular phylogenetic survey of sea-ice microbial communities (SIMCO). FEMS Microbiol. Ecol. 35, 267–275 (2001).

  68. 68.

    et al. Protists in Arctic drift and land-fast sea ice. J. Phycol. 49, 229–240 (2013).

  69. 69.

    et al. Distinct bacterial assemblages reside at different depths in Arctic multiyear sea ice. FEMS Microbiol. Ecol. 90, 115–125 (2014). This is a comparative investigation of the bacterial community composition of distinct multi-year ice layers and surface seawater indicates that sea ice communities are structured more by conditions at the time of ice formation than by in situ physicochemical parameters.

  70. 70.

    et al. Bacterial community dynamics and activity in relation to dissolved organic matter availability during sea-ice formation in a mesocosm experiment. Microbiologyopen 3, 139–156 (2014).

  71. 71.

    et al. The psychrophilic lifestyle as revealed by the genome sequence of Colwellia psychrerythraea 34H through genomic and proteomic analyses. Proc. Natl Acad. Sci. USA 102, 10913–10918 (2005). This paper provides comprehensive background information on cold adaptation in general and detailed insights into the numerous specific adaptations of the marine psychrophilic bacterium C. psychrerythraea 34H.

  72. 72.

    et al. Elevated mercury measured in snow and frost flowers near Arctic sea ice leads. Geophys. Res. Lett. 32, 1–4 (2005).

  73. 73.

    , , & Selective occurrence of Rhizobiales in frost flowers on the surface of young sea ice near Barrow, Alaska and distribution in the polar marine rare biosphere. Environ. Microbiol. Rep. 5, 575–582 (2013).

  74. 74.

    , , & The genetic potential for key biogeochemical processes in Arctic frost flowers and young sea ice revealed by metagenomic analysis. FEMS Microbiol. Ecol. 89, 376–387 (2014). In this first metagenomic analysis of a sea ice habitat, focused on the surface of young sea ice exposed to a very cold atmosphere, genes unique to survival and activity at the ice–atmosphere interface were detected.

  75. 75.

    , , & Bacterial and extracellular polysaccharide content of brine-wetted snow over Arctic winter first-year sea ice. J. Geophys. Res. Ocean. 118, 726–735 (2013).

  76. 76.

    et al. Nitrogen fixation on Arctic glaciers, Svalbard. J. Geophys. Res. 116, G03039 (2011).

  77. 77.

    et al. Photophysiology and albedo-changing potential of the ice algal community on the surface of the Greenland ice sheet. ISME J. 6, 2302–2313 (2012). This study provides evidence for how the development of pigmentation in eukaryotic algae during the melting season promotes darkening of large areas of the Greenland Ice Sheet and thus influences its reflective properties.

  78. 78.

    , , & Variations of algal communities cause darkening of a Greenland glacier. FEMS Microbiol. Ecol. 89, 402–414 (2014).

  79. 79.

    , & Biological processes on glacier and ice sheet surfaces. Nat. Geosci. 5, 771–774 (2012). This work provides insights into how organic carbon accumulates at the surface of glaciers and is subsequently modified and transported, with particular attention to CO2 cycling.

  80. 80.

    & in Snow Ecology (eds Jones, H. et al.) 168–228 (Cambridge Univ. Press, 2001).

  81. 81.

    Seasonal and altitudinal variations in snow algal communities on an Alaskan glacier (Gulkana glacier in the Alaska range). Environ. Res. Lett. 8, 035002 (2013).

  82. 82.

    , & Microbial communities on glacier surfaces in Svalbard: impact of physical and chemical properties on abundance and structure of cyanobacteria and algae. Microb. Ecol. 52, 644–654 (2006).

  83. 83.

    , & Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J. 4, 191–202 (2010). Using targeted sequencing of 16S rRNA of cyanobacteria, this study demonstrates a global distribution of low-temperature cyanobacterial ecotypes throughout the cold terrestrial biosphere.

  84. 84.

    et al. A metagenomic snapshot of taxonomic and functional diversity in an alpine glacier cryoconite ecosystem. Environ. Res. Lett. 8, 035003 (2013).

  85. 85.

    , & Diversity, cold active enzymes and adaptation strategies of bacteria inhabiting glacier cryoconite holes of High Arctic. Extremophiles 18, 229–242 (2014).

  86. 86.

    et al. Glaciers as a source of ancient and labile organic matter to the marine environment. Nature 462, 1044–1047 (2009).

  87. 87.

