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Seasonal Viral Loop Dynamics in Two Large Ultraoligotrophic Antarctic Freshwater Lakes

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Abstract

The effect of viruses on the microbial loop, with particular emphasis on bacteria, was investigated over an annual cycle in 2003–2004 in Lake Druzhby and Crooked Lake, two large ultraoligotrophic freshwater lakes in the Vestfold Hills, Eastern Antarctica. Viral abundance ranged from 0.16 to 1.56 × 109 particles L-1;1 and bacterial abundances ranged from 0.10 to 0.24 × 109 cells L-1;1, with the lowest bacterial abundances noted in the winter months. Virus-to-bacteria ratios (VBR) were consistently low in both lakes throughout the season, ranging from 1.2 to 8.4. lysogenic bacteria, determined by induction with mitomycin C, were detected on three sampling occasions out of 10 in both lakes. In Lake Druzhby and Crooked Lake, lysogenic bacteria made up between 18% and 73% of the total bacteria population during the lysogenic events. Bacterial production ranged from 8.2 to 304.9 × 106 cells L-1;1 day-1;1 and lytic viral production ranged from 47.5 to 718.4 × 106 viruslike particles L-1;1 day-1;1. When only considering primary production, heterotrophic nanoflagellate (HNF) grazing and viral lysis as the major contributors to the DOC pool (i.e., autochthonous sources), we estimated a high contribution from viruses during the winter months when >60% of the carbon supplied to the DOC pool originated from viral lysis. In contrast, during the summer <20% originated from viral lysis. Our study shows that viral process in ultraoligotrophic Antarctic lakes may be of quantitative significance with respect to carbon flow especially during the dark winter period.

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References

  1. Ackermann, HW, Dubow, MS (1987) Viruses of prokaryotes, Vol. 1, In: General Properties of Bacteriophages. CRC Press, Boca Raton

  2. Aiken, G, McKnight, D, Harnish, R, Wershaw, R (1996) Geochemistry of aquatic humic substances in the Lake Fryxell Basin, Antarctica. Biogeochemistry 34: 157–188

    Article  CAS  Google Scholar 

  3. Azam, F, Fenchel, T, Field, JG, Gray, JS, Meyer-Reil, LA, Thingstad, TF (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257–263

    Google Scholar 

  4. Bayliss, P, Ellis-Evans, JC, Laybourn-Parry, J (1997) Temporal patterns of primary production in a large ultraoligotrophic Antarctic freshwater lake. Polar Biol 18: 363–370

    Article  Google Scholar 

  5. Bell, RT (1993) Estimating production of hetertrophic bacterioplankton via the incorporation of tritiated thymidine. In: Kemp, BF, Sherr, EB, Cole, JJ (Eds.) Handbook of Methods in Aquatic Microbial Ecology, CRC Press, Boca Raton, pp 495–503

    Google Scholar 

  6. Bettarel, Y, Amblard, C, Sime-Ngando, T, Carrias, J-F, Sargos, D, Garabétian, F, Lavandier, P (2003) Viral lysis, flagellate grazing potential and bacterial production in Lake Pavin. Microb Ecol 45: 119–127

    Article  PubMed  CAS  Google Scholar 

  7. Bettarel, Y, Sime-Ngando, T, Amblard, C, Dolan, C (2004) Viral activity in two contrasting lake ecosystems. Appl Environ Microbiol 70: 2941–2951

    Article  PubMed  CAS  Google Scholar 

  8. Binder, B (1999) Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquat Microb Ecol 18: 207–215

    Google Scholar 

  9. Bratbak, G, Dundas, I (1984) Bacterial dry matter content and biomass estimations. Appl Environ Microbiol 48: 755–757

    PubMed  CAS  Google Scholar 

  10. Bratbak, G, Heldal, M (2000) Viruses rule the waves—the smallest and most abundant members of marine ecosystems. Microbiol Today 27: 171–173

    Google Scholar 

  11. 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: 273–280

    Google Scholar 

  12. Choi, DH, Hwang, CY, Byung, CC (2003) Comparision of virus- and bacteriovory-induced bacterial mortality in the eutrophic Masan Bay, Korea. Aquat Microb Ecol 30: 117–125

    Google Scholar 

  13. Cole, JJ, Carpenter, SR, Kitchell, JF, Pace, ML (2002) Pathways of organic carbon utilization in small lakes: results from whole-lake 13C addition and coupled model. Limnol Oceanogr 47: 1664–1675

