Advertisement

Viruses in Glacial Environments

  • Sara M. E. RassnerEmail author
Chapter

Abstract

Viruses play a central role in glacial microbial communities. Prokaryotes in glacial environments support surprisingly large viral communities, which, in turn, have a considerable impact on the prokaryotic communities. Through the lysis of host cells and by lowering the growth efficiency of prokaryotic communities, viruses substantially alter the carbon cycling in glacial environments. Despite many similarities with viruses in other habitats, the unique characteristics of glacial environments have accentuated certain features in glacial viruses and their interactions with their hosts, e.g. low viral decay rates in supraglacial viruses as a mechanism for overcoming low host contact rates in systems with low prokaryotic abundances, virus-specific temperature adaptation that differ from that of the host, and virus-mediated transfer of CRISPR arrays that confer immunity against superinfection. Current literature suggests that viral communities in glacial environments are as genetically diverse as those in other environments and, with recent technological advances in environmental genomics and bioinformatics, we are posed to tackle the next great challenge in viral ecology of identifying and quantifying the dynamics of individual virus–host pairs in environmental samples.

Notes

Acknowledgements

This work was supported by the Freshwater Biological Association through the Hugh Cary Gilson Award 2013 and by the Welsh Government and HEFCW through the Sêr Cymru National Research Network for Low Carbon, Energy and the Environment.

References

  1. Ackermann H-W (2007) 5500 phages examined in the electron microscope. Arch Virol 152(2):227–243. doi: 10.1007/s00705-006-0849-1 PubMedCrossRefGoogle Scholar
  2. Aguirre de Cárcer D, López-Bueno A, Alonso-Lobo JM, Quesada A, Alcami A (2016) Metagenomic analysis of lacustrine viral diversity along a latitudinal transect of the Antarctic Peninsula. FEMS Microbiol Ecol 92(6). doi: 10.1093/femsec/fiw074
  3. Aguirre de Cárcer D, López-Bueno A, Pearce DA, Alcamí A (2015) Biodiversity and distribution of polar freshwater DNA viruses. Sci Adv 1(5):e1400127. doi: 10.1126/sciadv.1400127 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Allen B, Willner D, Oechel WC, Lipson D (2010) Top-down control of microbial activity and biomass in an Arctic soil ecosystem. Environ Microbiol 12(3):642–648. doi: 10.1111/j.1462-2920.2009.02104.x PubMedCrossRefGoogle Scholar
  5. Anesio AM, Bellas CM (2011) Are low temperature habitats hot spots of microbial evolution driven by viruses? Trends Microbiol 19(2):52–57. doi: 10.1016/j.tim.2010.11.002 PubMedCrossRefGoogle 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 Chang Biol 15(4):955–960. doi: 10.1111/j.1365-2486.2008.01758.x CrossRefGoogle Scholar
  7. Anesio AM, Mindl B, Laybourn-Parry J, Hodson AJ, Sattler B (2007) Viral dynamics in cryoconite holes on a high Arctic glacier (Svalbard). J Geophys Res Biogeosci 112(G4):10. doi: 10.1029/2006jg000350 CrossRefGoogle Scholar
  8. Anesio AM, Sattler B, Foreman C, Telling J, Hodson A, Tranter M, Psenner R (2010) Carbon fluxes through bacterial communities on glacier surfaces. Ann Glaciol 51(56):32–40CrossRefGoogle Scholar
  9. Azam F, Fenchel T, Field JG, Gray J, Meyer-Reil L, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263CrossRefGoogle Scholar
  10. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315(5819):1709–1712. doi: 10.1126/science.1138140 PubMedCrossRefGoogle Scholar
  11. Bellas CM, Anesio AM (2013) High diversity and potential origins of T4-type bacteriophages on the surface of Arctic glaciers. Extremophiles 17(5):861–870. doi: 10.1007/s00792-013-0569-x PubMedCrossRefGoogle Scholar