    , , , & Comparison of cryoconite organic matter composition from Arctic and Antarctic glaciers at the molecular-level. Geochim. Cosmochim. Acta 104, 1–18 (2013).

  88. 88.

    et al. Organic carbon export from the Greenland ice sheet. Geochim. Cosmochim. Acta 109, 329–344 (2013). This study shows that glacial runoff from the Greenland Ice Sheet is responsible for the delivery of large amounts of labile and microbially produced dissolved organic carbon to coastal waters.

  89. 89.

    et al. in Polar Lakes and Rivers (eds Vincent, W. F. & Laybourn-Parry, J.) 119–136 (Oxford Univ. Press, 2008).

  90. 90.

    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).

  91. 91.

    et al. A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512, 310–313 (2014). This unprecedented study presents initial microbiological findings from water and sediment samples collected from an Antarctic subglacial lake.

  92. 92.

    , , , & in Psychrophiles: from Biodiversity to Biotechnology (eds Margesin, R. et al.) 51–71 (Springer, 2008).

  93. 93.

    in Antarctic Subglacial Environments, Geophysical Monograph Series (eds Siegert, M. J. & Kennicutt, M. C.) 61–81 (Wiley, 2011).

  94. 94.

    , , & Molecular evidence for an active endogenous microbiome beneath glacial ice. ISME J. 7, 1402–1412 (2013).

  95. 95.

    & Bacterial diversity associated with blood falls, a subglacial outflow from the Taylor Glacier, Antarctica. Appl. Environ. Microbiol. 73, 4029–4039 (2007).

  96. 96.

    et al. A viable microbial community in a subglacial volcanic crater lake, Iceland. Astrobiology 4, 327–344 (2004).

  97. 97.

    et al. A contemporary microbially maintained subglacial ferrous 'ocean'. Science 324, 397–400 (2009). This work provides important insight into the biogeochemistry of anoxic subglacial brine and microbial diversity in subglacial habitats and their role in global iron fluxes.

  98. 98.

    , , , & Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes. Appl. Environ. Microbiol. 71, 6986–6997 (2005).

  99. 99.

    , & Hydrological controls on microbial communities in subglacial environments. Hydrol. Process. 19, 995–998 (2005).

  100. 100.

    et al. Diversity, abundance, and potential activity of nitrifying and nitrate-reducing microbial assemblages in a subglacial ecosystem. Appl. Environ. Microbiol. 77, 4778–4787 (2011).

  101. 101.

    , , & Stable isotope evidence for microbial sulphate reduction at the bed of a polythermal High Arctic glacier. Earth Planet. Sci. Lett. 219, 341–355 (2004).

  102. 102.

    , , , & Methanogenesis in subglacial sediments. Environ. Microbiol. Rep. 2, 685–692 (2010).

  103. 103.

    et al. Molecular and biogeochemical evidence for methane cycling beneath the western margin of the Greenland Ice Sheet. ISME J. 8, 2305–2316 (2014).

  104. 104.

    , , & Subglacial methanogenesis: a potential climatic amplifier? Global Biogeochem. Cycles 22, GB2021 (2008).

  105. 105.

    et al. Potential methane reservoirs beneath Antarctica. Nature 488, 633–637 (2012). Experimental evidence and modelling in this study show the potential for the existence of microbial methane production in glacially covered organic matter.

  106. 106.

    et al. Groundwater seeps in Taylor Valley Antarctica: an example of a subsurface melt event. Ann. Glaciol. 40, 200–206 (2005).

  107. 107.

    et al. Microbial communities in the subglacial waters of the Vatnajökull ice cap, Iceland. ISME J. 7, 427–437 (2013).

  108. 108.

    , , , & Chemolithotrophic primary production in a subglacial ecosystem. Appl. Environ. Microbiol. 80, 6146–6153 (2014).

  109. 109.

    et al. Deep groundwater and potential subsurface habitats beneath an Antarctic dry valley. Nat. Commun. 6, 6831 (2015).

  110. 110.

    et al. Ice sheets as a significant source of highly reactive nanoparticulate iron to the oceans. Nat. Commun. 5, 3929 (2014).

  111. 111.

    et al. Iron from melting glaciers fuels phytoplankton blooms in the Amundsen Sea (Southern Ocean): phytoplankton characteristics and productivity. Deep. Res. Part II Top. Stud. Oceanogr. 71–76, 32–48 (2012).

  112. 112.

    et al. The potential role of the Antarctic ice sheet in global biogeochemical cycles. Earth Environ. Sci. Trans. R. Soc. Edinburgh 104, 55–67 (2013).

