Viral activity in two contrasting lake ecosystems

Applied and Environmental Microbiology

Volumn 70, Issue 5, 2004, Pages 2941-2951

  Bettarel, Yvan ^a,c   Sime Ngando, Télesphore ^a   Amblard, Christian ^a   Dolan, John ^b  

^a UNIVERSITÉ BLAISE PASCAL   (France)

^b LABORATOIRE D OCÉANOGRAPHIE DE VILLEFRANCHE   (France)

^c SMITHSONIAN ENVIRONMENTAL RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CELLS; ECOSYSTEMS; LAKES; TRANSMISSION ELECTRON MICROSCOPY; VIRUSES;

EUTROPIC LAKES; FRESHWATERS;

MICROBIOLOGY;

BACTERIVORY; FLAGELLATE; GRAZING; LAKE ECOSYSTEM; VERTICAL PROFILE; VIRUS;

ANOXIA; AQUATIC ENVIRONMENT; ARTICLE; AUTUMN; BACTERICIDAL ACTIVITY; CILIATE; CYTOLYSIS; FLAGELLATE; FRESHWATER ENVIRONMENT; GROWTH RATE; HETEROTROPHY; LAKE ECOSYSTEM; NONHUMAN; SPRING; TRANSMISSION ELECTRON MICROSCOPY; VIRUS INFECTION; VIRUS PARTICLE;

ANIMALS; BACTERIA; BACTERIOPHAGES; CILIOPHORA; ECOSYSTEM; FRESH WATER; LYSOGENY; MASTIGOPHORA; OXYGEN; PREDATORY BEHAVIOR; TEMPERATURE;

EURASIA; EUROPE; FRANCE; MASSIF CENTRAL; WESTERN EUROPE;

BACTERIA (MICROORGANISMS); CILIOPHORA; MASTIGOPHORA (FLAGELLATES); PROTISTA;

EID: 2442658221     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.5.2941-2951.2004     Document Type: Article

References (68)