  12. Bellas CM, Anesio AM, Barker G (2015) Analysis of virus genomes from glacial environments reveals novel virus groups with unusual host interactions. Front Microbiol 6:14. doi: 10.3389/fmicb.2015.00656 CrossRefGoogle Scholar
  13. Bellas CM, Anesio AM, Telling J, Stibal M, Tranter M, Davis S (2013) Viral impacts on bacterial communities in Arctic cryoconite. Environ Res Lett 8(4):9. doi: 10.1088/1748-9326/8/4/045021 CrossRefGoogle Scholar
  14. Biller SJ, Schubotz F, Roggensack SE, Thompson AW, Summons RE, Chisholm SW (2014) Bacterial vesicles in marine ecosystems. Science 343(6167):183–186. doi: 10.1126/science.1243457 PubMedCrossRefGoogle Scholar
  15. Boetius A, Anesio AM, Deming JW, Mikucki JA, Rapp JZ (2015) Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat Rev Microbiol 13(11):677–690. doi: 10.1038/nrmicro3522 PubMedCrossRefGoogle Scholar
  16. Bonilla-Findji O, Malits A, Lefèvre D, Rochelle-Newall E, Lemée R, Weinbauer MG, Gattuso J-P (2008) Viral effects on bacterial respiration, production and growth efficiency: consistent trends in the Southern Ocean and the Mediterranean Sea. Deep-Sea Res II Top Stud Oceanogr 55(5):790–800CrossRefGoogle Scholar
  17. Bruder K, Malki K, Cooper A, Sible E, Shapiro JW, Watkins SC, Putonti C (2016) Freshwater metaviromics and bacteriophages: a current assessment of the state of the art in relation to bioinformatic challenges. Evol Bioinforma 12:25–33. doi: 10.4137/ebo.s38549 Google Scholar
  18. Castello JD, Rogers SO, Starmer WT, Catranis CM, Ma LJ, Bachand GD, Zhao YH, Smith JE (1999) Detection of tomato mosaic tobamovirus RNA in ancient glacial ice. Polar Biol 22(3):207–212. doi: 10.1007/s003000050411 CrossRefGoogle Scholar
  19. Cattaneo R, Rouviere C, Rassoulzadegan F, Weinbauer MG (2010) Association of marine viral and bacterial communities with reference black carbon particles under experimental conditions: an analysis with scanning electron, epifluorescence and confocal laser scanning microscopy. FEMS Microbiol Ecol 74(2):382–396. doi: 10.1111/j.1574-6941.2010.00953.x PubMedCrossRefGoogle Scholar
  20. Cavicchioli R (2015) Microbial ecology of Antarctic aquatic systems. Nat Rev Microbiol 13(11):691–706. doi: 10.1038/nrmicro3549 PubMedCrossRefGoogle Scholar
  21. Cavicchioli R, Erdmann S (2015) The discovery of Antarctic RNA viruses: a new game changer. Mol Ecol 24(19):4809–4811. doi: 10.1111/mec.13387 PubMedCrossRefGoogle Scholar
  22. Chénard C, Wirth JF, Suttle CA (2016) Viruses infecting a freshwater filamentous cyanobacterium (Nostoc sp.) encode a functional CRISPR array and a proteobacterial DNA polymerase B. mBio 7(3):e00667-16. doi: 10.1128/mBio.00667-16 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Clarke DK, Duarte EA, Elena SF, Moya A, Domingo E, Holland J (1994) The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci 91(11):4821–4824PubMedPubMedCentralCrossRefGoogle Scholar
  24. Collins RE, Deming JW (2011) Abundant dissolved genetic material in Arctic sea ice. Part II: Viral dynamics during autumn freeze-up. Polar Biol 34(12):1831–1841. doi: 10.1007/s00300-011-1008-z CrossRefGoogle Scholar
  25. Cottrell MT, Kirchman DL (2012) Virus genes in Arctic marine bacteria identified by metagenomic analysis. Aquat Microb Ecol 66(2):107–116. doi: 10.3354/ame01569 CrossRefGoogle Scholar
  26. Drewes F, Peter H, Sommaruga R (2016) Are viruses important in the plankton of highly turbid glacier-fed lakes? Sci Report 6:24608. doi: 10.1038/srep24608 CrossRefGoogle Scholar
  27. Dudley JP, Hoberg EP, Jenkins EJ, Parkinson AJ (2015) Climate change in the North American Arctic: a one health perspective. EcoHealth 12(4):713–725. doi: 10.1007/s10393-015-1036-1 PubMedCrossRefGoogle Scholar
