Skip to main content
SpringerLink
Log in

Seasonal Depth-Related Gradients in Virioplankton: Lytic Activity and Comparison with Protistan Grazing Potential in Lake Pavin (France)

  • Microbiology of aquatic systems
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

This study presents an original depth-related survey of virioplankton lytic activity in relation to prokaryotic production and potential protistan bacterivory in the deep (Z max = 92 m) meromictic volcanic Lake Pavin (Massif Central, France). The sampling strategy was designed to be representative of the physico-chemical gradients of the water column of the lake, and of the seasonal variability as well, i.e. 12 different depths sampled in triplicates from April to December 2005. In the space, viral lytic activity estimated from the frequency of visibly infected prokaryotic cells and from burst size over the study period generally decreased with depth. This was viewed as a paradox compared to the abundances of viruses and prokaryotes and to the prokaryotic production which increased with depth. The seasonal variability in viral lytic activity was correlated with prokaryotic variables (abundance and production) in the deepest waters, i.e. from the hypolimnion downwards. Compared to previous studies known from the mixolimnion, we conclude that the deep waters in Lake Pavin represent an exclusive environment for heterotrophic prokaryotes whose seasonal activity offers an optimal and unique resource for thriving viral communities, some of which may be typical, endemic to the ambient dark, cold and stable deep water masses. Overall, the main findings in the present study get well around a previous statement that the ecology of the deepest waters of Lake Pavin is essentially driven by the dark viral loop (dissolved organic matter–prokaryotes–viruses) processes, which can sequester organic matters and nutrients for a long-lived turnover time. This is in agreement with recent demonstrations from marine systems that meso- and bathypelagic waters are optimal environments for viral survival and proliferation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4

Similar content being viewed by others

References

  1. Aeschbach-Hertig W, Hofer M, Schmid M, Kipfer R, Imboden DM (2002) The physical structure and dynamics of a deep, meromictic crater lake (Lac Pavin, France). Hydrobiologia 487:111–136

    Article  CAS  Google Scholar 

  2. Almeida MA, Cunha MA, Alcantara F (2001) Loss of estuarine bacteria by viral infection and predation in microcosm conditions. Microb Ecol 42:562–571

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  4. Bergh Ø, Børsheim KY, Bratbak G, Heldal M (1989) High abundance of viruses found in aquatic environments. Nature 340:467–468

    Article  PubMed  CAS  Google Scholar 

  5. Bettarel Y, Amblard C, Sime-Ngando T, Carrias JF, Sargos D, Garabetian 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 

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

    Article  PubMed  CAS  Google Scholar 

  7. Billen G, Servais P, Becquevort S (1990) Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia 207:37–42

    Article  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

    Article  Google Scholar 

  9. Bird DF, Kalff J (1984) Empirical relationships between bacterial abundance and chlorophyll concentration in fresh and marine waters. Can J Fish Aquat Sci 41:1015–1023

    Article  Google Scholar 

  10. Bohannan BJM, Lenski RE (2000) The relative importance of competition and predation varies with productivity in a model community. Am Nat 156:329–340

    Article  Google Scholar 

  11. Bonilla-Findji O, Herndl GJ, Gattuso JP, Weinbauer MG (2009) Viral and flagellate control of prokaryotic production and community structure in offshore Mediterranean waters. Appl Environ Microbiol 75:4801–4812

    Article  PubMed  CAS  Google Scholar 

  12. Boras JA, Sala MM, Vazquez-Dominguez E, Weinbauer MG, Vaqué D (2009) Annual changes of bacterial mortality due to viruses and protists in an oligotrophic coastal environment (NW Mediterranean). Environ Microbiol 11:1181–1193

    Article  PubMed  CAS  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. Brum JR, Steward GF, Jiang SC, Jellison R (2005) Spatial and temporal variability of prokaryotes, viruses, and viral infections of prokaryotes in an alkaline, hypersaline lake. Aquat Microb Ecol 41:247–260

    Article  Google Scholar 

  15. Carrias JF, Amblard C, Bourdier G (1996) Protistan bacterivory in an oligomesotrophic lake: importance of attached ciliates and flagellates. Microb Ecol 31:249–268

    Article  PubMed  Google Scholar 

  16. Carrias JF, Amblard C, Quiblier-Lloberas C, Bourdier G (1998) Seasonal dynamics of free and attached heterotrophic nanoflagellates in an oligomesotrophic lake. Freshw Biol 39:101–111

