To kill or not to kill: The balance between lytic and lysogenic viral infection is driven by trophic status

Limnology and Oceanography

Volumn 58, Issue 2, 2013, Pages 465-474

  Payet, Jérôme P ^a,b   Suttle, Curtis A ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABUNDANCE; BACTERIUM; CARBON CYCLE; CHLOROPHYLL A; DATA SET; MORTALITY; ORGANIC CARBON; SEASONAL VARIATION; SPATIOTEMPORAL ANALYSIS; TROPHIC STATUS; VIRAL DISEASE;

ARCTIC OCEAN; BEAUFORT SEA; CANADA; CANADIAN ARCTIC;

EID: 84875288872     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2013.58.2.0465     Document Type: Article

References (44)

1. Alonso-Sáez, L., O. SANCHEZ, J. GASOL, V. BALAGUE, and C. Pedrós-Alió. 2008. Winter-to-summer changes in the composition and single-cell activity of near-surface Arctic prokaryotes. Environ. Microbiol. 10: 2444-2454. doi:10.1111/j.1462-2920.2008.01674.x
2. ANGLY, F. E., and OTHERS. 2006. The marine viromes of four oceanic regions. PLoS Biol. 4: 2121-2131. doi:10.1371/journal.pbio.0040368
3. BONGIORNI, L., M. MAGAGNINI, M. ARMENI, R. NOBLE, and R. DANOVARO. 2005. Viral production, decay rates, and life strategies along a trophic gradient in the North Adriatic Sea. Appl. Environ. Microbiol. 71: 6644-6650. doi:10.1128/ AEM.71.11.6644-6650.2005
4. BRUGEL, S., and OTHERS. 2009. Phytoplankton biomass and production in the southeastern Beaufort Sea in autumn 2002 and 2003. Mar. Ecol. Prog. Ser. 377: 63-77. doi:10.3354/ meps07808
5. BRUSSAARD, C. P. D., J. P. PAYET, C. WINTER, and M. G. WEINBAUER. 2010. Quantification of aquatic viruses by flow cytometry, p. 102-109. In S. W. Wilhelm, M. G. Weinbauer, and C. A. Suttle [eds.], Manual of aquatic viral ecology. ASLO. doi:10.4319/mave.2010.978-0-9845591-0-7
6. BRUSSOW, H., C. CANCHAYA, and W.-D. HARDT. 2004. Phages and the evolution of bacterial pathogens: From genomics rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68: 560-602. doi:10.1128/MMBR.68.3.560-602.2004
7. CARMACK, E. C., and R. W. MACDONALD. 2002. Oceanography of the Canadian shelf of the Beaufort Sea: A setting for marine life. Arctic 55: 29-45.
8. CARMACK, E. C., and R. W. MACDONALD, and S. JASPER. 2004. Phytoplankton productivity on the Canadian Shelf of the Beaufort Sea. Mar. Ecol. Prog. Ser. 227: 37-50. doi:10.3354/meps277037
9. Chibani-Chennoufi, S., A. BRUTTIN, M.-L. DILLMANN, and H. BRUSSOW. 2004. Phage-host interaction: An ecological perspective. J. Bacteriol. 186: 3677-3686. doi:10.1128/ JB.186.12.3677-3686.2004
10. COCHRAN, P. K., and J. H. PAUL. 1998. Seasonal abundance of lysogenic bacteria in a subtropical estuary. Appl. Environ. Microbiol. 64: 2308-2312.
11. FORTIER, L., and J. K. COCHRAN. 2008. Introduction to special section on annual cycles on the Arctic Ocean Shelf. J. Geophys. Res. 113: C03S00. doi:10.1029/2007JC004457
12. FUHRMAN, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 299: 541-548. doi:10.1038/ 21119
13. GARNEAU, M.-È., S. ROY, C. LOVEJOY, Y. GRATTON, and W. F. VINCENT. 2008. Seasonal dynamics of bacterial biomass and production in a coastal arctic ecosystem: Franklin Bay, western Canadian Arctic. J. Geophys. Res. 113: C07S91. doi:10.1029/2007JC004281
