Microbial Life in Supraglacial Environments

  • Arwyn EdwardsEmail author
  • Karen A. Cameron


Supraglacial environments occupy 11% of Earth’s surface area and represent a critical interface between climate and ice. This century has brought a renewed appreciation that glacier surfaces represent a collective of diverse microbial niches which occur wherever sufficient liquid water is available to support microbial activity: even at the microscopic scales of ice crystal boundaries within the crystalline matrices of snow or glacial ice. Within this chapter, we review the range of microbial habitats associated with snowpacks, the glacial ice photic zone, and phototrophic microbial biofilms formed by supraglacial algae or by the darkening of microbe–mineral aggregates known as cryoconite. In summary, glacier surfaces are home to surprisingly biodiverse and active microbial communities despite their low temperatures and austere conditions. Consequently, microbial communities and their processes are interposed between climate and ice and merit urgent consideration in the light of the effects of climate warming on Earth’s supraglacial environments.


  1. Abbot DS, Pierrehumbert RT (2010) Mudball: surface dust and snowball Earth deglaciation. J Geophys Res 115(D3):D03104. doi: 10.1029/2009jd012007 CrossRefGoogle Scholar
  2. Amato P, Parazols M, Sancelme M, Laj P, Mailhot G, Delort A-M (2007) Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures. FEMS Microbiol Ecol 59(2):242–254. doi: 10.1111/j.1574-6941.2006.00199.x PubMedCrossRefGoogle Scholar
  3. Amoroso A, Domine F, Esposito G, Morin S, Savarino J, Nardino M, Montagnoli M, Bonneville JM, Clement JC, Ianniello A, Beine HJ (2009) Microorganisms in dry polar snow are involved in the exchanges of reactive nitrogen species with the atmosphere. Environ Sci Technol 44(2):714–719. doi: 10.1021/es9027309 CrossRefGoogle Scholar
  4. Andrews TD, MacKay G (2012) The archaeology and paleoecology of alpine ice patches: a global perspective. Arctic 65(5):iii–iviGoogle Scholar
  5. Anesio AM, Laybourn-Parry J (2012) Glaciers and ice sheets as a biome. Trends Ecol Evol 27(4):219–225PubMedCrossRefGoogle Scholar
  6. Anesio AM, Hodson AJ, Fritz A, Psenner R, Sattler B (2009) High microbial activity on glaciers: importance to the global carbon cycle. Glob Change Biol 15(4):955–960. doi: 10.1111/j.1365-2486.2008.01758.x CrossRefGoogle Scholar
  7. Benn D, Evans DJ (2014) Glaciers and glaciation. Routledge, AbingdonGoogle Scholar
  8. Bidle KD, Lee S, Marchant DR, Falkowski PG (2007) Fossil genes and microbes in the oldest ice on Earth. Proc Natl Acad Sci 104(33):13455–13460. doi: 10.1073/pnas.0702196104 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Björkman MP, Zarsky JD, Kühnel R, Hodson A, Sattler B, Psenner R (2014) Microbial cell retention in a melting high Arctic snowpack, Svalbard. Arct Antarct Alp Res 46(2):471–482CrossRefGoogle Scholar
  10. Blazewicz SJ, Barnard RL, Daly RA, Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7(11):2061–2068. doi: 10.1038/ismej.2013.102 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Boyd ES, Skidmore M, Mitchell AC, Bakermans C, Peters JW (2010) Methanogenesis in subglacial sediments. Environ Microbiol Rep 2(5):685–692. doi: 10.1111/j.1758-2229.2010.00162.x PubMedCrossRefGoogle Scholar
  12. Boyd ES, Lange RK, Mitchell AC, Havig JR, Hamilton TL, Lafrenière MJ, Shock EL, Peters JW, Skidmore M (2011) Diversity, abundance, and potential activity of nitrifying and nitrate-reducing microbial assemblages in a subglacial ecosystem. Appl Environ Microbiol 77(14):4778–4787. doi: 10.1128/aem.00376-11 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brown SP, Olson BJ, Jumpponen A (2015) Fungi and algae co-occur in snow: an issue of shared habitat or algal facilitation of heterotrophs? Arct Antarct Alp Res 47(4):729–749CrossRefGoogle Scholar
  14. Brown SP, Ungerer MC, Jumpponen A, Graham LE (2016) A community of clones: snow algae are diverse communities of spatially structured clones. Int J Plant Sci 177(5):432–439CrossRefGoogle Scholar
  15. Cameron K, Hodson AJ, Osborn AM (2012a) Carbon and nitrogen biogeochemical cycling potentials of supraglacial cryoconite communities. Polar Biol 35(9):1375–1393. doi: 10.1007/s00300-012-1178-3 CrossRefGoogle Scholar