1. Azam, F., T. Fenchel, J. G. Field, J. S. Gray, L. A. Meyer-Reil, and T. F. Thingstad. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10:257-263.
2. Bell, R. T. 1993. Estimating production of heterotrophic bacterioplankton via incorporation of tritiated thymidine, p. 495-503. In P. F. Kemp, B. F. Sherr, E. B. Sherr, and J. J. Cole (ed.), Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, Fla.
3. Bergh, O., K. Y. Børsheim, G. Bratbak, and M. Heldal. 1989. High abundance of viruses found in aquatic environments. Nature 340:467-468.
4. Bettarel, Y., J. R. Dolan, K. Hornak, R. Lemee, M. Masin, M.-L. Pedrotti, E. Rochell-Newell, K. Simek, and T. Sime-Ngando. 2002. Strong, weak, and missing links in a microbial community of the N. W. Mediterranean Sea. FEMS Microb. Ecol. 42:451-462.
5. Bettarel, Y., C. Amblard, T. Sime-Ngando, J.-F. Carrias, D. Sargos, F. Garabetian, and P. Lavandier. 2003. Viral lysis, flagellate grazing potential, and bacterial production in Lake Pavin. Microb. Ecol. 45:119-127.
6. Bettarel, Y., T. Sime-Ngando, C. Amblard, J.-F. Carrias, and C. Portelli. 2003. Virioplankton and microbial communities in aquatic systems: a seasonal study in two lakes of different trophy. Freshw. Biol. 48:810-820.
7. Billen, G., P. Servais, and S. Becquevort. 1990. Dynamics of bacterioplankton in oligotrophic and eutrophic aquatic environments: bottom-up or top-down control? Hydrobiologia 207:37-42.
8. Binder, B. 1999. Reconsidering the relationship between virally induced bacterial mortality and frequency of infected cells. Aquat. Microb. Ecol. 18:207-215.
9. Bratbak, G., M. Heldal, T. F. Thingstad, B. Riemann, and O. H. Haslund. 1992. Incorporation of viruses into the budget of microbial C-transfer. A first approach. Mar. Ecol. Prog. Ser. 83:273-280.
10. Carrias, J. F., C. Amblard, and G. Bourdier. 1996. Protistan bacterivory in an oligomesotrophic lake: importance of attached ciliates and flagellates. Microb. Ecol. 31:249-268.
11. Carrias, J. F., C. Amblard, C. Quiblier-Lloberas, and G. Bourdier. 1998. Seasonal dynamics of free and attached heterotrophic nanoflagellates in an oligomesotrophic lake. Freshw. Biol. 39:91-101.
12. Choi, D. H., C. Y. Hwang, and B. C. Cho. 2003. Comparison of virus- and bacterivory-induced bacterial mortality in the eutrophic Masan Bay, Korea. Aquat. Microb. Ecol. 30:117-125.
13. Christaki, U., J. R. Dolan, S. Pelegri, and F. Rassoulzadegan. 1998. Consumption of picoplankton-size particles by marine ciliates: effects of physiological state of the ciliate and particle quality. Limnol. Oceanogr. 43:458-464.
14. Christaki, U., S. Jacquet, J. R. Dolan, S. D. Vaulot, and F. Rassoulzadegan. 1999. Growth and grazing on Prochlorococcus and Synechococcus by two marine ciliates. Limnol. Oceanogr. 44:52-61.
15. Dominik, K., and M. G. Höfle. 2002. Changes in bacterioplankton community structure and activity with depth in a eutrophic lake as revealed by 5S rRNA analysis. Appl. Environ. Microbiol. 68:3606-3613.
16. Fischer, U. R., and B. Velimirov. 2002. High control of bacterial production by viruses in a eutrophic oxbow lake. Aquat. Microb. Ecol. 27:1-12.
17. Fuhrman, J. A., and R. T. Noble. 1995. Viruses and protists cause similar bacterial mortality in coastal seawater. Limnol. Oceanogr. 40:1236-1242.
18. Guixa-Boixareu, N., J. I. Calderon-Paz, M. Heldal, G. Bratbak, and C. Pedros-Alio. 1996. Viral lysis and bacterivory as prokaryotic loss factors along a salinity gradient. Aquat. Microb. Ecol. 11:215-227.
19. Guixa-Boixareu, N., D. Vaque, J. M. Gasol, and C. Pedros-Alio. 1999. Distribution of viruses and their potential effect on bacterioplankton in an oligotrophic marine system. Aquat. Microb. Ecol. 19:205-213.
20. Guixa-Boixareu, N., K. Lysnes, and C. Pedros-Alio. 1999. Viral lysis and bacterivory during a phytoplankton bloom in a coastal water microcosm. Appl. Environ. Microbiol. 65:1949-1958.
21. Heldal, M., and G. Bratbak. 1991. Production and decay of viruses in aquatic environments. Mar. Ecol. Prog. Ser. 72:205-212.