  113. 113.

    & Genomic analysis of cold-active Colwelliaphage 9A and psychrophilic phage–host interactions. Extremophiles 17, 99–114 (2013). This comparative genomic and proteomic analysis of a bacterial virus–host system holding the lower temperature record for viral production (−12 °C) revealed that the only viral cold-active proteins are enzymes involved in cell entry and lysis, disruption of host transcription and protection of the viral genome, which are all essential viral processes. Evidence for lateral gene transfer was also obtained.

  114. 114.

    & Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat. Microb. Ecol. 45, 15–19 (2006).

  115. 115.

    & An inter-order horizontal gene transfer event enables the catabolism of compatible solutes by Colwellia psychrerythraea 34H. Extremophiles 17, 601–610 (2013). In this genomic study, lateral gene transfer was linked to the organism's ability to use compatible solutes in respiration, after their osmoprotective function was no longer needed.

  116. 116.

    , , & Extensive gene acquisition in the extremely psychrophilic bacterial species Psychroflexus torquis and the link to sea-ice ecosystem specialism. Genome Biol. Evol. 6, 133–148 (2014).

  117. 117.

    , & Purification, characterization, and sequencing of an extracellular cold-active aminopeptidase produced by marine psychrophile Colwellia psychrerythraea strain 34H. Appl. Environ. Microbiol. 70, 3321–3328 (2004).

  118. 118.

    , & Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditions. Can. J. Microbiol. 55, 63–72 (2009).

  119. 119.

    et al. A unique capsular polysaccharide structure from the psychrophilic marine bacterium Colwellia psychrerythraea 34H that mimics antifreeze (glyco)proteins. J. Am. Chem. Soc. 137, 179–189 (2015).

  120. 120.

    , , , & Hyperactive antifreeze protein from an Antarctic sea ice bacterium Colwellia sp. has a compound ice-binding site without repetitive sequences. FEBS J. 281, 3576–3590 (2014).

  121. 121.

    et al. Ca2+-stabilized adhesin helps an Antarctic bacterium reach out and bind ice. Biosci. Rep. 34, e00121 (2014).

  122. 122.

    , , & Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl. Environ. Microbiol. 75, 7519–7526 (2009).

  123. 123.

    et al. Microbial sulfur transformations in sediments from Subglacial Lake Whillans. Front. Microbiol. 5, 594 (2014).

  124. 124.

    in Sea Ice — An Introduction to its Physics, Chemistry, Biology and Geology (eds Thomas, D. N. & Dieckmann, G. S.) 247–282 (Blackwell Science Ltd, 2010).

  125. 125.

    , & Review: the Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis. Extremophiles 17, 711–722 (2013).

  126. 126.

    , , , & Widespread, rapid grounding line retreat of Pine Island, Thwaites, Smith, and Kohler glaciers, West Antarctica, from 1992 to 2011. Geophys. Res. Lett. 41, 3502–3509 (2014).

  127. 127.

    , , , & Dust from the dark region in the western ablation zone of the Greenland ice sheet. Cryosphere 5, 589–601 (2011).

  128. 128.

    , , & Stronger ocean circulation and increased melting under Pine Island Glacier ice shelf. Nat. Geosci. 4, 519–523 (2011).

  129. 129.

    in Encyclopedia of Microbiology (ed. Schaechter, M.) 147–158 (Elsevier, 2009).

  130. 130.

    , & An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol. Ecol. 61, 214–221 (2007).

  131. 131.

    , , & Characterization of an antifreeze protein from the polar diatom Fragilariopsis cylindrus and its relevance in sea ice. Cryobiology 63, 210–219 (2011).

  132. 132.

    , , & High concentrations of exopolymeric substances in Arctic winter sea ice: implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep. Res. Part I Oceanogr. Res. Pap. 49, 2163–2181 (2002).

  133. 133.

    , & Exopolymer particles: microbial hotspots of enhanced bacterial activity in Arctic fast ice (Chukchi Sea). Aquat. Microb. Ecol. 52, 195–207 (2008).

  134. 134.

    et al. Dissolved extracellular polymeric substances (dEPS) dynamics and bacterial growth during sea ice formation in an ice tank study. Polar Biol. 35, 661–676 (2012).

  135. 135.

    & Selective retention in saline ice of extracellular polysaccharides produced by the cold-adapted marine bacterium Colwellia psychrerythraea strain 34H. Ann. Glaciol. 52, 111–117 (2011).

  136. 136.