  28. Edwards A (2015) Coming in from the cold: potential microbial threats from the terrestrial cryosphere. Front Earth Sci 3:12CrossRefGoogle Scholar
  29. Edwards A, Debbonaire AR, Sattler B, Mur LA, Hodson AJ (2016) Extreme metagenomics using nanopore DNA sequencing: a field report from Svalbard, 78 N. bioRxiv. doi: 10.1101/073965
  30. Evans C, Pearce I, Brussaard CPD (2009) Viral-mediated lysis of microbes and carbon release in the sub-Antarctic and polar frontal zones of the Australian Southern Ocean. Environ Microbiol 11(11):2924–2934. doi: 10.1111/j.1462-2920.2009.02050.x PubMedCrossRefGoogle Scholar
  31. Filippova SN, Surgucheva NA, Sorokin VV, Akimov VN, Karnysheva EA, Brushkov AV, Andersen D, Gal'chenko VF (2016) Bacteriophages in Arctic and Antarctic low-temperature systems. Microbiology 85(3):359–366. doi: 10.1134/s0026261716030048 CrossRefGoogle Scholar
  32. Frada M, Probert I, Allen MJ, Wilson WH, de Vargas C (2008) The “Cheshire Cat” escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc Natl Acad Sci 105(41):15944–15949. doi: 10.1073/pnas.0807707105 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Giovannoni S, Temperton B, Zhao Y (2013) Giovannoni et al. reply. Nature 499(7459):E4–E5. doi: 10.1038/nature12388 PubMedCrossRefGoogle Scholar
  34. Gokul JK, Hodson AJ, Saetnan ER, Irvine-Fynn TDL, Westall PJ, Detheridge AP, Takeuchi N, Bussell J, Mur LAJ, Edwards A (2016) Taxon interactions control the distributions of cryoconite bacteria colonizing a High Arctic ice cap. Mol Ecol 25(15):3752–3767. doi: 10.1111/mec.13715 PubMedCrossRefGoogle Scholar
  35. Goldfarb T, Sberro H, Weinstock E, Cohen O, Doron S, Charpak-Amikam Y, Afik S, Ofir G, Sorek R (2015) BREX is a novel phage resistance system widespread in microbial genomes. EMBO J 34(2):169–183. doi: 10.15252/embj.201489455 PubMedCrossRefGoogle Scholar
  36. Gorniak D, Marszalek H, Jankowska K, Dunalska J (2016) Bacterial community succession in an Arctic lake-stream system (Brattegg Valley, SW Spitsbergen). Boreal Environ Res 21(1-2):115–133Google Scholar
  37. Guixa-Boixereu N, Vaqué D, Gasol JM, Sánchez-Cámara J, Pedrós-Alió C (2002) Viral distribution and activity in Antarctic waters. Deep Sea Res II Top Stud Oceanogr 49(4–5):827–845. doi: 10.1016/S0967-0645(01)00126-6 CrossRefGoogle Scholar
  38. Hanks MC, Newman B, Oliver IR, Masters M (1988) Packaging of transducing DNA by bacteriophage P1. Mol Gen Genet MGG 214(3):523–532. doi: 10.1007/bf00330490 PubMedCrossRefGoogle Scholar
  39. Heldal M, Bratbak G (1991) Production and decay of viruses in aquatic environments. Mar Ecol Prog Ser 72(3):205–212CrossRefGoogle Scholar
  40. Hodson A, Anesio AM, Tranter M, Fountain A, Osborn M, Priscu J, Laybourn-Parry J, Sattler B (2008) Glacial ecosystems. Ecol Monogr 78(1):41–67. doi: 10.1890/07-0187.1 CrossRefGoogle Scholar
  41. Hornung C, Poehlein A, Haack FS, Schmidt M, Dierking K, Pohlen A, Schulenburg H, Blokesch M, Plener L, Jung K, Bonge A, Krohn-Molt I, Utpatel C, Timmermann G, Spieck E, Pommerening-Röser A, Bode E, Bode HB, Daniel R, Schmeisser C, Streit WR (2013) The Janthinobacterium sp. HH01 genome encodes a homologue of the V. cholerae CqsA and L. pneumophila LqsA autoinducer synthases. PLoS One 8(2):e55045. doi: 10.1371/journal.pone.0055045 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ji XL, Zhang CJ, Fang Y, Zhang Q, Lin LB, Tang B, Wei YL (2015) Isolation and characterization of glacier VMY22, a novel lytic cold-active bacteriophage of Bacillus cereus. Virol Sin 30(1):52–58. doi: 10.1007/s12250-014-3529-4 PubMedCrossRefGoogle Scholar
  43. Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64(8):2780–2787PubMedPubMedCentralGoogle Scholar