14. GARNEAU, M.-È., W. F. VINCENT, L. Alonso-Sáez, and Y. GRATTON. 2006. Prokaryotic community structure and heterotrophic production in a river-influenced coastal arctic ecosystem. Aquat. Microb. Ecol. 42: 27-40. doi:10.3354/ame042027
15. GARNEAU, M.-È., W. F. VINCENT, R. TERRADO, and C. LOVEJOY. 2009. Importance of particle-associated bacterial heterotrophy in a coastal Arctic ecosystem. J. Mar. Syst. 75: 185-197. doi:10.1016/ j.jmarsys.2008.09.002
16. JIANG, S. C., and J. H. PAUL. 1996. Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Mar. Ecol. Prog. Ser. 142: 27-38. doi:10.3354/meps142027
17. LONG, A., L. D. MCDANIEL, J. MOBBERLEY, and J. H. PAUL. 2008. Comparison of lysogeny (prophage induction) in heterotrophic bacterial and Synechococcus populations in the Gulf of Mexico and Mississippi river plume. ISME J. 2: 132-144. doi:10.1038/ismej.2007.102
18. MIDDELBOE, M., N. JØRGENSEN, and N. KROER. 1996. Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl. Environ. Microbiol. 62: 1991-1997.
19. MIDDELBOE, M., T. NIELSEN, and P. BJØRNSEN. 2002. Viral and bacterial production in the North Water: In situ measurements, batchculture experiments and characterization and distribution of a virus-host system. Deep-Sea Res. II 49: 5063-5079. doi:10.1016/S0967-0645(02)00178-9
20. NOBLE, R. T., and J. A. FUHRMAN. 1998. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Appl. Environ. Microbiol. 59: 905-911.
21. PAUL, J. H. 2008. Prophages in marine bacteria: Dangerous molecular time bombs or the key to survival in the seas? ISME J. 2: 579-589. doi:10.1038/ismej.2008.35
22. PAUL, J. H., and M. G. WEINBAUER. 2010. Detection of lysogeny in marine environments, p. 30-33. In S. W. Wilhelm, M. G. Weinbauer, and C. A. Suttle [eds.], Manual of aquatic viral ecology. ASLO.
23. PAYET, J. P., and C. A. SUTTLE. 2008. Physical and biological correlates of virus dynamics in the southern Beaufort Sea and Amundsen Gulf. J. Mar. Syst. 74: 933-945. doi:10.1016/ j.jmarsys.2007.11.002
24. ROWE, J. M., and OTHERS. 2008. Constraints on virus production in the Sargasso Sea and North Atlantic. Aquat. Microb. Ecol. 52: 233-244. doi:10.3354/ame01231
25. SHELFORD, E. J., M. MIDDELBOE, E. F. MØLLER, and C. A. SUTTLE. 2012. Virus-driven nitrogen cycling enhances phytoplankton growth. Aquat. Microb. Ecol. 66: 41-46. doi:10.3354/ame01553
26. STEIN, R., and R. W. MACDONALD [EDS.], The organic carbon cycle in the Arctic Ocean. Springer.
27. STEWARD, G. F., D. 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. doi:10.3354/ meps131287
28. SUTTLE, C. A. 2005. Viruses in the sea. Nature 437: 356-361. doi:10.1038/nature04160
29. SUTTLE, C. A., and J. A. FUHRMAN. 2010. Enumeration of virus particles in aquatic or sediment samples by epifluorescence microscopy, p. 145-153. In S. W. Wilhelm, M. G. Weinbauer, and C. A. Suttle [eds.], Manual of aquatic viral ecology. ASLO. doi:10.4319/mave.2010.978-0-9845591-0-7