22. Hennes, K. P., and M. Simon. 1995. Significance of bacteriophages for controlling bacterioplankton growth in a mesotrophic lake. Appl. Environ. Microbiol. 61:333-340.
23. Hewson, I., J. M. O'Neil, J. A. Fuhrman, and W. C. Dennison. 2001. Virus-like particle distribution and abundance in sediments and overlaying waters along eutrophication gradients in two subtropical estuaries. Limnol. Oceanogr. 46:1734-1746.
24. Hofer, J. S., and R. Sommaruga. 2001. Seasonal dynamics of viruses in an alpine lake: importance of filamentous forms. Aquat. Microb. Ecol. 26:1-11.
25. Höfle, M. G., and I. Brettar. 1995. Taxonomic diversity and metabolic activity of microbial communities in the water column of the central Baltic Sea. Limnol. Oceanogr. 40:868-874.
26. Hwang, C. Y., and B. C. Cho. 2002. Virus-infected bacteria in oligotrophic open waters of the East Sea, Korea. Aquat. Microb. Ecol. 30:1-9.
27. Jones, R. I., and S. Rees. 1994. Characteristics of particle uptake by the phagotrophic phytoflagellate, Dinobryon divergens. Mar. Microb. Food Webs 8:97-110.
28. Jonsson, P. R. 1986. Particle size selection, feeding rates, and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora, Oligotrichida). Mar. Ecol. Prog. Ser. 33:265-277.
29. Mathias, C. B., K. T. Kirschner, and B. Velimirov. 1995. Seasonal variations of virus abundance and viral control of the bacterial population in backwater system of the Danube River. Appl. Environ. Microbiol. 61:3734-3740.
30. McManus, G. B., and J. A. Fuhrman. 1988. Control of marine bacterioplankton populations: measurement and significance of grazing. Hydrobiologia 159:51-62.
31. Middelboe, M. 2000. Bacterial growth rate and marine virus-host dynamics. Microb. Ecol. 40:114-124.
32. Murray, A. G., and P. M. Eldridge. 1994. Marine viral ecology: incorporation of bacteriophages into the microbial planktonic food web paradigm. J. Plankton Res. 16:627-641.
33. Noble, R. T., and J. A. Fuhrman. 1997. Virus decay and its causes in coastal waters. Appl. Environ. Microbiol. 63:77-83.
34. Noble, R. T., and J. A. Fuhrman. 2000. Rapid virus production and removal as measured with fluorescently labeled viruses as tracers. Appl. Environ. Microb. 66:3790-3797.
35. Organization for Economic Cooperation and Development. 1982. Eutrophication of waters: monitoring, assessment and control. Environment Directorate, OECD, Paris, France.
36. Pace, M. L., and M. D. Bailif. 1987. Evaluation of fluorescent microsphere technique for measuring grazing rates of phagotrophic microorganisms. Mar. Ecol. Prog. Ser. 40:185-193.
37. Pedros-Alio, C., J. I. Calderon-Paz, and J. M. Gasol. 2000. Comparative analysis shows that bacterivory, not viral lysis, controls the abundance of heterotrophic prokaryotic plankton. FEMS Microbiol. Ecol. 32:157-165.
38. Proctor, L. M., and J. A. Fuhrman. 1990. Viral mortality of marine bacteria and cyanobacteria. Nature 343:60-62.
39. Proctor, L. M. 1997. Advances in the study of marine viruses. Microsc. Res. Tech. 37:136-161.
40. Rioual, P. 2002. Limnological characteristics of 25 lakes of the French Massif Central. Ann. Limnol. 38:311-327.
41. Sanders, R. W., K. G. Porter, S. J. Bennett, and A. E. Debiase. 1989. Seasonal patterns of bacterivory by flagellates, ciliates, rotifers, and cladocerans in a freshwater planktonic community. Limnol. Oceanogr. 34:673-687.
42. Šimek, K., J. Pernthaler, M. G. Weinbauer, K. Hornak, J. R. Dolan, J. Nedoma, M. Masin, and R. Amann. 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.
43. Sime-Ngando, T., G. Bourdier, C. Amblard, and B. Pinel-Alloul. 1991. Short-term variations in specific biovolumes of different forms in aquatic ecosystems. Microb. Ecol. 21:211-226.
44. Sime-Ngando, T., J.-P. Mignot, C. Amblard, G. Bourdier, C. Desvilettes, and C. Quiblier-Lloberas. 1996. Characterization of planktonic virus-like particles in a French mountain lake: methodological aspects and preliminary results. Ann. Limnol. 32:1-5.