    , , , & Ubiquity of biological ice nucleators in snowfall. Science 319, 1214 (2008).

  137. 137.

    et al. Effect of ice melting on bacterial carbon fluxes channelled by viruses and protists in the Arctic Ocean. Polar Biol. 33, 1695–1707 (2010).

  138. 138.

    , , , & Viral dynamics in cryoconite holes on a High Arctic glacier (Svalbard). J. Geophys. Res. 112, G04S31 (2007).

  139. 139.

    et al. Viral impacts on bacterial communities in Arctic cryoconite. Environ. Res. Lett. 8, 045021 (2013).

  140. 140.

    & Antarctic sea ice viral dynamics over an annual cycle. Polar Biol. 35, 491–497 (2012).

  141. 141.

    & Abundant dissolved genetic material in Arctic sea ice part II: viral dynamics during autumn freeze-up. Polar Biol. 34, 1831–1841 (2011).

  142. 142.

    et al. High diversity of the viral community from an Antarctic lake. Science 326, 858–861 (2009).

  143. 143.

    , & Analysis of virus genomes from glacial environments reveals novel virus groups with unusual host interactions. Front. Microbiol. 6, 656 (2015).

  144. 144.

    et al. High level of intergenera gene exchange shapes the evolution of haloarchaea in an isolated Antarctic lake. Proc. Natl Acad. Sci. USA 110, 16939–16944 (2013).

  145. 145.

    & in Antarctic Subglacial Aquatic Environments (eds Siegert, M. J. & Kennicutt, M. C.) 149–157 (American Geophysical Union, 2011). These authors present recommendations to maintain environmental stewardship when accessing pristine Antarctica subglacial aquatic environments.

  146. 146.

    et al. Entry approach into pristine ice-sealed lakes — Lake Vida, East Antarctica, a model ecosystem. Limnol. Oceanogr. Methods 6, 542–547 (2008).

  147. 147.

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

  148. 148.

    et al. IceMole: a maneuverable probe for clean in situ analysis and sampling of subsurface ice and subglacial aquatic ecosystems. Ann. Glaciol. 55, 14–22 (2014).

  149. 149.

    et al. The dynamic bacterial communities of a melting High Arctic glacier snowpack. ISME J. 7, 1814–1826 (2013).

  150. 150.

    et al. Snow surface microbiome on the High Antarctic Plateau (DOME C). PLoS ONE 9, e104505 (2014).

  151. 151.

    et al. Coupled cryoconite ecosystem structure-function relationships are revealed by comparing bacterial communities in alpine and Arctic glaciers. FEMS Microbiol. Ecol. 89, 222–237 (2014).

  152. 152.

    Bacterial community structure, function and diversity in Antarctic sea ice. Victoria University of Wellington , (2011).

  153. 153.

    Bacterial diversity in sea ice, melt ponds, water column, ice algal aggregates and deep-sea sediments of the Central Arctic Ocean. AWI , (2014).

  154. 154.

    et al. Metagenomic analysis of a permafrost microbial community reveals a rapid response to thaw. Nature 480, 368–371 (2011).

  155. 155.

    , & The structure of bacterial communities in the western Arctic Ocean as revealed by pyrosequencing of 16S rRNA genes. Environ. Microbiol. 12, 1132–1143 (2010).

  156. 156.

    & The identification and physiographical setting of Antarctic subglacial lakes: an update based on recent discoveries. Geophys. Monogr. Ser. 192, 9–26 (2011).

Download references

Acknowledgements

Support was received from the European Research Council (ERC) Adv G (grant 294757 to A.B.), the Natural Environment Research Council (NERC; grant NE/J02399X/1 to A.M.A.), and the National Science Foundation (NSF; grant ARC-1203267 to J.W.D. and grant ANT-1144178 to J.A.M.).

Author information

Affiliations

  1. Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany.

    • Antje Boetius
    •  & Josephine Z. Rapp
  2. Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359 Bremen, Germany.

    • Antje Boetius
    •  & Josephine Z. Rapp
  3. Bristol Glaciology Center, School of Geographical Sciences, University of Bristol, BS8 1SS, UK.

    • Alexandre M. Anesio
  4. School of Oceanography, Box 357940, University of Washington, Seattle, Washington 98195, USA.

    • Jody W. Deming
  5. Department of Biology, 276 Bicentennial Way, Middlebury College, Middlebury, Vermont 05753, USA.

    • Jill A. Mikucki

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Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Antje Boetius.