  44. Jungblut AD, Lovejoy C, Vincent WF (2009) Global distribution of cyanobacterial ecotypes in the cold biosphere. ISME J 4(2):191–202. http://www.nature.com/ismej/journal/v4/n2/suppinfo/ismej2009113s1.html PubMedCrossRefGoogle Scholar
  45. Kay A, Zoulim F (2007) Hepatitis B virus genetic variability and evolution. Virus Res 127(2):164–176. doi: 10.1016/j.virusres.2007.02.021 PubMedCrossRefGoogle Scholar
  46. Knowles B, Silveira CB, Bailey BA, Barott K, Cantu VA, Cobián-Güemes AG, Coutinho FH, Dinsdale EA, Felts B, Furby KA, George EE, Green KT, Gregoracci GB, Haas AF, Haggerty JM, Hester ER, Hisakawa N, Kelly LW, Lim YW, Little M, Luque A, McDole-Somera T, McNair K, de Oliveira LS, Quistad SD, Robinett NL, Sala E, Salamon P, Sanchez SE, Sandin S, Silva GGZ, Smith J, Sullivan C, Thompson C, Vermeij MJA, Youle M, Young C, Zgliczynski B, Brainard R, Edwards RA, Nulton J, Thompson F, Rohwer F (2016) Lytic to temperate switching of viral communities. Nature 531(7595):466–470. doi: 10.1038/nature17193 PubMedCrossRefGoogle Scholar
  47. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8(5):317–327PubMedCrossRefGoogle Scholar
  48. Legendre M, Bartoli J, Shmakova L, Jeudy S, Labadie K, Adrait A, Lescot M, Poirot O, Bertaux L, Bruley C, Couté Y, Rivkina E, Abergel C, Claverie J-M (2014) Thirty-thousand-year-old distant relative of giant icosahedral DNA viruses with a pandoravirus morphology. Proc Natl Acad Sci 111(11):4274–4279. doi: 10.1073/pnas.1320670111 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Li MY, Wang JL, Zhang Q, Lin LB, Kuang AX, Materon L, Ji XL, Wei Y (2016) Isolation and characterization of the lytic cold-active bacteriophage MYSP06 from the Mingyong Glacier in China. Curr Microbiol 72(2):120–127. doi: 10.1007/s00284-015-0926-3 PubMedCrossRefGoogle Scholar
  50. López-Bueno A, Rastrojo A, Peiro R, Arenas M, Alcami A (2015) Ecological connectivity shapes quasispecies structure of RNA viruses in an Antarctic lake. Mol Ecol 24(19):4812–4825. doi: 10.1111/mec.13321 PubMedCrossRefGoogle Scholar
  51. López-Bueno A, Tamames J, Velázquez D, Moya A, Quesada A, Alcamí A (2009) High diversity of the viral community from an Antarctic lake. Science 326(5954):858–861. doi: 10.1126/science.1179287 PubMedCrossRefGoogle Scholar
  52. Madan NJ, Marshall WA, Laybourn-Parry J (2005) Virus and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshw Biol 50(8):1291–1300. doi: 10.1111/j.1365-2427.2005.01399.x CrossRefGoogle Scholar
  53. Middelboe M, Glud RN, Sejr MK (2012) Bacterial carbon cycling in a subarctic fjord: a seasonal study on microbial activity, growth efficiency, and virus-induced mortality in Kobbefjord, Greenland. Limnol Oceanogr 57(6):1732–1742CrossRefGoogle Scholar
  54. Middelboe M, Jorgensen N, Kroer N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62(6):1991–1997PubMedPubMedCentralGoogle Scholar
  55. Mojica KDA, Brussaard CPD (2014) Factors affecting virus dynamics and microbial host–virus interactions in marine environments. FEMS Microbiol Ecol 89(3):495–515. doi: 10.1111/1574-6941.12343 PubMedCrossRefGoogle Scholar
  56. Motegi C, Nagata T, Miki T, Weinbauer MG, Legendre L, Rassoulzadegan F (2009) Viral control of bacterial growth efficiency in marine pelagic environments. Limnol Oceanogr 54(6):1901–1910CrossRefGoogle Scholar
  57. Noble RT, Fuhrman JA (1997) Virus decay and its causes in coastal waters. Appl Environ Microbiol 63(1):77–83PubMedPubMedCentralGoogle Scholar
  58. Noble RT, Fuhrman JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14(2):113–118CrossRefGoogle Scholar
  59. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304PubMedCrossRefGoogle Scholar
  60. Patel A, Noble RT, Steele JA, Schwalbach MS, Hewson I, Fuhrman JA (2007) Virus and prokaryote enumeration from planktonic aquatic environments by epifluorescence microscopy with SYBR Green I. Nat Protoc 2(2):269–276PubMedCrossRefGoogle Scholar