45. Steward, G. F., J. Wikner, D. C. Smith, W. P. Chochlan, and F. Azam. 1992. Estimation of virus production in the sea. I. Method development. Mar. Microb. Food Webs 6:57-78.
46. Steward, G. F., D. C. Smith, and F. Azam. 1996. Abundance and production of bacteria and viruses in the Bering and Chukchi Seas. Mar. Ecol. Prog. Ser. 131:287-300.
47. Strom, S. L. 2000. Bacterivory: interactions between bacteria and their grazers, p. 351-386. In D. L. Kirchman (ed.), Microbial ecology of the oceans. Wiley-Liss, Inc., New York, N.Y.
48. Suttle, C. A., and F. Chen. 1992. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58:3721-3729.
49. Suttle, C. A. 1994. The significance of virus to mortality in aquatic microbial communities. Microb. Ecol. 28:237-243.
50. Tapper, M. A., and R. E. Hicks. 1998. Temperate viruses and lysogeny in Lake Superior bacterioplankton. Limnol. Oceanogr. 43:95-103.
51. Thingstad, T. F. 2000. Elements of theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45:1320-1328.
52. Thouvenot, A., M. Richardot, D. Debroas, and J. Devaux. 1999. Bacterivory of metazooplankton, ciliates and flagellates in a newly flooded reservoir. J. Plankton Res. 21:1659-1679.
53. Tuomi, P., C. Lundsgaard, J. Ekebom, K. Olli, and K. Kunnis. 1999. The production and potential loss mechanisms of bacterial biomass in the southern Gulf of Riga. J. Mar. Syst. 23:185-196.
54. Vrede, K., U. S. Tensdotter, and E. S. Lindstrom. 2003. Viral and bacterioplankton dynamics in two lakes with different humic contents. Microb. Ecol. 46:406-415.
55. Weinbauer, M. G., D. Fuks, and P. Peduzzi. 1993. Distribution of viruses and dissolved DNA along a coastal trophic gradient in the northern Adriatic Sea. Appl. Environ. Microbiol. 59:4074-4082.
56. Weinbauer, M. G., and P. Peduzzi. 1995. Significance of viruses versus heterotrophic nanoflagellates for controlling bacterial abundance in the northern Adriatic Sea. J. Plankton Res. 17:1851-1856.
57. Weinbauer, M. G., D. Fuks, S. Puskaric, and P. Peduzzi. 1995. Diel, seasonal and depth-related variability of viruses and dissolved DNA in the northern Adriatic Sea. Microb. Ecol. 30:25-41.
58. Weinbauer, M. G., and M. G. Höfle. 1998. Significance of viral lysis and flagellate grazing as factors controlling bacterioplankton production in a eutrophic lake. Appl. Environ. Microbiol. 64:431-438.
59. Weinbauer, M. G., and M. G. Höfle. 1998. Size-specific mortality of lake bacterioplankton by natural virus communities. Aquat. Microb. Ecol. 15:103-113.
60. Weinbauer, M. G., C. Winter, and M. G. Höfle. 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.
61. Weinbauer, M. G., U. Christaki, J. Nedoma, and K. Simek. 2003. Comparing the effects of resource enrichment and grazing on viral production in a meso-eutrophic reservoir. Aquat. Microb. Ecol. 31:137-144.
62. Weinbauer, M. G., I. Brettar, and M. G. Höfle. 2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep and anoxic marine waters. Limnol. Oceanogr. 48:1457-1465.
63. 3H]thymidine in aquatic bacterial production studies. J. Plankton Res. 9:1159-1166.
64. Wilhelm, S. W., M. G. Weinbauer, C. A. Suttle, and W. H. Jeffrey. 1998. The role of sunlight in the removal and repair of viruses in the sea. Limnol. Oceanogr. 43:586-592.
65. Wilhelm, S. W., and R. E. H. Smith. 2000. Bacterial carbon production in Lake Erie is influenced by viruses and solar radiation. Can. J. Fish. Aquat. Sci. 57:317-326.
66. Wilhelm, S. W., S. Briden, and C. A. Suttle. 2002. A dilution technique for the direct measurement of viral production: a comparison in stratified and tidally mixed coastal waters. Microb. Ecol. 43:168-173.
67. Wommack, K. E., R. T. Hill, T. A. Muller, and R. R. Colwell. 1996. Effects of sunlight on bacteriophage viability and structure. Appl. Environ. Microbiol. 62:1336-1341.
68. Wommack, K. E., and R. R. Colwell. 2000. Virioplankton: viruses in aquatic ecosystems. Microbiol. Mol. Biol. Rev. 64:69-114.