Synechococcus growth in the ocean may depend on the lysis of heterotrophic bacteria

Journal of Plankton Research

Volumn 33, Issue 10, 2011, Pages 1465-1476

  Weinbauer, Markus G ^a   Bonilla Findji, Osana ^a   Chan, Amy M ^b   Dolan, John R ^a   Short, Steven M ^c   Imek, Karel ^d   Wilhelm, Steven W ^e   Suttle, Curtis A ^b  

^a LABORATOIRE D OCÉANOGRAPHIE DE VILLEFRANCHE   (France)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^e UNIVERSITY OF TENNESSEE   (United States)

Author keywords

growth control of cyanobacteria; heterotrophic bacterioplankton; viruses

Indexed keywords

ABUNDANCE; BACTERIUM; DILUTION; EXPERIMENTAL STUDY; GROWTH RATE; HETEROTROPHY; INHIBITION; LYSIS; MARINE ENVIRONMENT; NUTRIENT CYCLING; SEAWATER; VIRUS;

BACTERIA (MICROORGANISMS); CYANOBACTERIA; SYNECHOCOCCUS;

EID: 80052600997     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbr041     Document Type: Article

References (68)

1. André, J. M., Navarette, C., Blanchot, J. et al. (1999) Picophytoplankton dynamics in the equatorial Pacific: growth and grazing rates from cytometric counts. J. Geophys. Res., 104, 3669-3380.
2. Ayukai, T. (1996) Possible limitation of the dilution technique for estimating growth and grazing mortality rates picoplancktonic cyano-bacteria in oligotrophic tropical waters. J. Exp. Mar. Biol. Ecol., 198, 101-111.
3. Baudoux, A.-C., Noordeloos, A., Veldhuis, M. et al. (2006) Virally induced mortality of Phaeocystsis globosa during two spring blooms in temperate coastal waters. Aquat. Microb. Ecol., 44, 207-217. (Pubitemid 44735072)
4. Baudoux, A.-C., Veldhuis, M., Noordeloos, A. A. et al. (2008) Estimates of virus grazing induced mortality of picophytoplankton in the North Sea during summer. Aquat. Microb. Ecol., 52, 69-82.
5. Baudoux, A.-C., Veldhuis, M., Witte, H. et al. (2007) Viruses as mortality agents of picophytoplankton in the deep chlorophyll maximum layer during IRONAGES III. Limnol. Oceanogr., 52, 2519-2529. (Pubitemid 350205805)
6. Bertilsson, S., Berglund, O., Karl, D. M. et al. (2003) Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr., 48, 1721-1731. (Pubitemid 37207580)
7. Bettarel, Y., Dolan, J. R., Hornak, K. et al. (2002) Strong, weak, and missing links in a microbial community of the NW Mediterranean Sea. FEMS Microbiol. Ecol., 42, 451-462. (Pubitemid 35346599)
8. Bonilla-Findji, O., Malits, A., Lefèvre, D. et al. (2008) Viral effects on bacterial respiration, production and growth efficiency: consistent trends in the Southern Ocean and the Mediterranean Sea. Deep-Sea Res. II., 55, 790-800.
9. Brussaard, C. P. D. (2004) Optimization of procedures for counting viruses by flow cytometry. Appl. Environ. Microbiol., 70, 1506-1513. (Pubitemid 38365132)
10. Brussaard, C. P. D., Timmermans, K. R., Uitz, J. et al. (2008a) Virioplankton dynamics and virally induced phytoplankton lysis versus microzooplankton grazing southeast of the Kerguelen (Southern Ocean). Deep Sea Res. Part II., 55, 752-765.
11. Brussaard, C. P. D., Wilhelm, S. W., Thingstad, T. F. et al. (2008b) Global-scale processes with a nanoscale drive: the role of marine viruses. ISME J., 2, 575-578. (Pubitemid 351793244)
12. Buitenhaus, E. T., Rivkin, R. B., Sailley, S. et al. (2010) Biogeochemical fluxes through microzooplankton. Global Biogeochem. Cycles, 24, GB4015, doi:10.1029/2009GB003601.
13. Cottrell, M. T. and Suttle, C. A. (1991) Wide-spread occurrence and clonal variation in viruses which cause lysis of a cosmopolitan, eukaryotic marine phytoplankter, Micromonas pusilla. Mar. Ecol. Prog. Ser., 78, 1-9.
