, Volume 12, Issue 2, pp 167–175 | Cite as

Bacteriophage in polar inland waters

  • Christin SäwströmEmail author
  • John Lisle
  • Alexandre M. Anesio
  • John C. Priscu
  • Johanna Laybourn-Parry


Bacteriophages are found wherever microbial life is present and play a significant role in aquatic ecosystems. They mediate microbial abundance, production, respiration, diversity, genetic transfer, nutrient cycling and particle size distribution. Most studies of bacteriophage ecology have been undertaken at temperate latitudes. Data on bacteriophages in polar inland waters are scant but the indications are that they play an active and dynamic role in these microbially dominated polar ecosystems. This review summarises what is presently known about polar inland bacteriophages, ranging from subglacial Antarctic lakes to glacial ecosystems in the Arctic. The review examines interactions between bacteriophages and their hosts and the abiotic and biotic variables that influence these interactions in polar inland waters. In addition, we consider the proportion of the bacteria in Arctic and Antarctic lake and glacial waters that are lysogenic and visibly infected with viruses. We assess the relevance of bacteriophages in the microbial loop in the extreme environments of Antarctic and Arctic inland waters with an emphasis on carbon cycling.


Bacteriophage Bacteria Arctic Antarctic Carbon cycling Lysogeny Polar inland waters Review 



The authors gratefully acknowledge the following funding bodies who have supported their data presented in this article: The Australian Antarctic Science Advisory Committee, Marie Curie European Science foundation, VR the Swedish Research Council, the US National Science Foundation (Grants MCB-0237335, OPP-432595 and OPP-440943), the Nuffield Foundation and the Leverhulme Trust. We are indebted to Lars-Anders Hansson for providing samples from the Beringia Area and to Rita Wallen, Gerry Nash and M. Young for help with TEM analyses. Thanks are due to two anonymous reviewers for valuable comments on an earlier draft of the manuscript.