    Article  Google Scholar 

  17. Carrick HJ, Fahnenstiel GL, Stoermer EF, Wetzel RG (1991) The importance of zooplankton-protozoan trophic couplings in Lake Michigan. Limnol Oceanogr 36:1135–1145

    Article  Google Scholar 

  18. Choi DH, Hwang CY, Cho BC (2003) Comparison of virus- and bacterivory-induced bacterial mortality in the eutrophic Masan Bay, Korea. Aquat Microb Ecol 30:117–125

    Article  Google Scholar 

  19. Cole JJ, Findlay S, Pace ML (1988) Bacterial production in fresh and saltwater acosystems: a cross-system overview. Mar Ecol Prog Ser 43:1–10

    Article  Google Scholar 

  20. Colombet J, Sime-Ngando T, Cauchie HM, Fonty G, Hoffman L, Demeure G (2006) Depth-related gradients of viral activity in Lake Pavin. Appl Environ Microbiol 72:4440–4445

    Article  PubMed  CAS  Google Scholar 

  21. Colombet J, Cauchie HM, Portelli C, Sime-Ngando T (2009) Seasonal depth-related gradients in virioplankton: standing stocks and relationships with microbial communities in Lake Pavin (France). Microb Ecol 58:728–736

    Article  PubMed  CAS  Google Scholar 

  22. Dolan JR, Gallegos CL (1991) Trophic couplings of rotifers, microflagellates, and bacteria during fall months in the Rhode River Estuary. Mar Ecol Prog Ser 77:147–156

    Article  Google Scholar 

  23. Ducklow HW, Carlson CA (1992) Oceanic bacterial production. Adv Microb Ecol 12:113–181

    Article  Google Scholar 

  24. Fenchel T (1982) Ecology of heterotrophic microflagellates. IV. Quantitative occurrence and importance as bacterial consumers. Mar Ecol Prog Ser 9:35–42

    Article  Google Scholar 

  25. Filippini M, Buesing N, Bettarel Y, Sime-Ngando T, Gessner MO (2006) Infection paradox: high abundance but low impact of freshwater benthic viruses. Appl Environ Microbiol 72:4893–4898

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  27. Fuhrman JA, Noble RT (1995) Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol Oceanogr 40:1236–1242

    Article  Google Scholar 

  28. Garza DR, Suttle CA (1998) The effect of cyanophages on the mortality of Synechococcus spp. and selection for UV resistant viral communities. Microb Ecol 36:281–292

    Article  PubMed  Google Scholar 

  29. Guixa-Boixereu N, Calderón-Paz JI, Heldal M, Bratbak G, Pedrós-Alió C (1996) Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat Microb Ecol 11:215–227

    Article  Google Scholar 

  30. Guixa-Boixereu N, Lysnes K, Pedrós-Alió C (1999) Viral lysis and bacterivory during a phytoplankton bloom in a coastal water microcosm. Appl Environ Microbiol 65:1949–1958

    PubMed  CAS  Google Scholar 

  31. Hennes KP, Simon M (1995) Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake. Appl Environ Microbiol 61:333–340

    PubMed  CAS  Google Scholar 

  32. Hofer JS, Sommaruga R (2001) Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat Microb Ecol 26:1–11

    Article  Google Scholar 

  33. Jacquet S, Domaizon I, Personnic S, Pradeep Ram AS, Heldal M, Duhamel S, Sime-Ngando T (2005) Estimates of protozoan- and viral- mediated mortality of bacterioplankton in Lake Bourget (France). Freshw Biol 50:627–645

    Article  CAS  Google Scholar 

  34. Jardillier L, Bettarel Y, Richardot M, Bardot C, Amblard C, Sime-Ngando T, Debroas D (2005) Effects of viruses and predators on prokaryotic community composition. Microb Ecol 50:557–569

    Article  PubMed  Google Scholar 

  35. Kirschner AKT, Velimirov B (1999) Modification of the H-leucine centrifugation method for determining bacterial protein synthesis in freshwater samples. Aquat Microb Ecol 17:201–206

    Article  Google Scholar 

  36. Lefèvre E, Bardot C, Noel C, Carrias JF, Viscogliosi E, Amblard C, Sime-Ngando T (2007) Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ Microbiol 9:61–71