  16. Cameron KA, Hodson AJ, Osborn AM (2012b) Structure and diversity of bacterial, eukaryotic and archaeal communities in glacial cryoconite holes from the Arctic and the Antarctic. FEMS Microbiol Ecol 82:254–267. doi: 10.1111/j.1574-6941.2011.01277.x PubMedCrossRefGoogle Scholar
  17. Cameron KA, Hagedorn B, Dieser M, Christner BC, Choquette K, Sletten R, Crump B, Kellogg C, Junge K (2014) Diversity and potential sources of microbiota associated with snow on western portions of the Greenland Ice Sheet. Environ Microbiol 17:594–609PubMedCrossRefGoogle Scholar
  18. Carpenter EJ, Lin S, Capone DG (2000) Bacterial activity in South Pole snow. Appl Environ Microbiol 66(10):4514–4517PubMedPubMedCentralCrossRefGoogle Scholar
  19. Castello JD, Rogers SO (2005) Life in ancient ice. Princeton University Press, Princeton, NJCrossRefGoogle Scholar
  20. Choudhari S, Smith S, Owens S, Gilbert JA, Shain DH, Dial RJ, Grigoriev A (2013) Metagenome sequencing of prokaryotic microbiota collected from Byron Glacier, Alaska. Genome Announc 1(2):e0009913. doi: 10.1128/genomeA.00099-13 PubMedCrossRefGoogle Scholar
  21. Chrismas NAM, Anesio A, Sanchez-Baracaldo P (2015) Multiple adaptations to polar and alpine environments within cyanobacteria: a phylogenomic and Bayesian approach. Front Microbiol 6:1070PubMedPubMedCentralCrossRefGoogle Scholar
  22. Chrismas NA, Barker G, Anesio AM, Sánchez-Baracaldo P (2016) Genomic mechanisms for cold tolerance and production of exopolysaccharides in the Arctic cyanobacterium Phormidesmis priestleyi BC1401. BMC Genom 17(1):533CrossRefGoogle Scholar
  23. Christner BC, Morris CE, Foreman CM, Cai R, Sands DC (2008) Ubiquity of biological ice nucleators in snowfall. Science 319(5867):1214. doi: 10.1126/science.1149757 PubMedCrossRefGoogle Scholar
  24. Cook J, Hodson A, Telling J, Anesio A, Irvine-Fynn T, Bellas C (2010) The mass-area relationship within cryoconite holes and its implications for primary production. Ann Glaciol 51(56):106–110. doi: 10.3189/172756411795932038 CrossRefGoogle Scholar
  25. Cook JM, Hodson AJ, Anesio AM, Hanna E, Yallop M, Stibal M, Telling J, Huybrechts P (2012) An improved estimate of microbially mediated carbon fluxes from the Greenland ice sheet. J Glaciol 58(212):1098–1108CrossRefGoogle Scholar
  26. Cook J, Edwards A, Hubbard A (2015a) Biocryomorphology: integrating microbial processes with ice surface hydrology, topography and roughness. Front Earth Sci 3:78. doi: 10.3389/feart.2015.00078 CrossRefGoogle Scholar
  27. Cook JM, Hodson AJ, Irvine-Fynn TDL (2015b) Supraglacial weathering crust dynamics inferred from cryoconite hole hydrology. Hydrol Process 30:433–443. doi: 10.1002/hyp.10602 CrossRefGoogle Scholar
  28. Cook J, Edwards A, Takeuchi N, Irvine-Fynn T (2016a) Cryoconite: the dark biological secret of the cryosphere. Prog Phys Geogr 40(1):66–111CrossRefGoogle Scholar
  29. Cook J, Edwards A, Bulling M, Mur L, Cook S, Gokul J, Cameron K, Sweet M, Irvine-Fynn T (2016b) Metabolome-mediated biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes. Environ Microbiol 18(12):4674–4686. doi: 10.1111/1462-2920.13349 PubMedCrossRefGoogle Scholar
  30. Darcy JL, Lynch RC, King AJ, Robeson MS, Schmidt SK (2011) Global distribution of Polaromonas phylotypes – evidence for a highly successful dispersal capacity. PLoS ONE 6(8):e23742PubMedPubMedCentralCrossRefGoogle Scholar
  31. Davies TD, Brimblecombe P, Tranter M, Tsiouris S, Vincent CE, Abrahams P, Blackwood IL (1987) The removal of soluble ions from melting snowpacks. In: Jones HG, Orville-Thomas WJ (eds) Seasonal snowcovers: physics, chemistry, hydrology. Springer Netherlands, Dordrecht, pp 337–392. doi: 10.1007/978-94-009-3947-9_20 CrossRefGoogle Scholar
  32. Desmet WH, Vanrompus EA (1994) Rotifera and Tardigrada from some cryoconite holes on a Spitsbergen (Svalbard) Glacier. Belg J Zool 124(1):27–37Google Scholar
  33. Edwards A, Anesio AM, Rassner SM, Sattler B, Hubbard B, Perkins WT, Young M, Griffith GW (2011) Possible interactions between bacterial diversity, microbial activity and supraglacial hydrology of cryoconite holes in Svalbard. ISME J 5:150–160. doi: 10.1038/ismej.2010.100 PubMedCrossRefGoogle Scholar
