Polar Biology

, Volume 34, Issue 12, pp 1831–1841 | Cite as

Abundant dissolved genetic material in Arctic sea ice Part II: Viral dynamics during autumn freeze-up

  • R. Eric CollinsEmail author
  • Jody W. Deming
Original Paper


Viruses play a significant role in nutrient cycling within the world’s oceans and are important agents of horizontal gene transfer, but little is know about their entrainment into sea ice or their temporal dynamics once entrained. Nilas, grease ice, pancake ice, first-year sea ice floes up to 78 cm in thickness, and under-ice seawater were sampled widely across Amundsen Gulf (ca. \(71^\circ \hbox{N}, 125^\circ \hbox{W}\)) for concentrations of viruses and bacteria. Here, we report exceptionally high virus-to-bacteria ratios in seawater (45–340) and sea ice (93–2,820) during the autumn freeze-up. Virus concentrations ranged from 4.8 to 27 × 106  ml−1 in seawater and, scaled to brine volume, 5.5 to 170 × 107 ml−1 in sea ice. Large enrichment indices indicated processes of active entrainment from source seawater, or viral production within the ice, which was observed in 2 of 3 bottle incubations of sea ice brine at a temperature (\(-7^\circ\hbox{C}\)) and salinity (\(110 \permille\)) approximating that in situ. Median predicted virus-to-bacteria contact rates (relative to underlying seawater) were greatest in the top of thick sea ice (66–78 cm: 130×) and lowest in the bottom of medium-thickness ice (33–37 cm: 23×). The great abundance of viruses and more frequent interactions between bacteria and viruses predicted in sea ice relative to underlying seawater suggest that sea ice may be a hot spot for virally mediated horizontal gene transfer in the polar marine environment.


Arctic Sea ice Viruses Bacteria Horizontal gene transfer 



We thank the captain, crew, and scientific party of the CCGS Amundsen for a successful cruise. We gratefully acknowledge M. Pucko, W. Walkusz, P. Galand, B. Else, N. Sutherland, and M. Gupta for field assistance, C. Marrasé for assistance with chlorophyll a measurements, J. Islefson, D. Barber and CFL Team 2 for ice microstructure information and the use of ice-coring equipment, and S. Carpenter for help with laboratory analyses. The input of three reviewers helped to improve the manuscript, we thank them for their efforts.

Supplementary material

300_2011_1008_MOESM1_ESM.pdf (359 kb)
PDF (359 KB)