  61. Pearce DA, Wilson WH (2003) Viruses in Antarctic ecosystems. Antarct Sci 15(3):319–331. doi: 10.1017/s0954102003001330 CrossRefGoogle Scholar
  62. Philippe N, Legendre M, Doutre G, Couté Y, Poirot O, Lescot M, Arslan D, Seltzer V, Bertaux L, Bruley C, Garin J, Claverie J-M, Abergel C (2013) Pandoraviruses: Amoeba viruses with genomes up to 2.5 Mb reaching that of parasitic eukaryotes. Science 341(6143):281–286. doi: 10.1126/science.1239181 PubMedCrossRefGoogle Scholar
  63. Pomeroy LR (1974) The Ocean's food web, a changing paradigm. Bioscience 24(9):499–504. doi: 10.2307/1296885 CrossRefGoogle Scholar
  64. Qin KH, Cheng BX, Zhang ST, Wang N, Fang Y, Zhang Q, Kuang AX, Lin LB, Ji XL, Wei YL (2016) Complete genome sequence of the cold-active bacteriophage VMY22 from Bacillus cereus. Virus Genes 52(3):432–435. doi: 10.1007/s11262-016-1300-7 PubMedCrossRefGoogle Scholar
  65. Rassner SME, Anesio AM, Girdwood SE, Hell K, Gokul JK, Whitworth DE, Edwards A (2016) Can the bacterial community of a high Arctic glacier surface escape viral control? Front Microbiol 7:956. doi: 10.3389/fmicb.2016.00956 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Rogers SO, Starmer WT, Castello JD (2004) Recycling of pathogenic microbes through survival in ice. Med Hypotheses 63(5):773–777. doi: 10.1016/j.mehy.2004.04.004 PubMedCrossRefGoogle Scholar
  67. Rohwer F, Thurber RV (2009) Viruses manipulate the marine environment. Nature 459(7244):207–212PubMedCrossRefGoogle Scholar
  68. Rose R, Constantinides B, Tapinos A, Robertson DL, Prosperi M (2016) Challenges in the analysis of viral metagenomes. Virus Evol 2(2):vew022. doi: 10.1093/ve/vew022 CrossRefGoogle Scholar
  69. Sanguino L, Franqueville L, Vogel TM, Larose C (2015) Linking environmental prokaryotic viruses and their host through CRISPRs. FEMS Microbiol Ecol 91(5). doi: 10.1093/femsec/fiv046
  70. Sano E, Carlson S, Wegley L, Rohwer F (2004) Movement of viruses between biomes. Appl Environ Microbiol 70(10):5842–5846. doi: 10.1128/AEM.70.10.5842-5846.2004 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Säwström C, Anesio MA, Graneli W, Laybourn-Parry J (2007a) Seasonal viral loop dynamics in two large ultraoligotrophic Antarctic freshwater lakes. Microb Ecol 53(1):1–11. doi: 10.1007/s00248-006-9146-5 PubMedCrossRefGoogle Scholar
  72. Säwström C, Laybourn-Parry J, Graneli W, Anesio AM (2007b) Heterotrophic bacterial and viral dynamics in Arctic freshwaters: results from a field study and nutrient-temperature manipulation experiments. Polar Biol 30(11):1407–1415. doi: 10.1007/s00300-007-0301-3 CrossRefGoogle Scholar
  73. Säwström C, Lisle J, Anesio AM, Priscu JC, Laybourn-Parry J (2008) Bacteriophage in polar inland waters. Extremophiles 12(2):167–175. doi: 10.1007/s00792-007-0134-6 PubMedCrossRefGoogle Scholar
  74. Sengupta M, Nielsen HJ, Youngren B, Austin S (2010) P1 plasmid segregation: accurate redistribution by dynamic plasmid pairing and separation. J Bacteriol 192(5):1175–1183. doi: 10.1128/JB.01245-09 PubMedCrossRefGoogle Scholar
  75. Sillankorva S, Oliveira R, Vieira MJ, Sutherland I, Azeredo J (2004) Pseudomonas fluorescens infection by bacteriophage ΦS1: the influence of temperature, host growth phase and media. FEMS Microbiol Lett 241(1):13–20. doi: 10.1016/j.femsle.2004.06.058 PubMedCrossRefGoogle Scholar
  76. Skidmore M, Anderson SP, Sharp M, Foght J, Lanoil BD (2005) Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes. Appl Environ Microbiol 71(11):6986–6997. doi: 10.1128/AEM.71.11.6986-6997.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Smith AW, Skilling DE, Castello JD, Rogers SO (2004) Ice as a reservoir for pathogenic human viruses: specifically, caliciviruses, influenza viruses, and enteroviruses. Med Hypotheses 63(4):560–566. doi: 10.1016/j.mehy.2004.05.011 PubMedCrossRefGoogle Scholar