14. Currie, D. J. and Kalff, J. (1984) A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus. Limnol. Oceanogr., 29, 298-310.
15. Dolan, J. R. and Simek, K. (1999) Diel periodicity in Synechococcus populations and grazing by heterotropohic nanoflagellates: analysis of food vacuole content. Limnol. Oceanogr., 44, 1565-1570. (Pubitemid 29405297)
16. Dolan, J. R., Thingstad, T. F. and Rassoulzadegan, F. (1995) Phosphate transfer between microbial size-fractions in Villefranche Bay (NW Mediterranean Sea), France in autumn 1992. Ophelia, 41, 71-85.
17. Evans, C., Archer, S., Jacquet, S. et al. (2003) Direct estimates of the contribution of viral lysis and microzooplankton grazing to the decline of a Micromonas spp. population. Aquat. Microb. Ecol., 30, 207-219. (Pubitemid 36251044)
18. Fuhrman, J. A. (1999) Marine viruses and their biogeochemical and ecological effects. Nature, 399, 541-548.
19. Garza, D. R. and Suttle, C. A. (1998) The effect of cyanophages on the mortality of Synechococcus spp. and selection for UV resistant viral communities. Microb. Ecol., 36, 281-292. (Pubitemid 29014576)
20. Gasol, J. M. and del Giorgio, P. (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar., 64, 197-224. (Pubitemid 30615216)
21. Gobler, C. J., Hutchins, D. A., Fisher, N. S. et al. (1997) Release and bioavailability of C, N, P, Se and Fe following viral lysis of a marine chrysophyte. Limnol. Oceanogr., 42, 1492-1504. (Pubitemid 28181001)
22. Goldman, J. C., Caron, D. A. and Dennett, M. R. (1987) Regulation of gross growth efficiency and ammonium regeneration in bacteria by substrate C:N ratio. Limnol. Oceanogr., 32, 1239-1252.
23. Hagström, A., Azam, F., Andersson, A. et al. (1988) Microbial loop in an oligotrophic pelagic marine ecosystem: possible roles of cyano-bacteria and nanoflagellates in the organic fluxes. Mar. Ecol. Prog. Ser., 49, 171-178.
24. Hennes, K. P. and Suttle, C. A. (1995) Direct counts of viruses in natural waters and laboratory cultures by epifluorescence microscopy. Limnol. Oceanogr., 40, 1050-1055. (Pubitemid 26454093)
25. Hurley, M. A. and Roscoe, M. E. (1983) Automated statistical analysis of microbial enumeration by dilution series. J. Appl. Bacteriol., 55, 159-164.
26. Jacquet, S., Delesalle, B., Torréton, J.-P. et al. (2006) Response of phy-toplankton communities to increased anthropogenic influences (Southwestern Lagoon, New Caledonia). Mar. Ecol. Prog. Ser., 320, 65-78. (Pubitemid 44504605)
27. Kimmance, S. A., Wilson, W. H. and Archer, S. D. (2007) Modified dilution technique to estimate viral versus grazing mortality of phy-toplankton: limitations associated with method sensitivity in natural waters. Aquat. Microb. Ecol., 49, 207-222. (Pubitemid 351525772)
28. Kirchman, D. L. and Wheeler, P. A. (1998) Uptake of ammonium and nitrate by heterotrophic bacteria and phytoplankton in the sub-Arctic Pacific. Deep-Sea Res. I, 45, 347-365. (Pubitemid 28335768)
29. Landry, M. R. and Hassett, R. P. (1982) Estimating the grazing impact of marine micro-zooplankton. Mar. Biol., 67, 283-288.
30. Landry, M. R., Selph, K. E., Taylor, A. G. et al. (2010) Phytoplankton growth, grazing and production balances in the HNLC equatorial Pacific. Deep-Sea Res. Part II, 58, 524-535.
31. Lee, S. and Fuhrman, J. A. (1987) Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol., 53, 1298-1303.
