Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies

Applied and Environmental Microbiology

Volumn 73, Issue 2, 2007, Pages 554-562

  Martínez Martínez, Joaquín ^a,e   Schroeder, Declan C ^b   Larsen, Aud ^c   Bratbak, Gunnar ^c   Wilson, William H ^a,d  

^a PLYMOUTH MARINE LABORATORY   (United Kingdom)

^b THE LABORATORY   (United Kingdom)

^c UNIVERSITY OF BERGEN   (Norway)

^d BIGELOW LABORATORY FOR OCEAN SCIENCES   (United States)

^e ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELLS; ELECTROPHORESIS; GENES; MOLECULAR DYNAMICS; PROTEINS;

CALCIUM-BINDING MOTIFS (GPA); EMILIANIA HUXLEYI; GENOTYPES; HUXLEYI ALLELES; INFECTIONS; MAJOR CAPSID PROTEIN (MCP);

VIRUSES;

CAPSID PROTEIN;

ALGAL BLOOM; FJORD; GENETIC ANALYSIS; GENETIC VARIATION; GENOTYPE; MESOCOSM; MOLECULAR ANALYSIS; PHYTOPLANKTON; VIRUS;

ALLELE; ARTICLE; CALCIUM BINDING; DENATURING GRADIENT GEL ELECTROPHORESIS; EMILIANIA HUXLEYI; FLOW CYTOMETRY; GENETIC CODE; GENETIC VARIABILITY; GENOTYPE; GPA GENE; HOST; MESOCOSM; MICROBIAL GENETICS; MICROFLORA; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOPLANKTON; PROTEIN BINDING; PROTEIN MOTIF; SEQUENCE ANALYSIS; VIRUS; VIRUS GENE;

ALGAE; BASE SEQUENCE; ECOSYSTEM; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLOW CYTOMETRY; GENOTYPE; MOLECULAR SEQUENCE DATA; NORWAY; SEAWATER; SEQUENCE ANALYSIS, DNA; VIRUSES;

EMILIANIA HUXLEYI; MIRIDAE;

EID: 33846436106     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00864-06     Document Type: Article

References (52)