  34. Edwards A, Douglas B, Anesio AM, Rassner SM, Irvine-Fynn TDL, Sattler B, Griffith GW (2013a) A distinctive fungal community inhabiting cryoconite holes on glaciers in Svalbard. Fung Ecol 6(2):168–176. doi: 10.1016/j.funeco.2012.11.001 CrossRefGoogle Scholar
  35. Edwards A, Pachebat JA, Swain M, Hegarty M, Hodson A, Irvine-Fynn TDL, Rassner SME, Sattler B (2013b) A metagenomic snapshot of taxonomic and functional diversity in an alpine glacier cryoconite ecosystem. Environ Res Lett 8(3):035003CrossRefGoogle Scholar
  36. Edwards A, Rassner SM, Anesio AM, Worgan H, Irvine-Fynn T, Williams HW, Sattler B, Griffith GW (2013c) Contrasts between the cryoconite and ice-marginal bacterial communities of Svalbard glaciers. Polar Res 32:19468CrossRefGoogle Scholar
  37. Edwards A, Irvine-Fynn T, Mitchell AC, Rassner SME (2014a) A germ theory for glacial systems? Wiley Interdiscip Rev Water 1:331–340. doi: 10.1002/wat2.1029 Google Scholar
  38. Edwards A, Mur LAJ, Girdwood S, Anesio A, Stibal M, Rassner SM, Hell K, Pachebat JA, Post B, Bussell J, Cameron SJ, Griffith GW, Hodson AJ, Sattler B (2014b) Coupled cryoconite ecosystem structure-function relationships are revealed by comparing bacterial communities in Alpine and Arctic glaciers. FEMS Microbiol Ecol 89:222–237PubMedCrossRefGoogle Scholar
  39. Feng L, Xu J, Kang S, Li X, Li Y, Jiang B, Shi Q (2016) Chemical composition of microbe-derived dissolved organic matter in cryoconite in Tibetan Plateau glaciers: insights from Fourier transform ion cyclotron resonance mass spectrometry analysis. Environ Sci Technol 50(24):13215–13223PubMedCrossRefGoogle Scholar
  40. Fettweis X, van Ypersele JP, Gallée H, Lefebre F, Lefebvre W (2007) The 1979–2005 Greenland ice sheet melt extent from passive microwave data using an improved version of the melt retrieval XPGR algorithm. Geophys Res Lett 34(5):L05502CrossRefGoogle Scholar
  41. FitzGerald DM, Fenster MS, Argow BA, Buynevich IV (2008) Coastal impacts due to sea-level rise. Annu Rev Earth Planet Sci 36:601–647CrossRefGoogle Scholar
  42. Forster RR, Box JE, van den Broeke MR, Miege C, Burgess EW, van Angelen JH, Lenaerts JTM, Koenig LS, Paden J, Lewis C, Gogineni SP, Leuschen C, McConnell JR (2013) Extensive liquid meltwater storage in firn within the Greenland ice sheet. Nat Geosci 7:95–98CrossRefGoogle Scholar
  43. Franzetti A, Tatangelo V, Gandolfi I, Bertolini V, Bestetti G, Diolaiuti G, D’Agata C, Mihalcea C, Smiraglia C, Ambrosini R (2013) Bacterial community structure on two alpine debris-covered glaciers and biogeography of Polaromonas phylotypes. ISME J 7:1483–1492PubMedPubMedCentralCrossRefGoogle Scholar
  44. Franzetti A, Tagliaferri I, Gandolfi I, Bestetti G, Minora U, Mayer C, Azzoni RS, Diolaiuti G, Smiraglia C, Ambrosini R (2016) Light-dependent microbial metabolisms drive carbon fluxes on glacier surfaces. ISME J 10:2984–2988PubMedCrossRefGoogle Scholar
  45. Fuhrman J, Steele J (2008) Community structure of marine bacterioplankton: patterns, networks, and relationships to function. Aquat Microb Ecol 53(1):69–81. doi: 10.3354/ame01222 CrossRefGoogle Scholar
  46. Gokul JK, Hodson AJ, Saetnan ER, Irvine-Fynn TD, Westall PJ, Detheridge AP, Takeuchi N, Bussell J, Mur LA, Edwards A (2016) Taxon interactions control the distributions of cryoconite bacteria colonizing a High Arctic ice cap. Mol Ecol 25:3752–3767PubMedCrossRefGoogle Scholar
  47. Gribbon PWF (1979) Cryoconite holes on Sermikavask, West Greenland. J Glaciol 22(86):177–181CrossRefGoogle Scholar
  48. Hamilton TL, Peters JW, Skidmore ML, Boyd ES (2013) Molecular evidence for an active endogenous microbiome beneath glacial ice. ISME J 7:1402–1412PubMedPubMedCentralCrossRefGoogle Scholar
  49. Harding T, Jungblut AD, Lovejoy C, Vincent WF (2011) Microbes in High Arctic snow and implications for the cold biosphere. Appl Environ Microbiol 77(10):3234–3243. doi: 10.1128/aem.02611-10 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Hawkings JR, Wadham JL, Tranter M, Raiswell R, Benning LG, Statham PJ, Tedstone A, Nienow P, Lee K, Telling J (2014) Ice sheets as a significant source of highly reactive nanoparticulate iron to the oceans. Nat Commun 5:3929. doi: 10.1038/ncomms4929 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hell K, Edwards A, Zarsky J, Podmirseg SM, Girdwood S, Pachebat JA, Insam H, Sattler B (2013) The dynamic bacterial communities of a melting high Arctic glacier snowpack. ISME J 7(9):1814–1826PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hodson AJ (2014) Understanding the dynamics of black carbon and associated contaminants in glacial systems. Wiley Interdiscip Rev Water 1(2):141–149. doi: 10.1002/wat2.1016 CrossRefGoogle Scholar