32. Li, W. K. W. (1994) Primary production of prochlorophytes, cyanobac-teria, and eukaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol. Oceanogr., 39, 169-175. (Pubitemid 2050709)
33. Liu, H., Campell, L., Landry, M. R. et al. (1998) Prochlorococcus and Synechococcus growth rates and contributions to production in the Arabian Sea during the 1995 southwest and northeast monsoons. Deep-Sea Res. II, 45, 2327-2352. (Pubitemid 29006868)
34. Middelboe, M. and Jorgensen, N. (2006) Viral lysis of bacteria: an important source of dissolved amino acids and cell wall compounds. J. Mar. Biol. Ass. UK, 86, 605-612.
35. Middelboe, M., Jørgensen, N. O. G. and Kroer, N. (1996) Effects of viruses on nutrient turnover and growth efficiency of noninfected marine bacterioplankton. Appl. Environ. Microbiol., 62, 1991-1997.
36. Middelboe, M. and Lyck, P. (2002) Regeneration of dissolved organic matter by viral lysis in marine microbial communities. Aquat. Microb. Ecol., 27, 187-194. (Pubitemid 34287223)
37. Middelboe, M., Riemann, L., Steward, C. et al. (2003) Virus-induced transfer of organic carbon released between marine bacteria in a model community. Aquat. Microb. Ecol., 33, 1-10. (Pubitemid 37171945)
38. Motegi, C., Nagata, T., Miki, T. et al. (2009) Viral control of bacterial growth efficiency in marine pelagic environments. Limnol. Oceanogr., 54, 1901-1910.
39. Noble, R. T. and Fuhrman, J. A. (1999) Breakdown and microbial uptake of marine viruses and other lysis products. Aquat. Microb. Ecol., 20, 1-11. (Pubitemid 30144050)
40. Ortmann, A. C., Lawrence, J. E. and Suttle, C. A. (2002) Lysogeny and lytic viral production during a bloom of the cyanobacterium Synechococcus spp. Microb. Ecol., 43, 225-231. (Pubitemid 36941351)
41. Peduzzi, P. and Weinbauer, M. G. (1993) Effect of concentrating the virus-rich 2-200 nm size fraction of seawater on the formation of algal flocs (marine snow). Limnol. Oceanogr., 38, 1562-1565. (Pubitemid 2015370)
42. Poorvin, L., Rinta-Kanto, J. M., Hutchins, D. A. et al. (2004) Viral release of iron and its bioavailability to marine plankton. Limnol. Oceanogr., 49, 1734-1741. (Pubitemid 39320763)
43. Porter, K. G. and Feig, Y. S. (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol. Oceanogr., 25, 943-948.
44. Riemann, L. and Middelboe, M. (2002) Viral lysis of marine bacterio-plankton: implications for organic matter cycling and bacterial clonal composition. Ophelia, 56, 57-68.
45. Sullivan, M. B., Waterbury, J. B. and Chisholm, S. W. (2003) Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature, 424, 1047-1051. (Pubitemid 37064303)
46. Suttle, C. A. (1992) Inhibition of photosynthesis in phytoplankton by the submicron size fraction concentrated from seawater. Mar. Ecol. Prog. Ser., 87, 105-112.
47. Suttle, C. A. (2000) Cyanophages and their role in the ecology of cya-nobacteria. In Whitton, B. and Potts, M. (eds), The Ecology of Cyanobacteria. Kluwer Acadamic Publishers, The Netherlands, pp. 563-589.
48. Suttle, C. A. (2005) Viruses in the sea. Nature, 43, 356-361. (Pubitemid 41613491)
49. Suttle, C. A. and Chan, A. M. (1993) Marine cyanophages infecting oceanic and coastal strains of Synechococcus: abundance, morphology, cross-infectivity and growth characteristics. Mar. Ecol. Prog. Ser., 92, 99-109. (Pubitemid 24407363)
50. Suttle, C. A. and Chan, A. M. (1994) Dynamics and distribution of cyanophages and their effect on marine Synechococcus spp. Appl. Environ. Microbiol., 60, 3167-3174. (Pubitemid 24272340)