  78. Stibal M, Schostag M, Cameron KA, Hansen LH, Chandler DM, Wadham JL, Jacobsen CS (2015) Different bulk and active bacterial communities in cryoconite from the margin and interior of the Greenland ice sheet. Environ Microbiol Rep 7(2):293–300. doi: 10.1111/1758-2229.12246 PubMedCrossRefGoogle Scholar
  79. Suttle CA, Chen F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58(11):3721–3729PubMedPubMedCentralGoogle Scholar
  80. Thingstad TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45(6):1320–1328. doi: 10.4319/lo.2000.45.6.1320 CrossRefGoogle Scholar
  81. Thingstad TF, Lignell R (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat Microb Ecol 13(1):19–27CrossRefGoogle Scholar
  82. Tschitschko B, Williams TJ, Allen MA, Paez-Espino D, Kyrpides N, Zhong L, Raftery MJ, Cavicchioli R (2015) Antarctic archaea-virus interactions: metaproteome-led analysis of invasion, evasion and adaptation. ISME J 9(9):2094–2107. doi: 10.1038/ismej.2015.110 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Tu M, Liu F, Chen S, Wang M, Cheng A (2015) Role of capsid proteins in parvoviruses infection. Virol J 12:114. doi: 10.1186/s12985-015-0344-y PubMedPubMedCentralCrossRefGoogle Scholar
  84. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28(2):127–181. doi: 10.1016/j.femsre.2003.08.001 PubMedCrossRefGoogle Scholar
  85. Weinbauer MG, Rassoulzadegan F (2004) Are viruses driving microbial diversification and diversity? Environ Microbiol 6(1):1–11. doi: 10.1046/j.1462-2920.2003.00539.x PubMedCrossRefGoogle Scholar
  86. Wells LE, Deming JW (2006a) Characterization of a cold-active bacteriophage on two psychrophilic marine hosts. Aquat Microb Ecol 45(1):15–29CrossRefGoogle Scholar
  87. Wells LE, Deming JW (2006b) Effects of temperature, salinity and clay particles on inactivation and decay of cold-active marine bacteriophage 9A. Aquat Microb Ecol 45(1):31–39. doi: 10.3354/ame045031 CrossRefGoogle Scholar
  88. Wilhelm SW, Matteson AR (2008) Freshwater and marine virioplankton: a brief overview of commonalities and differences. Freshw Biol 53(6):1076–1089. doi: 10.1111/j.1365-2427.2008.01980.x CrossRefGoogle Scholar
  89. Wilhelm SW, Suttle CA (1999) Viruses and nutrient cycles in the sea: viruses play critical roles in the structure and function of aquatic food webs. Bioscience 49(10):781–788. doi: 10.2307/1313569 CrossRefGoogle Scholar
  90. Wilkins D, Yau S, Williams TJ, Allen MA, Brown MV, DeMaere MZ, Lauro FM, Cavicchioli R (2013) Key microbial drivers in Antarctic aquatic environments. FEMS Microbiol Rev 37(3):303–335. doi: 10.1111/1574-6976.12007 PubMedCrossRefGoogle Scholar
  91. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64(1):69–114PubMedPubMedCentralCrossRefGoogle Scholar
  92. Yau S, Lauro FM, DeMaere MZ, Brown MV, Thomas T, Raftery MJ, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Gibson JA, Cavicchioli R (2011) Virophage control of antarctic algal host–virus dynamics. Proc Natl Acad Sci 108(15):6163–6168. doi: 10.1073/pnas.1018221108 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Zhang G, Shoham D, Gilichinsky D, Davydov S, Castello JD, Rogers SO (2006) Evidence of influenza A virus RNA in Siberian lake ice. J Virol 80(24):12229–12235. doi: 10.1128/jvi.00986-06 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, Ellisman M, Deerinck T, Sullivan MB, Giovannoni SJ (2013) Abundant SAR11 viruses in the ocean. Nature 494(7437):357–360. http://www.nature.com/nature/journal/v494/n7437/abs/nature11921.html#supplementary-information PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Geography and Earth SciencesAberystwyth UniversityAberystwythUK

Personalised recommendations