  1. Ackermann HW (2007) 5500 phages examined in the electron microscope. Arch Viriol 152:227–243CrossRefGoogle Scholar
  2. Anesio AM, Mindl B, Laybourn-Parry J, Hodson A, Sattler B (2007) Virus dynamics in cryoconite holes on a high Arctic glacier (Svalbard). J Geophys Res Biogeosci 112, G04531. doi:  10.1029/2006JG000350
  3. Bettarel Y, Sime-Ngando T, Amblard C, Carrias J-F, Portelli C (2003) Virioplankton and microbial communities in aquatic systems: a seasonal study in two lakes of differing trophy. Freshw Biol 28:810–822CrossRefGoogle Scholar
  4. Borriss M, Helmke E, Hanschke R, Schweder T (2003) Isolation and characterization of marine psychrophilic phage-host systems from Arctic sea ice. Extremophiles 7:377–384PubMedCrossRefGoogle Scholar
  5. Bratbak G, Egge JK, Heldal M (1993) Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar Ecol Prog Ser 93:39–48CrossRefGoogle Scholar
  6. Bratbak G, Heldal M, Thingstad TF, Riemann B, Haslund OH (1992) Incorporation of viruses into the budget of microbial C-transfer: a first approach. Mar Ecol Prog Ser 83:273–280CrossRefGoogle Scholar
  7. Cochran PK, Kellogg CA, Paul JP (1998) Prophage induction of indigenous marine lysogenic bacteria by environmental pollutants. Mar Ecol Prog Ser 164:125–133CrossRefGoogle Scholar
  8. Cochran PK, Paul JH (1998) Seasonal abundance of lysogenic bacteria in a sub-tropical estuary. Appl Environ Microbiol 64:2308–2312PubMedGoogle Scholar
  9. Cole JJ, Carpenter SR, Kitchell JF, Pace ML (2002) Pathways of organic carbon utilization in small lakes: results from a whole-lake 13C addition and coupled model. Limnol Oceanogr 47:1664–1675CrossRefGoogle Scholar
  10. Dore JE, Priscu JC (2001) Phytoplankton phosphorus deficiency and alkaline phosphatase activity in the McMurdo Dry Valley lakes, Antarctica. Limnol Oceanogr 46:1331–1346CrossRefGoogle Scholar
  11. Fischer UR, Velimirov B (2002) High control of bacterial production by viruses in a eutrophic oxbow lake. Aquat Microbial Ecol 27:1–12CrossRefGoogle Scholar
  12. Gobler CJ, Hutchins DA, Fisher NS, Cosper EM, Sañudo-Wilhelmy SA (1997) Release and bioavailability of C, N, P, Se and Fe following viral lysis of a marine chrysophyte. Limnol Oceanogr 42:1492–1504Google Scholar
  13. Granéli W, Bertilsson S, Philibert A (2004) Phosphorous limitation of bacterial growth in high Arctic lakes and ponds. Aquat Sci 66:430–439CrossRefGoogle Scholar
  14. 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 49:827–845CrossRefGoogle Scholar
  15. Hewson I, O’Neil JM, Fuhrman JA, Dennison WC (2001) Virus-like particle distribution and abundance in sediments and overlying waters along eutrophication gradients in two subtropical estuaries. Limnol Oceaongr 46:1734–1746Google Scholar
  16. Hobbie JE, Bahr M, Rublee PA (1999) Control on microbial food webs in oligotrophic arctic lakes. Arch Hydrobiol Spec Issue Adv Limnol 54:61Google Scholar
  17. Hofer SJ, Sommaruga R (2001) Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat Microb Ecol 26:1–11CrossRefGoogle Scholar
  18. Jiang SC, Paul JH (1996) Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar Ecol Prog Ser 142:27–38CrossRefGoogle Scholar
  19. Jiang SC, Paul JH (1998) Significance of lysogeny in the marine environment: studies with isolates and a model of lysogenic phage production. Microb Ecol 35:235–243PubMedCrossRefGoogle Scholar
  20. Karr EA, Ng JM, Belchik SM, Sattley WM, Madigan MT, Achenbach LA (2006) Biodiversity of methanogenic and other Archaea in the permanently frozen lake Fryxell, Antarctica. Appl Environ Microbiol 72:1663–1666PubMedCrossRefGoogle Scholar
  21. Kepner RL, Wharton RA, Suttle CA (1998) Viruses in Antarctic lakes. Limnol Oceanogr 43:1754–1761PubMedCrossRefGoogle Scholar
  22. Laybourn-Parry J (1997) The microbial loop in Antarctic lakes. In: Howard-Williams C, Lyons WB, Hawes I (eds) Ecosystem processes in Antarctic ice-free landscapes. A.A. Balkema/Rotterdam/Brookfield, Rotterdam, pp 231–240Google Scholar
  23. Laybourn-Parry J (2002) Survival strategies in Antarctic lakes. Phil Trans R Soc B 357:863–869PubMedCrossRefGoogle Scholar
  24. Laybourn-Parry J, Madan NJ, Marshall WA, Marchant HJ, Wright SW (2006) Carbon dynamics in an ultra-oligotrophic epishelf lake (Beaver Lake, Antarctica) in summer. Freshw Biol 51:1116–1130CrossRefGoogle Scholar
  25. Laybourn-Parry J, Marshall WA, Madan NJ (2007) Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol 30:351–358CrossRefGoogle Scholar