30. VALLIÉRES, C., L. RETAMAL, C. OSBURN, and W. F. VINCENT. 2008. Bacterial production and microbial food web structure in a large arctic river and the coastal Arctic Ocean. J. Mar. Syst. 74: 756-773. doi:10.1016/j.jmarsys.2007.12.002
31. VINCENT, W. F., and C. Pedrós-Alió. 2008. Sea ice and life in a river-influenced arctic shelf ecosystem. J. Mar. Syst. 74: 739-1024. doi:10.1016/j.jmarsys.2008.03.003
32. WEINBAUER, M. G. 2004. Ecology of prokaryotic viruses. FEMS Microbiol. Rev. 28: 127-181. doi:10.1016/j.femsre.2003.08.00
33. WEINBAUER, M. G., J.-M. ARRIETA, C. GRIEBLER, and G. J. HERNDL. 2009. Enhanced viral production and infection of bacterioplankton during an iron induced phytoplankton bloom in the Southern Ocean. Limnol. Oceanogr. 54: 774-784. doi:10.4319/ lo.2009.54.3.0774
34. WEINBAUER, M. G., I. BRETTAR, and M. HOFLE. 2003. Lysogeny and virusinduced mortality of bacterioplankton in surface, deep, and anoxic marine waters. Limnol. Oceanogr. 48: 1457-1465. doi:10.4319/lo.2003.48.4.1457
35. WEINBAUER, M. G., J. M. ROWE, and S. W. WILHELM. 2010. Determining rates of virus production in aquatic systems by the virus reduction approach, p. 1-8. In S. W. Wilhelm, M. G. Weinbauer, and C. A. Suttle [eds.], Manual of aquatic viral ecology. ASLO. doi:10.4319/mave.2010.978-0-9845591-0-7
36. WEINBAUER, M. G., and C. A. SUTTLE. 1996. Potential significance of lysogeny to bacteriophage production and bacterial mortality in coastal waters of the Gulf of Mexico. Appl. Environ. Microbiol. 62: 4374-4380.
37. WEINBAUER, M. G., and C. A. SUTTLE. 1999. Lysogeny and prophage induction in coastal and offshore bacterial communities. Aquat. Microb. Ecol. 18: 217-225. doi:10.3354/ame018217
38. WEINBAUER, M. G., and OTHERS. 2011. Synechococcus growth in the ocean may depend on the lysis of heterotrophic bacteria. J. Plankton Res. 33: 1465-1476. doi:10.1093/plankt/fbr041
39. WELLS, L. E., and J. W. DEMING. 2006. Significance of bacteriovory and viral lysis in bottom waters of Franklin Bay, Canadian Arctic, during winter. Aquat. Microb. Ecol. 43: 209-221. doi:10.3354/ame043209
40. WILHELM, S. W., S. M. BRIGDEN, and C. A. SUTTLE. 2002. A dilution technique for the direct measurement of viral production: A comparison in stratified and tidally mixed coastal waters. Microbial. Ecol. 43: 168-173. doi:10.1007/ s00248-001-1021-9
41. WILHELM, S. W., and C. A. SUTTLE. 1999. Viruses and nutrient cycles in the sea. Bioscience 49: 781-788. doi:10.2307/1313569
42. WILLIAMSON, S. J., L. A. HOUCHIN, L. D. MCDANIEL, and J. H. PAUL. 2002. Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl. Environ. Microbiol. 68: 4307-4314. doi:10.1128/AEM.68.9.43074314.2002
43. WINGET, D. M., R. R. HELTON, K. E. WILLIAMSON, S. R. BENCH, S. J. WILLIAMSON, and K. E. WOMMACK. 2011. Repeating patterns of virioplankton production within an estuaring ecosystem. Proc. Natl. Acad. Sci. USA 106: 11506-11511. doi:10.1073/pnas.1101907108
44. WINGET, D. M., K. E. WILLIAMSON, R. R. HELTON, and K. E. WOMMACK. 2005. Tangential flow diafiltration: an improved technique for estimation of virioplankton production. Aquat. Microb. Ecol. 41: 221-232. doi:10.3354/ame041221