    Article  CAS  Google Scholar 

  14. Cole, JJ (1999) Aquatic microbiology for ecosystem scientists: new and recycled paradigms in ecological microbiology. Ecosystems 2: 215–225

    Article  Google Scholar 

  15. Dartnall, HJG (2000) A limnological reconnaissance of the Vestfold Hills. ANARE Rep 141: 57

    Google Scholar 

  16. del Giorgio, P, Cole, JJ (1998) Bacterial growth efficiency in natural aquatic systems. Annu Rev Ecol Syst 29: 503–541

    Article  Google Scholar 

  17. Fischer, UR, Velimirov, B (2002) High control of bacterial production by viruses in a eutrophic oxbow lake. Aquat Microb Ecol 27: 1–12

    Google Scholar 

  18. Fuhrman, JA (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541–548

    Article  PubMed  CAS  Google Scholar 

  19. 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: 1492–1504

    CAS  Google Scholar 

  20. Henshaw, T, Laybourn-Parry, J (2002) The annual patterns of photosynthesis in two large freshwater, ultra-oligotrophic Antarctic lakes. Polar Biol 25: 744–752

    Google Scholar 

  21. Jespersen, AM, Christoffersen, K (1987) Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109: 445–454

    CAS  Google Scholar 

  22. 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: 235–243

    Article  PubMed  Google Scholar 

  23. Kepner, RL, Wharton, RA, Suttle, CA (1998) Viruses in Antarctic lakes. Limnol Oceanogr 43: 1754–1761

    Article  PubMed  Google Scholar 

  24. Kirchman, D (2001) Measuring bacterial biomass production and growth rates from leucine incorporation in natural aquatic environments. In: Paul, JH (Ed.) Marine Microbiology—Methods in Microbiology, Academic Press, London, pp 225–237

    Google Scholar 

  25. Laybourn-Parry, J (1997) The microbial loop in the Antarctic lakes. In: Lyons, WB, Howard-Williams, C, Hawes, I (Eds.) Ecosystem Processes in Antarctic Ice-Free Landscapes, Balkema, Rotterdam, Netherlands, pp 231–240

  26. Laybourn-Parry, J (2002) Survival mechanisms in Antarctic lakes. Philos Trans R Soc Lond B 357: 863–869

    Article  CAS  Google Scholar 

  27. Laybourn-Parry, J, Bayliss, P (1996) Seasonal dynamics of the planktonic community in Lake Druzhby. Princess Elizabeth Land, Eastern Antarctica. Freshw Biol 35: 57–67

    Article  Google Scholar 

  28. Laybourn-Parry, J, Bayliss, P, Ellis-Evans, JC (1995) The dynamics of heterotrophic nanoflagellates in a large ultra-oligotrophic Antarctic lake. J Plank Res 17: 1835–1850

    Article  Google Scholar 

  29. Laybourn-Parry, J, Henshaw, T, Jones, DJ, Quayle, W (2004) Bacterioplankton production in freshwater Antarctic lakes. Freshw Biol 49: 735–744

    Article  CAS  Google Scholar 

  30. Laybourn-Parry, J, Hofer, JS, Sommaruga, R (2001) Viruses in the plankton of freshwater and saline antarctic lakes. Freshw Biol 46: 1279–1287

    Article  Google Scholar 

  31. Laybourn-Parry, J, Marchant, HJ, Brown, PE (1992) Seasonal cycle of the microbial plankton in Crooked Lake, Antarctica. Polar Biol 12: 411–416

    Google Scholar 

  32. 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: 427–439

    Article  PubMed  CAS  Google Scholar 

  33. Mackereth, FJH, Heron, J, Talling, JF (1989) Water analysis. Freshwater Biological Association UK, Publ No 36

  34. 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: 1291–1300

    Article  Google Scholar 

  35. Middelboe, M, Jørgensen, NOG, Kroer, N (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl Environ Microbiol 62: 1991–1997

    PubMed  CAS  Google Scholar 

  36. Middelboe, M, Lyck, PG (2002) Regeneration of dissolved organic matter by viral lysis in marine microbial communities. Aquat Microb Ecol 27: 187–194

    Google Scholar 

  37. Murray, AG, Eldridge, PM (1994) Marine viral ecology: incorporation of bacteriophage into the microbial planktonic food web paradigm. J Plank Res 16: 627–641