  53. Hodson AJ, Mumford PN, Kohler J, Wynn PM (2005) The high Arctic glacial ecosystem: new insights from nutrient budgets. Biogeochemistry 72(2):233–256. doi: 10.1007/s10533-004-0362-0 CrossRefGoogle Scholar
  54. Hodson A, Anesio AM, Tranter M, Fountain A, Osborn M, Priscu J, Laybourn-Parry J, Sattler B (2008) Glacial ecosystems. Ecol Monogr 78(1):41–67CrossRefGoogle Scholar
  55. Hodson A, Cameron K, Bøggild C, Irvine-Fynn T, Langford H, Pearce D, Banwart S (2010) The structure, biogeochemistry and formation of cryoconite aggregates upon an Arctic valley glacier; Longyearbreen, Svalbard. J Glaciol 56(196):349–362CrossRefGoogle Scholar
  56. Hodson A, 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 59(214):255–268CrossRefGoogle Scholar
  57. Hoffman PF (2016) Cryoconite pans on Snowball Earth: supraglacial oases for Cryogenian eukaryotes? Geobiology 14(6):531–542. doi: 10.1111/gbi.12191 PubMedCrossRefGoogle Scholar
  58. Hoffman PF, Kaufman AJ, Halverson GP, Schrag DP (1998) A neoproterozoic snowball Earth. Science 281(5381):1342–1346. doi: 10.1126/science.281.5381.1342 PubMedCrossRefGoogle Scholar
  59. Hood E, Fellman J, Spencer RG, Hernes PJ, Edwards R, D’Amore D, Scott D (2009) Glaciers as a source of ancient and labile organic matter to the marine environment. Nature 462(7276):1044–1047PubMedCrossRefGoogle Scholar
  60. Hood E, Battin TJ, Fellman J, O’Neel S, Spencer RGM (2015) Storage and release of organic carbon from glaciers and ice sheets. Nat Geosci 8(2):91–96. doi: 10.1038/ngeo2331 CrossRefGoogle Scholar
  61. Hubbard B, Glasser NF (2005) Field techniques in glaciology and glacial geomorphology. Wiley, ChichesterGoogle Scholar
  62. Irvine-Fynn TDL, Edwards A (2013) A frozen asset: the potential of flow cytometry in constraining the glacial biome. Cytometry A 85(1):3–7. doi: 10.1002/cyto.a.22411 PubMedCrossRefGoogle Scholar
  63. Irvine-Fynn TDL, Bridge JW, Hodson AJ (2011a) In situ quantification of supraglacial cryoconite morpho-dynamics using time-lapse imaging: an example from Svalbard. J Glaciol 57:651–657CrossRefGoogle Scholar
  64. Irvine-Fynn TDL, Hodson AJ, Moorman BJ, Vatne G, Hubbard AL (2011b) Polythermal glacier hydrology: a review. Rev Geophys 49(4):RG4002. doi: 10.1029/2010rg000350 CrossRefGoogle Scholar
  65. Irvine-Fynn TDL, Edwards A, Newton S, Langford H, Rassner SM, Telling J, Anesio AM, Hodson AJ (2012) Microbial cell budgets of an Arctic glacier surface quantified using flow cytometry. Environ Microbiol 14(11):2998–3012. doi: 10.1111/j.1462-2920.2012.02876.x PubMedCrossRefGoogle Scholar
  66. Irvine-Fynn TD, Sanz-Ablanedo E, Rutter N, Smith MW, Chandler JH (2014) Measuring glacier surface roughness using plot-scale, close-range digital photogrammetry. J Glaciol 60(223):957–969CrossRefGoogle Scholar
  67. Joughin I, Smith BE, Medley B (2014) Marine ice sheet collapse potentially under way for the Thwaites Glacier Basin, West Antarctica. Science 344(6185):735–738. doi: 10.1126/science.1249055 PubMedCrossRefGoogle Scholar
  68. Kol E (1942) The snow and ice algae of Alaska. Smithsonian Miscellaneous Collections 101:1–36Google Scholar
  69. Kuhn M (2001) The nutrient cycle through snow and ice, a review. Aquat Sci 63(2):150–167CrossRefGoogle Scholar
  70. Langford H, Hodson A, Banwart S, Bøggild C (2010) The microstructure and biogeochemistry of Arctic cryoconite granules. Ann Glaciol 51(56):87–94CrossRefGoogle Scholar
  71. Langford HJ, Irvine-Fynn TDL, Edwards A, Banwart SA, Hodson AJ (2014) A spatial investigation of the environmental controls over cryoconite aggregation on Longyearbreen glacier, Svalbard. Biogeosciences 11(19):5365–5380. doi: 10.5194/bg-11-5365-2014 CrossRefGoogle Scholar
  72. Larose C, Berger S, Ferrari C, Navarro E, Dommergue A, Schneider D, Vogel T (2010) Microbial sequences retrieved from environmental samples from seasonal Arctic snow and meltwater from Svalbard, Norway. Extremophiles 14(2):205–212. doi: 10.1007/s00792-009-0299-2 PubMedCrossRefGoogle Scholar