51. Suttle, C. A., Chan, A. M. and Cottrell, M. T. (1990a) Infection of phytoplankton by viruses and reduction of primary productivity. Nature, 347, 467-469.
52. Suttle, C. A., Chan, A. M. and Cottrell, M. T. (1991) Use of ultrafil-tration to isolate viruses from seawater which are pathogens of marine phytoplankton. Appl. Environ. Microbiol., 57, 721-726.
53. Suttle, C. A., Fuhrman, J. A. and Capone, D. G. (1990b) Rapid ammonium cycling and concentration-dependent partitioning of ammonium and phosphate: Implications for carbon transfer in planktonic communities. Limnol. Oceanogr., 35, 424-433.
54. Tanaka, T., Rassoulzadegan, F. and Thingstad, T. F. (2004) Orthophosphate uptake by heterotrophic bacteria, cyanobacteria, and autotrophic nanoflagellates in Villefranche Bay, Northwestern Mediterranean: vertical, seasonal, and short-term variations of the competitive relationship for phosphorus. Limnol. Oceanogr., 49, 1063-1072. (Pubitemid 39040343)
55. Thingstad, T. F. and Lignell, R. (1997) Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol., 13, 19-27. (Pubitemid 127476494)
56. Thingstad, T. F., Skjoldal, E. F. and Bohne, R. A. (1993) Phosphorus cycling and algal-bacterial competition in Sandsfjord, western Norway. Mar. Ecol. Prog. Ser., 99, 239-259. (Pubitemid 24415338)
57. Thingstad, T. F., Zweifel, U.-L. and Rassoulzadegan, F. (1998) P limitation of heterotrophic bacteria and phytoplankton in the northwestern Mediterranean. Limnol. Oceanogr., 43, 88-94. (Pubitemid 28290137)
58. Wang, K. and Chen, F. (2004) Genetic diversity and population dynamics of cyanophage communities in the Chesapeake Bay. Aquat. Microb. Ecol., 34, 105-116. (Pubitemid 39098824)
59. Waterbury, J. B. and Valois, F. W. (1993) Resistance to co-occurring phages enables marine Synechococcus communities to coexist with cyanophages abundant in seawater. Appl. Environ. Microbiol., 59, 3393-3399. (Pubitemid 23296459)
60. Wawrik, B., Paul, J. H., Bronk, D. A. et al. (2004) High rates of ammonium recycling drive phytoplankton productivity in the offshore Mississippi River plume. Aquat. Microb. Ecol., 35, 175-184. (Pubitemid 39098812)
61. Weinbauer, M. G. (2004) Ecology of prokaryotic viruses. FEMS Microbiol. Rev., 28, 127-181. (Pubitemid 38510500)
62. Weinbauer, M. G. and Suttle, C. A. (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. (Pubitemid 26399429)
63. Weinbauer, M. G. and Suttle, C. A. (1997) Comparison of epifluores-cence and transmission electron microscopy for counting viruses and bacteria in natural marine waters. Aquat. Microb. Ecol., 13, 225-232. (Pubitemid 127471729)
64. Weinbauer, M. G., Winter, C. and Höfle, M. G. (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. (Pubitemid 34287216)
65. Wilhelm, S. W. and Suttle, C. A. (1999) Viruses and nutrient cycles in the Sea. Bioscience, 49, 781-788. (Pubitemid 29456233)
66. Wilhelm, S. W. and Trick, C. G. (1994) Iron-limited growth of cyano-bacteria: multiple siderophore production is a common response. Limnol. Oceanogr., 39, 1979-1984.
67. Winter, C., Smit, A., Herndl, G. J. et al. (2004) Impact of virioplankton on archaeal and bacterial community richness in seawater batch cultures. Appl. Environ. Microbiol., 70, 804-813. (Pubitemid 38568202)
68. Zubkov, M. V., Fuchs, B. M., Tarran, G. A. et al. (2003) High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobac-teria as a key to their dominance in oligotrophic oceanic waters. Appl. Environ. Microbiol., 69, 1299-1304. (Pubitemid 36204867)