  26. Lisle JT, Priscu JC (2004) The occurrence of lysogenic bacteria and microbial aggregates in the lakes of the McMurdo Dry valleys, Antarctica. Microb Ecol 47:427–439PubMedCrossRefGoogle Scholar
  27. Lymer D, Vrede K (2006) Nutrient additions resulting in phage release and formation of non-nucleoid-containing bacteria. Aquat Microb Ecol 43:107–112CrossRefGoogle Scholar
  28. Madan NJ, Marshall WA, Laybourn-Parry J (2005) Virus and microbial loop dynamics over and annual cycle in three contrasting Antarctic lakes. Freshw Biol 50:1291–1300CrossRefGoogle Scholar
  29. Maranger R, Bird AF (1995) Viral abundance in aquatic systems: a comparison between marine and freshwaters. Mar Ecol Prog Ser 121:217–226CrossRefGoogle Scholar
  30. Mei ML, Danovaro R (2004) Virus production and life strategies in aquatic sediments. Limnol Oceanogr 49:459–470Google Scholar
  31. Middelboe M, Lyck PG (2002) Regeneration of dissolved organic matter by viral lysis in marine microbial communities. Aquat Microb Ecol 27:187–194CrossRefGoogle Scholar
  32. Middelboe M, Jørgensen NOG, Kroer N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62:1991–1997PubMedGoogle Scholar
  33. Miller ES, Heidelberg JF, Eisen JA, Nelson WC, Durkin AS, Ciecko A, Feldblyum TV, White O, Paulsen IT, Nierman WC, Lee J, Szczypinski B, Fraser CM (2003) Complete genome sequence of the broad-host-range vibriophage KVP40: comparative genomics of a T4 related bacteriophage. J Bacteriol 185:5220–5233PubMedCrossRefGoogle Scholar
  34. Murray AG, Eldridge PM (1994) Marine viral ecology: incorporation of bacteriophage into the microbial planktonic food web paradigm. J Plankton Res 16:627–641CrossRefGoogle Scholar
  35. Nagasaki K, Tomaru Y, Katanozaka N, Shirai Y, Nishida K, Itakura S, Yamaguchi M (2004) Isolation and charaterization of a novel single-stranded RNA virus infecting the bloom-forming diatom Rhizosolenia setigera. Appl Environ Microbiol 70:704–711PubMedCrossRefGoogle Scholar
  36. Nagasaki K, Tomaru Y, Takao Y, Nishida K, Shirai Y, Suzuki H, Nagumo T (2005) Previously unknown virus infects marine diatom. Appl Environ Microbiol 71:3528–3535PubMedCrossRefGoogle Scholar
  37. Noble RT, Fuhrman JA (1997) Viral decay and its causes in coastal waters. Appl Environ Microbiol 63:77–83PubMedGoogle Scholar
  38. Noble RT, Steward GF (2001) Estimating viral proliferation in aquatic samples. In: Paul JH (ed) Marine microbiology—methods in microbiology. Academic, London, pp 67–82CrossRefGoogle Scholar
  39. Ortman A, Lawrence J, Suttle C (2002) Lysogeny and lytic viral production during a bloom of the cyanobacterium Synechococcus spp. Microb Ecol 43:225–231CrossRefGoogle Scholar
  40. Paul JH, Kellogg CA (1998) The ecology of bacteriophages in nature. In: Hurst CJ (ed) Viral ecology. Academic, San Diego, pp 211–247Google Scholar
  41. Paul JH, Jiang SC (2001) Lysogeny and transduction. In: Paul JH (ed) Marine microbiology—methods in microbiology. Academic, London, pp 105–125CrossRefGoogle Scholar
  42. Prangishvili D, Forterre P, Garrett RA (2006) View of the Archaea; a unifying view. Nat Rev Microbiol 4:837–848PubMedCrossRefGoogle Scholar
  43. Priscu JC, Bell RE, Bulat SA, Ellis-Evans JC, Lukin VV, Petit J-R, Powell RD, Siegert MJ, Tabacco I (2003) An international plan for Antarctic subglacial lake exploration. Polar Geog 27:69–83CrossRefGoogle Scholar
  44. Priscu JC, Wolf CF, Takacs CD, Fritsen CH, Laybourn-Parry J, Roberts EC, Lyons WB (1999) Carbon transformations in the water column of a perennially ice-covered Antarctic Lake. Bioscience 49:997–1008CrossRefGoogle Scholar
  45. Rohwer F, Segall A, Steward G, Seguritan V, Breitbart M, Wolven F, Azam F (2000) The complete genomic sequence of the marine phage Roseophage SI01 shares homology with non-marine phages. Limnol Oceanogr 45:408–418Google Scholar
  46. Sano E, Carlsson S, Wegley L, Rohwer F (2004) Movement of viruses between biomes. Appl Environ Microbiol 70:5842–5846PubMedCrossRefGoogle Scholar
  47. Säwström C, Mumford P, Marshall WA, Hodson A, Laybourn-Parry J (2002) The microbial communities and primary productivity of cryoconite holes in and Arctic glacier (Svalbard 79°N). Polar Biol 25:591–596Google Scholar
  48. Säwström C, Anesio AM, Granéli W, Laybourn-Parry J (2007a) Seasonal viral loop dynamics in two large ultra-oligotrophic Antarctic freshwater lakes. Microb Ecol 53:1–11PubMedCrossRefGoogle Scholar