  73. Larose C, Dommergue A, Vogel TM (2013) The dynamic arctic snow pack: an unexplored environment for microbial diversity and activity. Biology 2(1):317–330PubMedPubMedCentralCrossRefGoogle Scholar
  74. Lawson EC, Wadham JL, Tranter M, Stibal M, Lis GP, Butler CE, Laybourn-Parry J, Nienow P, Chandler D, Dewsbury P (2014) Greenland Ice Sheet exports labile organic carbon to the Arctic oceans. Biogeosciences 11(14):4015–4028CrossRefGoogle Scholar
  75. Lazzaro A, Wismer A, Schneebeli M, Erny I, Zeyer J (2015) Microbial abundance and community structure in a melting alpine snowpack. Extremophiles 19(3):631–642PubMedCrossRefGoogle Scholar
  76. Liu Y, Priscu JC, Yao T, Vick-Majors TJ, Xu B, Jiao N, Santibáñez P, Huang S, Wang N, Greenwood M (2016) Bacterial responses to environmental change on the Tibetan Plateau over the past half century. Environ Microbiol 18(6):1930–1941PubMedCrossRefGoogle Scholar
  77. Lopatina A, Krylenkov V, Severinov K (2013) Activity and bacterial diversity of snow around Russian Antarctic stations. Res Microbiol 164(9):949–958PubMedCrossRefGoogle Scholar
  78. Lopatina A, Medvedeva S, Shmakov S, Logacheva MD, Krylenkov V, Severinov K (2016) Metagenomic analysis of bacterial communities of Antarctic surface snow. Front Microbiol 7:398PubMedPubMedCentralCrossRefGoogle Scholar
  79. Lutz S, Anesio AM, Villar SEJ, Benning LG (2014) Variations of algal communities cause darkening of a Greenland glacier. FEMS Microbiol Ecol 89(2):402–414PubMedCrossRefGoogle Scholar
  80. Lutz S, Anesio AM, Edwards A, Benning LG (2015) Microbial diversity on Icelandic glaciers and ice caps. Front Microbiol 6:307PubMedPubMedCentralGoogle Scholar
  81. Lutz S, Anesio AM, Edwards A, Benning LG (2016a) Linking microbial diversity and functionality of arctic glacial surface habitats. Environ Microbiol. doi: 10.1111/1462-2920.13494 Google Scholar
  82. Lutz S, Anesio AM, Raiswell R, Edwards A, Newton RJ, Gill F, Benning LG (2016b) The biogeography of red snow microbiomes and their role in melting arctic glaciers. Nat Commun 7:11968PubMedPubMedCentralCrossRefGoogle Scholar
  83. Maccario L, Vogel TM, Larose C (2014) Potential drivers of microbial community structure and function in Arctic spring snow. Front Microbiol 5:413PubMedPubMedCentralCrossRefGoogle Scholar
  84. Mader HM, Pettitt ME, Wadham JL, Wolff EW, Parkes RJ (2006) Subsurface ice as a microbial habitat. Geology 34(3):169–172. doi: 10.1130/G22096.1 CrossRefGoogle Scholar
  85. Mattes TE, Alexander AK, Richardson PM, Munk AC, Han CS, Stothard P, Coleman NV (2008) The Genome of Polaromonas sp. strain JS666: insights into the evolution of a hydrocarbon- and xenobiotic-degrading bacterium, and features of relevance to biotechnology. Appl Environ Microbiol 74(20):6405–6416. doi: 10.1128/aem.00197-08 PubMedPubMedCentralCrossRefGoogle Scholar
  86. McGee D, Broecker WS, Winckler G (2010) Gustiness: the driver of glacial dustiness? Quat Sci Rev 29(17–18):2340–2350CrossRefGoogle Scholar
  87. Meier MF, Dyurgerov MB, Rick UK, O’Neel S, Pfeffer WT, Anderson RS, Anderson SP, Glazovsky AF (2007) Glaciers dominate eustatic sea-level rise in the 21st century. Science 317(5841):1064–1067PubMedCrossRefGoogle Scholar
  88. Müller F, Keeler CM (1969) Errors in short-term ablation measurements on melting ice surfaces. J Glaciol 8(52):91–105CrossRefGoogle Scholar
  89. Nagatsuka N, Takeuchi N, Nakano T, Shin K, Kokado E (2014) Geographical variations in Sr and Nd isotopic ratios of cryoconite on Asian glaciers. Environ Res Lett 9(4):045007CrossRefGoogle Scholar
  90. Nghiem SV, Hall DK, Mote TL, Tedesco M, Albert MR, Keegan K, Shuman CA, DiGirolamo NE, Neumann G (2012) The extreme melt across the Greenland ice sheet in 2012. Geophys Res Lett 39:L20502. doi: 10.1029/2012gl053611 CrossRefGoogle Scholar
  91. Pachauri RK, Allen MR, Barros V, Broome J, Cramer W, Christ R, Church J, Clarke L, Dahe Q, Dasgupta P (2014) Climate change 2014: synthesis Report. Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. IPCC, Geneva, SwitzerlandGoogle Scholar
  92. Pantanella F, Berlutti F, Passariello C, Sarli S, Morea C, Schippa S (2007) Violacein and biofilm production in Janthinobacterium lividum. J Appl Microbiol 102(4):992–999. doi: 10.1111/j.1365-2672.2006.03155.x PubMedGoogle Scholar