Glossary

Psychrophilic

Organisms that thrive at low temperatures. From the Greek words psychrós (ψυχρός) meaning cold, and phílos (φίλος) meaning loving.

Extracellular polymeric substances

(EPS). High-molecular-weight, carbohydrate-rich exudates that are released by microorganisms in response to a shift in environmental conditions, including temperature, salinity and nutrient availability. EPS are composed primarily of polysaccharides but can also include proteins, DNA or lipopolysaccharides.

Aquifer

A body of permeable rock that can contain or transmit groundwater.

Albedo

A measure of how much solar energy a surface reflects, whereby light-coloured surfaces such as sea ice reflect more solar energy than dark surfaces such as open water. Dust particles and pigmentation by algal growth on the surface of ice lower albedo by decreasing ice reflectivity.

Cryoconite holes

Small holes (submetre scale) in the ablation zone on glacial ice surfaces. They form as a result of the deposition of cryoconite (a mixture of dark-coloured inorganic and organic particles, including microorganisms), which absorbs solar radiation and causes the ice to melt.

Ablation zones

Areas of a glacier or ice sheet where ice loss (caused by melting, sublimation, evaporation or ice calving) exceeds ice gain (due to snow accumulation).

Accretion ice

Ice that forms when liquid water freezes to the base of a glacier or ice sheet. An example is lake water from Lake Vostok, which has frozen to the base of the ice sheet, forming a layer of accretion ice.

Basal sediments

The loose debris that is produced by glacial erosion of the underlying material at the icebedrock interface of a glacier or ice sheet.

Brine

Salt-rich liquid trapped in channels and pockets within the ice matrix. In very cold sea ice, some sea salts approach saturating levels and precipitate.

Algal mats

A dense accumulation of phototrophic eukaryotic microorganisms, which grow, for example, on the underside of sea ice.

Foraminifera

A group of single-celled eukaryotes with a characteristic calcium carbonate shell and either a planktonic or benthic lifestyle. The remains of their calcareous fossils in seafloor sediments have important roles in paleoclimatology and paleooceanography.

Sympagic meiofauna

Small animals of <1mm in size that inhabit sea ice.

Diatoms

Unicellular algae, with silicate walls, that constitute the major fraction of phytoplankton in most coastal and polar oceans; they are also the dominant primary producers in sea ice.

Grazing pressure

Stress on a population of organisms due to grazing or consumption by other, typically larger organisms.

Proteorhodopsin

A photoactive protein that functions as a light-driven proton pump and is used by some marine microorganisms to generate additional energy.

Polyunsaturated fatty acids

(PUFAs). Lipids that contain carbon backbones with two or more carboncarbon double bonds. They are unsaturated with respect to the number of hydrogen atoms per carbon atom.

Seed communities

The source of organisms to a transient ecosystem.

Glacial runoff

The meltwater draining from glaciers and ice sheets that may come from both surface (supraglacial) and subsurface (subglacial) melt.

Glacier forefields

The terrain most recently exposed by a retreating glacier. This region lies between the current terminus or leading edge of a glacier and the accumulation of glacial debris that marks the previous (greater) extent of the glacier.

Bedrock

The deeper layer of consolidated rock that underlies loose materials, such as soil, gravel and sediment.

Chemolithoautotrophs

Organisms that gain their energy through the oxidation of reduced inorganic compounds and use CO2 as the sole carbon source for growth. The term is often used synonymously with chemoautotrophy and chemosynthesis.

Heterotrophs

Organisms that use organic compounds as their carbon source and obtain energy through the oxidation of these compounds.

Redox chemistry

Pairs of reactions in which one compound becomes oxidized and releases electrons, and the other compound becomes reduced and accepts the released electrons.

Remotely operated vehicles

(ROVs). Tethered unmanned underwater robots often used for deep-water research or industrial purposes.

Methanogenesis

The biological production of methane (CH4) in an anaerobic process mediated exclusively by methanogenic archaea.

Phylotypes

Different taxonomic groups of microorganisms that can be determined by comparative analyses of their 16S rRNA gene sequences.

Calvin cycle

A series of biochemical reactions used by many photosynthetic organisms to convert CO2 into organic compounds.

Isotopic signature

The ratio of isotopes of a particular element in a molecule of interest, as measured by isotope ratio mass spectrometry.

Ice-binding proteins

Proteins used by microorganisms to prevent or limit the growth of ice structures within or outside of their body fluids, by, for example, adhering to the ice or otherwise inhibiting ice crystal growth or recrystallization.

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DOI

https://doi.org/10.1038/nrmicro3522

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