  49. Säwström C, Granéli W, Laybourn-Parry J, Anesio AM (2007b) High viral infection rates in Antarctic and Arctic bacterioplankton. Environ Microbiol 9:250–255PubMedCrossRefGoogle Scholar
  50. Säwström C, Laybourn-Parry J, Granéli W, Anesio AM (2007c) Heterotrophic bacterial and viral dynamics in Arctic freshwaters: results from a field study and nutrient-temperature manipulation experiments. Polar Biol 30:1407–1415CrossRefGoogle Scholar
  51. Säwström C, Pearce I, Davidson AT, Rosén P, Laybourn-Parry J (2008) The influence of environmental conditions, bacterial activity and viability on the viral component in ten Antarctic lakes. FEMS Microbiol Ecol 63:12–22PubMedCrossRefGoogle Scholar
  52. Steward GF, Wickner J, Cochlan WP, Smith DC, Azam F (1992) Estimation of virus production in the sea: I. Method development. Mar Microb Food Webs 6:57–78Google Scholar
  53. Suttle CA, Chen F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58:3721–3729PubMedGoogle Scholar
  54. Tapper MA, Hick RE (1998) Temperate viruses and lysogeny in Lake Superior bacterioplankton. Limnol Oceanogr 43:95–103Google Scholar
  55. Van Etten JL, Lane LC, Meints RH (1991) Viruses and virus like particles of eukaryotic algae. Microbiol Rev 55:586–620PubMedGoogle Scholar
  56. Van Etten JL, Graves MV, Mueller DG, Boland WW, Delaroque N (2002) Phycodnaviridae-large DNA algal viruses. Arch Virol 147:1479–1516PubMedCrossRefGoogle Scholar
  57. Vincent WF, Rae R, Laurion I, Howard-Williams C, Priscu JC (1997) Transparency of Antarctic ice-covered lakes to solar UV radiation. Limnol Oceanogr 43:618–624Google Scholar
  58. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181PubMedCrossRefGoogle Scholar
  59. Weinbauer MG, Brettar I, Höfle M (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep and anoxic waters. Limnol Oceanogr 48:1457–1465CrossRefGoogle Scholar
  60. Weinbauer MG, Höfle MG (1998) Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a Eutrophic lake. Appl Environ Microbiol 64:431–438PubMedGoogle Scholar
  61. Weinbauer MG, Suttle CA (1996) Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the Gulf of Mexico. Appl Environ Microbiol 62:4374–4380PubMedGoogle Scholar
  62. Weinbauer MG, Suttle CA (1999) Lysogeny and prophage induction in coastal and offshore bacterial communities. Aquat Microb Ecol 18:217–225CrossRefGoogle Scholar
  63. Wichels A, Biel SS, Gelderblom HR, Brinkhoff T, Muyzer G, Schutt C (1998) Bacteriophage diversity in the North Sea. Appl Environ Microbiol 64:4128–4133PubMedGoogle Scholar
  64. Wilhelm SW, Weinbauer MG, Suttle CA, Jeffrey WH (1998) The role of sunlight in the removal and repair of viruses in the sea. Limnol Oceanogr 43:586–592CrossRefGoogle Scholar
  65. Wilhelm SW, Brigden SM, Suttle CA (2002) A dilution technique for the direct measurement of viral production: a comparison in stratified and tidally mixed coastal waters. Microb Ecol 43:168–173PubMedCrossRefGoogle Scholar
  66. Williamson SJ, Houchin LA, McDaniel L, Paul JH (2002) Seasonal variation inlysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol 68:4307–4314PubMedCrossRefGoogle Scholar
  67. Wilson WH, Lane D, Pearce DA, Ellis-Evans JC (2000) Transmission electron microscope analysis of virus-like particles in the freshwater lakes of Signy Island, Antarctica. Polar Biol 23:657–660CrossRefGoogle Scholar
  68. Wilson WH, Mann NH (1997) Lysogenic and lytic viral production in marine microbial communities. Aquat Microb Ecol 13:95–100CrossRefGoogle Scholar
  69. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114PubMedCrossRefGoogle Scholar
  70. Wommack KE, Hill RT, Muller TA, Colwell RR (1996) Effects of sunlight on bacteriophage viability and structure. Appl Environ Microbiol 62:1336–1341PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Christin Säwström
    • 1
    Email author
  • John Lisle
    • 2
  • Alexandre M. Anesio
    • 3
  • John C. Priscu
    • 4
  • Johanna Laybourn-Parry
    • 5
  1. 1.Climate Impacts Research Centre (CIRC), Department of Ecology and Environmental ScienceUmeå UniversityAbiskoSweden
  2. 2.USGS Centre for Coastal and Watershed ResearchSt PetersburgUSA
  3. 3.School of Geographical SciencesUniversity of BristolBristolUK
  4. 4.Department of Land Resources and Environmental ScienceMontana State UniversityBozemanUSA
  5. 5.The Institute for Antarctic and Southern Ocean StudiesUniversity of TasmaniaHobartAustralia

Personalised recommendations