  93. Paterson W (1994) The Physics of Glaciers. Butterworth-Heinemann, Burlington, MAGoogle Scholar
  94. Pearce DA, Bridge PD, Hughes KA, Sattler B, Psenner R, Russell NJ (2009) Microorganisms in the atmosphere over Antarctica. FEMS Microbiol Ecol 69(2):143–157. doi: 10.1111/j.1574-6941.2009.00706.x PubMedCrossRefGoogle Scholar
  95. Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola JM, Basile I, Bender M, Chappellaz J, Davis M, Delaygue G, Delmotte M, Kotlyakov VM, Legrand M, Lipenkov VY, Lorius C, Pepin L, Ritz C, Saltzman E, Stievenard M (1999) Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399(6735):429–436CrossRefGoogle Scholar
  96. Pfeffer WT, Arendt AA, Bliss A, Bolch T, Cogley JG, Gardner AS, Hagen J-O, Hock R, Kaser G, Kienholz C, Miles ES, Moholdt G, Mölg N, Paul F, Radic V, Rastner P, Raup BH, Rich J, Sharp MJ, Consortium R (2014) The Randolph glacier inventory (2014): a globally complete inventory of glaciers. J Glaciol 60:221. doi: 10.3189/2014JoG13J176 CrossRefGoogle Scholar
  97. Ransom-Jones E, Jones DL, Edwards A, McDonald JE (2014) Distribution and diversity of members of the bacterial phylum Fibrobacteres in environments where cellulose degradation occurs. Syst Appl Microbiol 37(7):502–509PubMedCrossRefGoogle Scholar
  98. Rassner SME, Anesio A, Girdwood SE, Hell K, Gokul J, Whitworth DE, Edwards A (2016) Can the bacterial community of a high Arctic glacier surface escape viral control? Front Microbiol 7:956PubMedPubMedCentralCrossRefGoogle Scholar
  99. Remias D (2012) Cell structure and physiology of alpine snow and ice algae. In: Lütz C (ed) Plants in Alpine regions. Springer, New York, NY, pp 175–185CrossRefGoogle Scholar
  100. Remias D, Lütz-Meindl U, Lütz C (2005) Photosynthesis, pigments and ultrastructure of the alpine snow alga Chlamydomonas nivalis. Eur J Phycol 40(3):259–268CrossRefGoogle Scholar
  101. Remias D, Holzinger A, Lütz C (2009) Ultrastructure and physiological characterization of the ice alga Mesotaenium berggrenii (Zygnemaphyceae, Chlorophyta) from glaciers in the European alps. Phycologia 48:302–312CrossRefGoogle Scholar
  102. Remias D, Holzinger A, Aigner S, Lütz C (2012a) Ecophysiology and ultrastructure of Ancylonema nordenskiöldii (Zygnematales, Streptophyta), causing brown ice on glaciers in Svalbard (high arctic). Polar Biol 35(6):899–908CrossRefGoogle Scholar
  103. Remias D, Schwaiger S, Aigner S, Leya T, Stuppner H, Lütz C (2012b) Characterization of an UV- and VIS-absorbing, purpurogallin-derived secondary pigment new to algae and highly abundant in Mesotaenium berggrenii (Zygnematophyceae, Chlorophyta), an extremophyte living on glaciers. FEMS Microbiol Ecol 79(3):638–648PubMedCrossRefGoogle Scholar
  104. Rodrigues DF, Tiedje JM (2008) Coping with our cold planet. Appl Environ Microbiol 74(6):1677–1686. doi: 10.1128/aem.02000-07 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Rohde RA, Price PB (2007) Diffusion-controlled metabolism for long-term survival of single isolated microorganisms trapped within ice crystals. Proc Natl Acad Sci 104(42):16592–16597. doi: 10.1073/pnas.0708183104 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Sattler B, Puxbaum H, Psenner R (2001) Bacterial growth in supercooled cloud droplets. Geophys Res Lett 28(2):239–242. doi: 10.1029/2000gl011684 CrossRefGoogle Scholar
  107. Säwström C, Mumford P, Marshall W, Hodson A, Laybourn-Parry J (2002) The microbial communities and primary productivity of cryoconite holes in an Arctic glacier (Svalbard 79°N). Polar Biol 25(8):591–596. doi: 10.1007/s00300-002-0388-5 Google Scholar
  108. Segawa T, Ishii S, Ohte N, Akiyoshi A, Yamada A, Maruyama F, Li Z, Hongoh Y, Takeuchi N (2014) The nitrogen cycle in cryoconites: naturally occurring nitrification-denitrification granules on a glacier. Environ Microbiol 16(10):3250–3262. doi: 10.1111/1462-2920.12543 PubMedCrossRefGoogle Scholar
  109. Shiklomanov I (1993) World freshwater resources. In: Gleick PH (ed) Water in crisis: a guide to the world’s fresh water resources. Oxford University Press, New York, NY, pp 13–14Google Scholar
  110. Simon C, Wiezer A, Strittmatter AW, Daniel R (2009) Phylogenetic diversity and metabolic potential revealed in a glacier ice metagenome. Appl Environ Microbiol 75(23):7519–7526. doi: 10.1128/aem.00946-09 PubMedPubMedCentralCrossRefGoogle Scholar