  1. Alonso-Sáez L, Sánchez O, Gasol JM, Balagué V, Pedrós-Alió C (2008) Winter-to-summer changes in the composition and single-cell activity of near-surface Arctic prokaryotes. Environ Microbiol 10:2444–2454PubMedCrossRefGoogle Scholar
  2. Baross J, Liston J, Morita R (1978) Incidence of Vibrio parahaemolyticus bacteriophages and other Vibrio bacteriophages in marine samples. Appl Environ Microbiol 36:492–499PubMedGoogle Scholar
  3. Bayer-Giraldi M, Uhlig C, John U, Mock T, Valentin K (2010) Antifreeze proteins in polar sea ice diatoms: diversity and gene expression in the genus Fragilariopsis. Environ Microbiol 12:1041–1052PubMedCrossRefGoogle Scholar
  4. Beiko RG, Harlow TJ, Ragan MA (2005) Highways of gene sharing in prokaryotes. PNAS 102:14332–14337PubMedCrossRefGoogle Scholar
  5. Börsheim K (1993) Native marine bacteriophages. FEMS Microbiol Ecol 102:141–159CrossRefGoogle Scholar
  6. Brown JR (2001) Genomic and phylogenetic perspectives on the evolution of prokaryotes. Syst Biol 50:497–512PubMedCrossRefGoogle Scholar
  7. Chiura HX (1997) Generalized gene transfer by virus-like particles from marine bacteria. Aquat Microb Ecol 13:75–83CrossRefGoogle Scholar
  8. Collins RE, Deming JW (submitted this issue) Abundant dissolved genetic material in Arctic sea ice, part I: extracellular DNA. Polar BiolGoogle Scholar
  9. Collins RE, Carpenter SD, Deming JW (2008) Spatial heterogeneity and temporal dynamics of particles, bacteria, and pEPS in Arctic winter sea ice. J Mar Sys 74:902–917CrossRefGoogle Scholar
  10. Comeau AM, Chan AM, Suttle CA (2006) Genetic richness of vibriophages isolated in a coastal environment. Environ Microbiol 8:1164–1176PubMedCrossRefGoogle Scholar
  11. Comiso JC, Parkinson CL, Gersten R, Stock L (2008) Accelerated decline in the Arctic sea ice cover. Geophys Res Lett 35:L01,703CrossRefGoogle Scholar
  12. Cox G, Weeks W (1975) Brine drainage and initial salt entrapment in sodium chloride ice. CRREL Res Rep 345:1–46Google Scholar
  13. Cox GFN, Weeks WF (1983) Equations for determining the gas and brine volumes in sea-ice samples. J Glaciol 29:306–316Google Scholar
  14. Cox GFN, Weeks WF (1986) Changes in the salinity and porosity of sea-ice samples during shipping and storage. J Glaciol 32:371–375Google Scholar
  15. Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19:2226–2238PubMedGoogle Scholar
  16. Gowing MM (2003) Large viruses and infected microeukaryotes in Ross Sea summer pack ice habitats. Mar Biol 142:1029–1040Google Scholar
  17. Gowing MM, Riggs BE, Garrison DL, Gibson AH, Jeffries MO (2002) Large viruses in Ross Sea late autumn pack ice habitats. Mar Ecol Prog Ser 241:1–11CrossRefGoogle Scholar
  18. Gowing MM, Garrison DL, Gibson AH, Krupp JM, Jeffries MO, Fritsen CH (2004) Bacterial and viral abundance in Ross Sea summer pack ice communities. Mar Ecol Prog Ser 279:3–12CrossRefGoogle Scholar
  19. Gradinger R, Ikavalko J (1998) Organism incorporation into newly forming Arctic sea ice in the Greenland Sea. J Plankton Res 20:871–886CrossRefGoogle Scholar
  20. Holmfeldt K, Middelboe M, Nybroe O, Riemann L (2007) Large variabilities in host strain susceptibility and phage host range govern interactions between lytic marine phages and their Flavobacterium hosts. Appl Environ Microbiol 73:6730–6739PubMedCrossRefGoogle Scholar
  21. Janech MG, Krell A, Mock T, Kang JS, Raymond JA (2006) Ice-binding proteins from sea ice diatoms (Bacillariophyceae). J Phycol 42:410–416CrossRefGoogle Scholar
  22. Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64:2780–2787PubMedGoogle Scholar
  23. Junge K, Krembs C, Deming J, Stierle A, Eicken H (2001) A microscopic approach to investigate bacteria under in situ conditions in sea-ice samples. Annal Glaciol 33:304–310CrossRefGoogle Scholar
  24. Junge K, Eicken H, Deming JW (2004) Bacterial activity at –2 to –20 degrees C in Arctic wintertime sea ice. Appl Environ Microbiol 70:550–557PubMedCrossRefGoogle Scholar
  25. Kiko R (2010) Acquisition of freeze protection in a sea-ice crustacean through horizontal gene transfer? Polar Biol 33:543–556CrossRefGoogle Scholar
  26. Kokjohn T (1989) Transduction: mechanism and potential for gene transfer in the environment. In: Levy S, Miller R (eds) Gene transfer in the environment. McGraw-Hill Publishing Co., New York, pp 73–97Google Scholar
  27. Lawrence JG, Hendrickson H (2003) Lateral gene transfer: when will adolescence end? Mol Microbiol 50:739–749PubMedCrossRefGoogle Scholar
  28. Laybourn-Parry J, Marshall W, Madan N (2007) Viral dynamics and patterns of lysogeny in saline Antarctic lakes. Polar Biol 30:351–358CrossRefGoogle Scholar