    Article  PubMed  Google Scholar 

  37. Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71:7389–7400

    Article  PubMed  CAS  Google Scholar 

  38. Lepère C, Boucher D, Jardillier L, Domaizon I, Debroas D (2006) Succession and regulation factors of small eukaryote community composition in a lacustrine ecosystem (Lake Pavin). Appl Environ Microbiol 72:2971–2981

    Article  PubMed  Google Scholar 

  39. Magagnini M, Corinaldesi C, Monticelli LS, De Domenico E, Danovaro R (2007) Viral abundance and distribution in mesopelagic and bathypelagic waters of the Mediterranean Sea. Deep-Sea Res I 54:1209–1220

    Article  Google Scholar 

  40. Middelboe M (2000) Bacterial growth rate and marine virus-host dynamics. Microb Ecol 40:114–124

    PubMed  Google Scholar 

  41. Noble RT, Fuhrman JA (1997) Virus decay and its causes in coastal water. Appl Environ Microbiol 63:77–83

    PubMed  CAS  Google Scholar 

  42. Ory P, Hartmann HJ, Jude F, Dupuy C, Del Amo Y, Catala P, Mornet F, Huet V, Jan B, Vincent D, Sautour B, Montanié H (2010) Pelagic food web patterns: do they modulate virus and nanoflagellate effects on picoplankton during the phytoplankton spring bloom? Environ Microbiol 12:2755–2772

    PubMed  Google Scholar 

  43. Parada V, Sintes E, Van Aken HM, Weinbauer MG, Herndl GJ (2007) Viral abundance, decay, and diversity in the meso- and bathypelagic waters of the North Atlantic. Appl Environ Microbiol 73:4429–4438

    Article  PubMed  CAS  Google Scholar 

  44. Peduzzi P, Schiemer F (2004) Bacteria and viruses in the water column of tropical freshwater reservoirs. Environ Microbiol 6:707–715

    Article  PubMed  Google Scholar 

  45. Pourriot R, Meybeck M (eds) (1995) Limnologie générale. Masson, Paris, 956 pp

    Google Scholar 

  46. Pradeep Ram A, Sime-Ngando T (2008) Functional responses of prokaryotes and viruses to grazer effects and nutrient additions in freshwater microcosms. ISME J 2:498–509

    Article  PubMed  Google Scholar 

  47. Pradeep Ram AS, Boucher D, Sime-Ngando T, Debroas D, Romagoux JC (2005) Phage bacteriolysis, protistan bacterivory potential, and bacterial production in a freshwater reservoir: coupling with temperature. Microb Ecol 50:64–72

    Article  PubMed  CAS  Google Scholar 

  48. Pradeep Ram AS, Bashir A, Danger M, Carrias JF, Lacroix G, Sime-Ngando T (2010) High and differential viral infection rates within bacterial ‘morphopopulations’ in a shallow sand pit lake (Lac de Créteil, France). FEMS Microbiol Ecol 74:83–92

    Article  Google Scholar 

  49. Pradeep Ram AS, Rasconi S, Jobard M, Palesse S, Colombet J, Sime-Ngando T (2011) High lytic infection rates but low abundances of prokaryote viruses in a humic lake (Vassivière, Massif Central, France). Appl Environ Microbiol 77:5610–5618

    Article  Google Scholar 

  50. Proctor L, Fuhrman JA (1990) Viral mortality of marine bacteria and cyanobacteria. Nature 343:60–62

    Article  Google Scholar 

  51. Rassoulzadegan F (1993) Protozoan patterns in the Azam-Ammerman’s bacteria-phytoplankton mutualism. In: Guerrero R, Pedros-Alio C (eds) Trends in microbial ecology. Spanish Society for Microbiology, Barcelona, pp 435–439

    Google Scholar 

  52. Sanders RW, Porter KG, Bennett SJ, Debiase AE (1989) Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol Oceanogr 34:673–687

    Article  Google Scholar 

  53. Sherr EB, Sherr BF (1987) High rates of consumption of bacteria by pelagic ciliates. Nature 325:710–711

    Article  Google Scholar 

  54. Sime-Ngando T, Bourdier G, Amblard C, Pinel-Alloul B (1991) Short-term variations in specific biovolumes of different bacterial forms in aquatic ecosystems. Microb Ecol 21:211–226