  111. Singer GA, Fasching C, Wilhelm L, Niggemann J, Steier P, Dittmar T, Battin TJ (2012) Biogeochemically diverse organic matter in Alpine glaciers and its downstream fate. Nat Geosci 5(10):710–714CrossRefGoogle Scholar
  112. Smith HJ, Schmit A, Foster R, Littman S, Kuypers MM, Foreman CM (2016) Biofilms on glacial surfaces: hotspots for biological activity. NPJ Biofilms Microbiomes 2:16008CrossRefGoogle Scholar
  113. Spijkerman E, Wacker A, Weithoff G, Leya T (2012) Elemental and fatty acid composition of snow algae in Arctic habitats. Front Microbiol 3:380PubMedPubMedCentralCrossRefGoogle Scholar
  114. Stanish LF, Bagshaw EA, McKnight DM, Fountain AG, Tranter M (2013) Environmental factors influencing diatom communities in Antarctic cryoconite holes. Environ Res Lett 8(4):045006CrossRefGoogle Scholar
  115. Stibal M, Sabacka M, Kastovska K (2006) Microbial communities on glacier surfaces in Svalbard: Impact of physical and chemical properties on abundance and structure of cyanobacteria and algae. Microb Ecol 52(4):644–654. doi: 10.1007/s00248-006-9083-3 PubMedCrossRefGoogle Scholar
  116. Stibal M, Gözdereliler E, Cameron KA, Box JE, Stevens IT, Gokul JK, Schostag M, Zarsky JD, Edwards A, Irvine-Fynn TD (2015a) Microbial abundance in surface ice on the Greenland Ice Sheet. Front Microbiol 6:225PubMedPubMedCentralCrossRefGoogle Scholar
  117. Stibal M, Schostag M, Cameron KA, Hansen LH, Chandler DM, Wadham JL, Jacobsen CS (2015b) Different bulk and active bacterial communities in cryoconite from the margin and interior of the Greenland ice sheet. Environ Microbiol Rep 7(2):293–300PubMedCrossRefGoogle Scholar
  118. Takeuchi N (2002) Optical characteristics of cryoconite (surface dust) on glaciers: the relationship between light absorency and the property of organic matter contained in the cryoconite. Ann Glaciol 34:409–414CrossRefGoogle Scholar
  119. Takeuchi N, Kohshima S, Goto-Azuma K, Koerner R (2001a) Biological characteristics of dark colored material (cryoconite) on Canadian Arctic glaciers (Devon and Penny ice caps). Memoirs of the National Institute of Polar Research 54:495–505Google Scholar
  120. Takeuchi N, Kohshima S, Seko K (2001b) Structure, formation, and darkening process of albedo-reducing material (cryoconite) on a Himalayan glacier: a granular algal mat growing on the glacier. Arct Antarct Alp Res 33(2):115–122CrossRefGoogle Scholar
  121. Tedesco M, Doherty S, Fettweis X, Alexander P, Jeyaratnam J, Noble E, Stroeve J (2016) The darkening of the Greenland ice sheet: trends, drivers and projections (1981–2100). Cryosphere 10:477–496CrossRefGoogle Scholar
  122. Telling J, Anesio AM, Tranter M, Irvine-Fynn T, Hodson A, Butler C, Wadham J (2011) Nitrogen fixation on Arctic glaciers, Svalbard. J Geophys Res-Biogeosci 116:G03039. doi: 10.1029/2010jg001632 CrossRefGoogle Scholar
  123. Telling J, Anesio AM, Tranter M, Stibal M, Hawkings J, Irvine-Fynn T, Hodson A, Butler C, Yallop M, Wadham J (2012a) Controls on the autochthonous production and respiration of organic matter in cryoconite holes on high Arctic glaciers. J Geophys Res 117(G1):G01017. doi: 10.1029/2011jg001828 CrossRefGoogle Scholar
  124. Telling J, Stibal M, Anesio AM, Tranter M, Nias I, Cook J, Lis G, Wadham JL, Sole A, Nienow P, Hodson A (2012b) Microbial nitrogen cycling on the Greenland ice sheet. Biogeosci Discuss 9:2431–2442. doi: 10.5194/bgd-8-10423-2011 CrossRefGoogle Scholar
  125. Temkiv TŠ, Finster K, Hansen BM, Nielsen NW, Karlson UG (2011) The microbial diversity of a storm cloud as assessed by hailstones. FEMS Microbiol Ecol 81(3):684–695. doi: 10.1111/j.1574-6941.2012.01402.x CrossRefGoogle Scholar
  126. Temkiv TŠ, Finster K, Hansen BM, Pašić L, Karlson UG (2013) Viable methanotrophic bacteria enriched from air and rain can oxidize methane at cloud-like conditions. Aerobiologia 29(3):373–384. doi: 10.1007/s10453-013-9287-1 CrossRefGoogle Scholar
  127. Tranter M, Fountain AG, Fritsen CH, Berry Lyons W, Priscu JC, Statham PJ, Welch KA (2004) Extreme hydrochemical conditions in natural microcosms entombed within Antarctic ice. Hydrol Process 18(2):379–387. doi: 10.1002/hyp.5217 CrossRefGoogle Scholar