  29. Madan NJ, Marshall WA, Laybourn-Parry J (2005) Virus and microbial loop dynamics over an annual cycle in three contrasting Antarctic lakes. Freshwater Biol 50:1291–1300CrossRefGoogle Scholar
  30. Maranger R, Bird D (1995) Viral abundance in aquatic systems: a comparison between marine and fresh waters. Mar Ecol Prog Ser 121:217–226CrossRefGoogle Scholar
  31. Maranger R, Bird DF, Juniper SK (1994) Viral and bacterial dynamics in Arctic sea-ice during the spring algal bloom near Resolute, NWT, Canada. Mar Ecol Prog Ser 111:121–127CrossRefGoogle Scholar
  32. Middelboe M, Nielsen TG, Bjørnsen PK (2002) Viral and bacterial production in the North Water: in situ measurements, batch-culture experiments and characterization and distribution of a virus-host system. Deep-Sea Res Pt II 49:5063–5079CrossRefGoogle Scholar
  33. Miller R (2001) Environmental bacteriophage-host interactions: factors contribution to natural transduction. Antonie van Leeuwenhoek 79:141–147PubMedCrossRefGoogle Scholar
  34. Murray AG, Jackson GA (1992) Viral dynamics: a model of the effects of size shape, motion and abundance of single-celled planktonic organisms and other particles. Mar Ecol Prog Ser 89:103–116CrossRefGoogle Scholar
  35. 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 2:269–276PubMedCrossRefGoogle Scholar
  36. Payet JP, Suttle CA (2008) Physical and biological correlates of virus dynamics in the southern Beaufort Sea and Amundsen Gulf. J Mar Sys 74:933–945CrossRefGoogle Scholar
  37. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, ISBN 3-900051-07-0Google Scholar
  38. Raymond JA, Fritsen C, Shen K (2007) An ice-binding protein from an Antarctic sea ice bacterium. FEMS Microbiol Ecol 61:214–221PubMedCrossRefGoogle Scholar
  39. Replicon J, Frankfater A, Miller RV (1995) A continuous culture model to examine factors that affect transduction among Pseudomonas aeruginosa strains in freshwater environments. Appl Environ Microbiol 61:3359–3366PubMedGoogle Scholar
  40. Riedel A, Michel C, Gosselin M, LeBlanc B (2007) Enrichment of nutrients, exopolymeric substances and microorganisms in newly formed sea ice on the Mackenzie shelf. Mar Ecol Prog Ser 342:55–67CrossRefGoogle Scholar
  41. Säwström C, Lisle J, Anesio A, Priscu J, Laybourn-Parry J (2008) Bacteriophage in polar inland waters. Extremophiles 12:167–175PubMedCrossRefGoogle Scholar
  42. Saye DJ, Ogunseitan O, Sayler GS, Miller RV (1987) Potential for transduction of plasmids in a natural freshwater environment: effect of plasmid donor concentration and a natural microbial community on transduction in Pseudomonas aeruginosa. Appl Environ Microbiol 53:987–995PubMedGoogle Scholar
  43. Steward G, Smith D, Azam F (1996) Abundance and production of bacteria and viruses in the Bering and Chukchi Seas. Mar Ecol Prog Ser 131:287–300CrossRefGoogle Scholar
  44. Wells LE, Deming JW (2006a) Effects of temperature, salinity and clay particles on inactivation and decay of cold-active marine Bacteriophage 9A. Aquat Microb Ecol 45:31–39CrossRefGoogle Scholar
  45. Wells LE, Deming JW (2006b) Modelled and measured dynamics of viruses in Arctic winter sea-ice brines. Environ Microbiol 8:1115–1121PubMedCrossRefGoogle Scholar
  46. Wen K, Ortmann AC, Suttle CA (2004) Accurate estimation of viral abundance by epifluorescence microscopy. Appl Environ Microbiol 70:3862–3867PubMedCrossRefGoogle Scholar
  47. Wilhelm S, Brigden S, Suttle C (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
  48. Winget DM, Williamson KE, Helton RR, Wommack KE (2005) Tangential flow diafiltration: an improved technique for estimation of virioplankton production. Aquat Microb Ecol 41:221–232CrossRefGoogle Scholar
  49. Winter C, Herndl GJ, Weinbauer MG (2004) Diel cycles in viral infection of bacterioplankton in the North Sea. Aquat Microb Ecol 35:207–216CrossRefGoogle Scholar
  50. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114PubMedCrossRefGoogle Scholar
  51. Yager PL, Connelly TL, Mortazavi B, Wommack KE, Bano N, Bauer JE, Opsahl S, Hollibaugh JT (2001) Dynamic bacterial and viral response to an algal bloom at subzero temperatures. Limnol Oceanogr 46:790–801CrossRefGoogle Scholar
  52. Zinder ND, Lederberg J (1952) Genetic exchange in Salmonella. J Bacteriol 64:679–699PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.School of Oceanography and Astrobiology ProgramUniversity of WashingtonSeattleUSA
  2. 2.Origins InstituteMcMaster UniversityHamiltonCanada

Personalised recommendations