    Article  Google Scholar 

  55. Simek K, Pernthaler J, Weinbauer MG, Hornak K, Dolan JR, Nedoma J, Masin M, Amann R (2001) Changes in bacterial community composition and dynamics and viral mortality rates associated with enhanced flagellate grazing in a mesoeutrophic reservoir. Appl Environ Microbiol 67:2723–2733

    Article  PubMed  CAS  Google Scholar 

  56. Sime-Ngando T, Bettarel Y, Chartogne C, Sean K (2003) The imprint of wild viruses on freshwater microbial ecology. Recent Res Dev Microbiol 7:481–497

    Google Scholar 

  57. Steward GF, Smith DC, Azam F (1996) Abundance and production of bacteria and viruses in the Bering and Chukchi Sea. Mar Ecol Prog Ser 131:287–300

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  59. Suttle CA, Chen F (1992) Mechanisms and rates of decay of marine viruses in seawater. Appl Environ Microbiol 58:3721–3729

    PubMed  CAS  Google Scholar 

  60. Suttle CA, Chan AM, Cottrell MT (1990) Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467–469

    Article  Google Scholar 

  61. Tanaka T, Rassoulzadegan F (2002) Full-depth profile (0–2000 m) of bacteria, heterotrophic nanoflagellates and ciliates in NW Mediterranean Sea: vertical partitioning of microbial trophic structures. Deep-Sea Res II 49:2093–2107

    Article  Google Scholar 

  62. Tanaka T, Rassoulzadegan F (2004) Vertical and seasonal variations of bacterial abundance and production in the mesopelagic layer of the NW Mediterranean Sea: bottom-up and top-down controls. Deep Sea Res I 51:531–544

    Article  CAS  Google Scholar 

  63. Tanaka T, Rassoulzadegan F, Thingstad TF (2004) Quantifying the structure of the mesopelagic microbial loop from observed depth profiles of bacteria and protozoa. Biogeosci Discuss 1:413–428

    Article  Google Scholar 

  64. Weinbauer MG, Peduzzi P (1994) Frequency, size and distribution of bacteriophages in different marine bacterial morphotypes. Mar Ecol Prog Ser 108:11–20

    Article  Google Scholar 

  65. 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 

  66. Weinbauer MG, Höfle MG (1998) Size-specific mortality of lake bacterioplankton by natural virus communities. Aquat Microb Ecol 15:103–113

    Article  Google Scholar 

  67. Weinbauer MG, Winter C, Höfle MG (2002) Reconsidering transmission electron microscopy based estimates of viral infection of bacterioplankton using conversion factors derived from natural communities. Aquat Microb Ecol 27:103–110

    Article  Google Scholar 

  68. Weinbauer MG, Brettar I, Höfle MG (2003) Lysogeny and virus-induced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol Oceanogr 48:169–177

    Article  Google Scholar 

  69. Weinbauer MG, Hornak K, Jezbera J, Nedoma J, Dolan JR, Simek K (2007) Synergistic and antagonistic effects of viral lysis and protistan grazing on bacterial biomass, production and diversity. Environ Microbiol 9:777–788

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  71. Zhang R, Weinbauer MG, Qian PY (2007) Viruses and flagellates sustain apparent richness and reduce biomass accumulation of bacterioplankton in coastal marine waters. Environ Microbiol 9:3008–3018

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

JC was supported by a Ph.D. Fellowship from the Grand Duché du Luxembourg (Ministry of Culture, High School, and Research). The study was partly supported by the French National Program ACI/FNS “ECCO” (VIRULAC research grant awarded to TSN, coordinator) and by the French ANR Program “Biodiversité” (AQUAPHAGE research grant to TSN, PI).

Author information

Authors and Affiliations

  1. Laboratoire Microorganismes: Génome et Environnement, Clermont Université Blaise Pascal, UMR CNRS 6023, 24 avenue des Landais, BP 80026, 63171, Aubière, France

    Jonathan Colombet & Télesphore Sime-Ngando

Authors
  1. Jonathan Colombet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Télesphore Sime-Ngando
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Télesphore Sime-Ngando.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Colombet, J., Sime-Ngando, T. Seasonal Depth-Related Gradients in Virioplankton: Lytic Activity and Comparison with Protistan Grazing Potential in Lake Pavin (France). Microb Ecol 64, 67–78 (2012). https://doi.org/10.1007/s00248-012-0032-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-012-0032-z

Keywords

Search

Navigation