    Article  Google Scholar 

  38. Noble, RT, Fuhrman, JA (1998) Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat Microb Ecol 14: 113–118

    Google Scholar 

  39. Parker, BC, Simmons, GM (1985) Paucity of nutrient cycling and absence of food chains in the unique lakes of southern Victoria Land. In: Sigfried, WR, Condy, RR, Laws, RM, (Eds.) Antarctic Nutrient Cycles and Food Webs, Springer-Verlag, Berlin, pp 238–244

    Google Scholar 

  40. Paul, JH, Jiang, SC (2001) Lysogeny and transduction. In: Paul, JH (Ed.) Marine Microbiology—Methods in Microbiology, Academic Press, London, pp 105–125

    Chapter  Google Scholar 

  41. Parada, V, Herndl, GJ, Weinbauer, MG (2006) Viral burst size of heterotrophic prokaryotes in aquatic systems. J Mar Biol Assoc UK 86: 613–621

    Article  Google Scholar 

  42. Priscu, JC, Wolf, CF, Takacs, CD, Fritsen, CH, Laybourn-Parry, J, Roberts, EC, Sattler, B, Lyons, WB (1999) Carbon transformations in a perennially ice-covered Antarctic lake. BioScience 49: 997–1008

    Article  Google Scholar 

  43. Strayer, D (1988) On the limits to secondary production. Limnol Oceanogr 33: 1217–1220

    Article  Google Scholar 

  44. Suttle, CA (2005) Viruses in the sea. Nature 437: 356–361

    Article  PubMed  CAS  Google Scholar 

  45. Takacs, CD, Priscu, JC, McKnight, DM (2001) Bacterial dissolved organic carbon demand in McMurdo Dry Valley Lakes, Antarctica. Limnol Oceanogr 46: 1189–1194

    Article  CAS  Google Scholar 

  46. Tapper, MA, Randall, EH (1998) Temperate viruses and lysogeny in lake superior bacterioplankton. Limnol Oceanogr 43: 95–103

    Article  Google Scholar 

  47. Theil-Nielsen, J, Søndergaard, M (1998) Bacterial carbon biomass calculated from biovolumes. Arch Hydrobiol 141: 195–207

    CAS  Google Scholar 

  48. Thingstad, TF (2000) Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol Oceanogr 45: 1320–1328

    Article  Google Scholar 

  49. Thingstad, TF, Heldal, M, Bratbak, G, Dundas, I (1993) Are viruses important partners in pelagic food webs? TREE 8: 209–212

    Google Scholar 

  50. Weinbauer, MG, Brettar, I, Höfle, MG (2003) Lysogeny and virus-induced mortality of bacetrioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48: 1457–1465

    Article  Google Scholar 

  51. 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: 431–438

    PubMed  CAS  Google Scholar 

  52. Weinbauer, MG, Suttle, CA (1999) Lysogeny and prophage induction in coastal and offshore bacterial communities. Aquat Microb Ecol 18: 217–225

    Google Scholar 

  53. Williamson, SJ, Houchin, LA, McDaniel, L, Paul, JH (2002) Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol 68: 4307–4314

    Article  PubMed  CAS  Google Scholar 

  54. Wilhelm, SW, Suttle, CA (1999) Viruses and nutrient cycles in the sea. BioSci 49: 781–788

    Article  Google Scholar 

  55. Wommack, KE, Colwell, RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64: 69–114

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was funded by a Marie Curie Scholarship, the Australian Antarctic Division and VR the Swedish Research Council. We thank the crew at Davis Station, Antarctica 2003/2004 for logistical support and field assistance.

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Authors and Affiliations

  1. Climate Impacts Research Centre (CIRC), Department of Ecology and Environmental Science, Umeå University, SE-901 87, Umeå, Sweden

    Christin Säwström

  2. Institute of Biological Sciences, University of Wales, Aberystwyth, SY23 3DA, UK

    M. Alexandre Anesio

  3. Department of Limnology, Ecology Building, Lund University, Lund, S-223 62, Sweden

    Wilhelm Granéli

  4. Institute for the Environment, Physical Sciences and Applied Mathematics, University of Keele, Staffordshire, ST5 5BG, UK

    Johanna Laybourn-Parry

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  1. Christin Säwström
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  2. M. Alexandre Anesio
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  4. Johanna Laybourn-Parry
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Correspondence to Christin Säwström.

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Säwström, C., Anesio, M.A., Granéli, W. et al. Seasonal Viral Loop Dynamics in Two Large Ultraoligotrophic Antarctic Freshwater Lakes. Microb Ecol 53, 1–11 (2007). https://doi.org/10.1007/s00248-006-9146-5

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  • DOI: https://doi.org/10.1007/s00248-006-9146-5

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