  128. Uetake J, Naganuma T, Hebsgaard MB, Kanda H, Kohshima S (2010) Communities of algae and cyanobacteria on glaciers in west Greenland. Polar Sci 4(1):71–80CrossRefGoogle Scholar
  129. Uetake J, Tanaka S, Hara K, Tanabe Y, Samyn D, Motoyama H, Imura S, Kohshima S (2014) Novel biogenic aggregation of moss gemmae on a disappearing African glacier. PLoS ONE 9(11):e112510PubMedPubMedCentralCrossRefGoogle Scholar
  130. van Leewenhoeck A (1677) Observations, Communicated to the Publisher by Mr. Antony van Leewenhoeck, in a Dutch Letter of the 9th of Octob. 1676. Here English'd: concerning little animals by him observed in rain-well-sea and snow water; as also in water wherein pepper had lain infused. Phil Trans 12(133–142):821–831. doi: 10.1098/rstl.1677.0003 CrossRefGoogle Scholar
  131. Vonnahme T, Devetter M, Žárský J, Šabacká M, Elster J (2015) Controls on microalgal community structures in cryoconite holes upon high Arctic glaciers, Svalbard. Biogeosci Discuss 12:11751–11795CrossRefGoogle Scholar
  132. Wadham JL, Arndt S, Tulaczyk S, Stibal M, Tranter M, Telling J, Lis GP, Lawson E, Ridgwell A, Dubnick A, Sharp MJ, Anesio AM, Butler CEH (2012) Potential methane reservoirs beneath Antarctica. Nature 488(7413):633–637PubMedCrossRefGoogle Scholar
  133. Warren SG, Hudson SR (2003) Bacterial activity in South Pole snow is questionable. Appl Environ Microbiol 69(10):6340–6341PubMedPubMedCentralCrossRefGoogle Scholar
  134. Warren SG, Brandt RE, Grenfell TC (2006) Visible and near-ultraviolet absorption spectrum of ice from transmission of solar radiation into snow. Appl Optics 45(21):5320–5334CrossRefGoogle Scholar
  135. Weiss RL (1983) Fine Structure of the snow algae (Chlamydamonas nivalis) and associated bacteria. J Phycol 19(2):200–204CrossRefGoogle Scholar
  136. Wharton RA, Mckay CP, Simmons GM, Parker BC (1985) Cryoconite holes on glaciers. Bioscience 35(8):499–503PubMedCrossRefGoogle Scholar
  137. Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci 95(12):6578–6583PubMedPubMedCentralCrossRefGoogle Scholar
  138. Wilhelm L, Singer GA, Fasching C, Battin TJ, Besemer K (2013) Microbial biodiversity in glacier-fed streams. ISME J 7:1651–1660PubMedPubMedCentralCrossRefGoogle Scholar
  139. Wilhelm L, Besemer K, Fasching C, Urich T, Singer GA, Quince C, Battin TJ (2014) Rare but active taxa contribute to community dynamics of benthic biofilms in glacier-fed streams. Environ Microbiol 16(8):2514–2524. doi: 10.1111/1462-2920.12392 PubMedCrossRefGoogle Scholar
  140. Willerslev E, Hansen AJ, Christensen B, Steffensen JP, Arctander P (1999) Diversity of Holocene life forms in fossil glacier ice. Proc Natl Acad Sci 96:8017–8021PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wunderlin T, Ferrari B, Power M (2016) Global and local-scale variation in bacterial community structure of snow from the Swiss and Australian Alps. FEMS Microbiol Ecol 92(9):fivq32CrossRefGoogle Scholar
  142. Wynn PM, Hodson AJ, Heaton TH, Chenery S (2007) Nitrate production beneath a High Arctic glacier, Svalbard. Chem Geol 244(1):88–102CrossRefGoogle Scholar
  143. Xiang S-R, Shang T-C, Chen Y, Yao T-D (2009) Deposition and postdeposition mechanisms as possible drivers of microbial population variability in glacier ice. FEMS Microbiol Ecol 70(2):165–176. doi: 10.1111/j.1574-6941.2009.00759.x CrossRefGoogle Scholar
  144. Yallop M, Anesio A (2010) Benthic diatom flora in supraglacial habitats: a generic-level comparison. Ann Glaciol 51(56):15–22CrossRefGoogle Scholar
  145. Yallop ML, Anesio AM, Perkins RG, Cook J, Telling J, Fagan D, MacFarlane J, Stibal M, Barker G, Bellas C, Hodson A, Tranter M, Wadham J, Roberts NW (2012) Photophysiology and albedo-changing potential of the ice algal community on the surface of the Greenland ice sheet. ISME J 6:2302–2313PubMedPubMedCentralCrossRefGoogle Scholar
  146. Yoshimura Y, Kohshima S, Ohtani S (1997) A community of snow algae on Himalayan glacier: change of algal biomass and community structure with altitude. Arct Alp Res 29(1):126–137. doi: 10.2307/1551843 CrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute of Biological, Rural and Environmental Sciences, Aberystwyth UniversityAberystwythUK
  2. 2.Aberystwyth University Interdisciplinary Centre for Environmental Microbiology (AU iCEM), Aberystwyth UniversityAberystwythUK

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