1. Allen, M. J., J. Martínez Martínez, D. C. Schroeder, P. J. Somerfield, and W. H. Wilson. Use of microarrays to assess viral diversity: from genotype to phenotype. Environ. Microbiol., in press.
2. Antia, J. J., C. D. McAllister, P. T. R., K. Stephens, and J. D. H. Strickland. 1963. Further measurements of primary production using a large-volume plastic sphere. Oceanography 8:166-183.
3. Bergh, O., K. Y. Borsheim, G. Bratbak, and M. Heldal. 1989. High abundance of viruses found in aquatic environments. Nature 340:467-468.
4. Bratbak, G., J. K. Egge, and M. Heldal. 1993. Viral mortality of the marine alga Emiliania huxleyi (Haptophyceae) and termination of algal blooms. Mar. Ecol. Prog. Ser. 93:39-48.
5. Brussaard, C. P. D., R. S. Kempers, A. J. Kop, R. Riegman, and M. Heldal. 1996. Virus-like particles in a summer bloom of Emiliania huxleyi in the North Sea. Aquat. Microb. Ecol. 10:105-113.
6. Brussaard, C. P. D., R. Thyrhaug, D. Marie, and G. Bratbak. 1999. Flow cytometric analyses of viral infection in two marine phytoplankton species, Micromonas pusilla (Prasinophyceae) and Phaeocystis pouchetii (Prymnesiophyceae). J. Phycol. 35:941-948.
7. Castberg, T., A. Larsen, R. A. Sandaa, C. P. D. Brussaard, J. K. Egge, M. Heldal, R. Thyrhaug, E. J. van Hannen, and G. Bratbak. 2001. Microbial population dynamics and diversity during a bloom of the marine coccolithophorid Emiliania huxleyi (Haptophyta). Mar. Ecol. Prog. Ser. 221:39-46.
8. Castberg, T., R. Thyrhaug, A. Larsen, R. A. Sandaa, M. Heldal, J. L. van Etten, and G. Bratbak. 2002. Isolation and characterization of a virus that infects Emiliania huxleyi (Haptophyta). J. Phycol. 38:767-774.
9. Chen, F., and C. A. Suttle. 1995. Amplification of DNA polymerase gene fragments from viruses infecting microalgae. Appl. Environ. Microbiol. 61: 1274-1278.
10. Corstjens, P., A. van der Kooij, C. Linschooten, G. J. Brouwers, P. Westbroek, and E. W. de Vrind-de Jong. 1998. GPA, a calcium-binding protein in the coccolithophorid Emiliania huxleyi (Prymnesiophyceae). J. Phycol. 34:622-630.
11. Cottrell, M. T., and C. A. Suttle. 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.
12. Davis, C. O. 1982. The importance of understanding phytoplankton life strategies in the design of enclosures experiments, p. 323-332. In G. D. Grice and M. R. Reeve (ed.), Marine mesocosms. Biological and chemical research in experimental ecosystems. Springer-Verlag, New York, NY.
13. Egge, J. K. 1993. Nutrient control of phytoplankton growth: effects of macronutrient composition (N, P, Si) on species succession. Ph.D. thesis. University of Bergen, Bergen, Norway.
14. Egge, J. K., and D. L. Aksnes. 1992. Silicate as regulating nutrient in phytoplankton competition. Mar. Ecol. Prog. Ser. 83:281-289.
15. Egge, J. K., and B. R. Heimdal. 1994. Blooms of phytoplankton including Emiliania huxleyi (Haptophyta)-effects of nutrient supply in different N-P ratios. Sarsia 79:333-348.
16. Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399:541-548.
17. Iglesias-Rodriguez, M. D., A. G. Saez, R. Groben, K. J. Edwards, J. Batley, L. K. Medlin, and P. K. Hayes. 2002. Polymorphic microsatellite loci in global populations of the marine coccolithophorid Emiliania huxleyi. Mol. Ecol. Notes 2:495-497.
18. Jacquet, S., M. Heldal, D. Iglesias-Rodriguez, A. Larsen, W. Wilson, and G. Bratbak. 2002. Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquat. Microb. Ecol. 27:111-124.
19. Larsen, A., T. Castberg, R. A. Sandaa, C. P. D. Brussaard, J. Egge, M. Heldal, A. Paulino, R. Thyrhaug, E. J. van Hannen, and G. Bratbak. 2001. Population dynamics and diversity of phytoplankton, bacteria and viruses in a seawater enclosure. Mar. Ecol. Prog. Ser. 221:47-57.
20. Malin, G., S. Turner, P. Liss, P. Holligan, and D. Harbour. 1993. Dimethylsulfide and dimethylsulphoniopropionate in the northeast Atlantic during the summer coccolithophore bloom. Deep-Sea Res. Part I Oceanogr. Res. Pap. 40:1487-1508.
21. Mann, N. H. 2003. Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol. Rev. 27:17-34.
22. Martínez Martínez, J., S. Norland, F. Thingstad, D. C. Schroeder, G. Bratbak, W. H. Wilson, and A. Larsen. 2006. Variability in microbial population dynamics between similarly perturbed mesocosms. J. Plankton Res. 28:783-791.
23. McAllister, C. D., K. S. Parsons, and J. D. H. Strickland. 1961. Measurements of primary production in coastal seawater using a large-volume plastic sphere. Limnol. Oceanogr. 6:237-258.
24. Medlin, L. K., G. L. A. Barker, L. Campbell, J. C. Green, P. K. Hayes, D. Marie, S. Wrieden, and D. Vaulot. 1996. Genetic characterisation of Emiliania huxleyi (Haptophyta). J. Mar. Syst. 9:13-31.
25. Middelboe, M., L. Riemann, G. F. Steward, V. Hansen, and O. Nybroe. 2003. Virus-induced transfer of organic carbon between marine bacteria in a model community. Aquat. Microb. Ecol. 33:1-10.
26. Mühling, M., N. J. Fuller, A. Millard, P. J. Somerfield, D. Marie, W. H. Wilson, D. J. Scanlan, A. F. Post, I. Joint, and N. H. Mann. 2005. Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: evidence for viral control of phytoplankton. Environ. Microbiol. 7:499-508.
27. Muyzer, G., and K. Smalla. 1998. Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Leeuwenhoek Int. J. Gen. Mol. Microbiol. 73:127-141.
28. Noble, R. T., and J. A. Fuhrman. 1998. Use of SYBR Green I for rapid epifluorescence counts of marine viruses and bacteria. Aquat. Microb. Ecol. 14:113-118.
29. Petersen, D. G., and I. Dahllöf. 2005. Improvements for comparative analysis of changes in diversity of microbial communities using internal standards in PCR-DGGE. FEMS Microbiol. Ecol. 53:339-348.
30. Proctor, L. M., and J. A. Fuhrman. 1990. Viral mortality of marine-bacteria and cyanobacteria. Nature 343:60-62.
31. Schafer, H., P. Servais, and G. Muyzer. 2000. Successional changes in the genetic diversity of a marine bacterial assemblage during confinement. Arch. Microbiol. 173:138-145.
32. Schroeder, D. C., G. F. Biggi, M. Hall, J. Davy, J. Martínez Martínez, A. J. Richardson, G. Malin, and W. H. Wilson. 2005. A genetic marker to separate Emiliania huxleyi (Prymnesiophyceae) morphotypes. J. Phycol. 41:874-879.
33. Schroeder, D. C., J. Oke, M. Hall, G. Malin, and W. H. Wilson. 2003. Virus succession observed during an Emiliania huxleyi bloom. Appl. Environ. Microbiol. 69:2484-2490.
34. Schroeder, D. C., J. Oke, G. Malin, and W. H. Wilson. 2002. Coccolithovirus (Phycodnaviridae): characterisation of a new large dsDNA algal virus that infects Emiliania huxleyi. Arch. Virol. 147:1685-1698.
35. Short, S. M., and C. A. Suttle. 2002. Sequence analysis of marine virus communities reveals that groups of related algal viruses are widely distributed in nature. Appl. Environ. Microbiol. 68:1290-1296.
36. Short, S. M., and C. A. Suttle. 2003. Temporal dynamics of natural communities of marine algal viruses and eukaryotes. Aquat. Microb. Ecol. 32:107-119.
37. Suttle, C. 2005. Viruses in the sea. Nature 437:356-361.
38. Suttle, C. A., and A. M. Chan. 1994. Dynamics and distribution of cyanohpphages and their effect on marine Synechococcus spp. Appl. Environ. Microbiol. 60:3167-3174.
39. Suttle, C. A., and A. M. Chan. 1993. Marine cyanophages infecting oceanic and coastal strains of Synechococcus-abundance, morphology, cross-infectivity and growth characteristics. Mar. Ecol. Prog. Ser. 92:99-109.
40. Suttle, C. A., A. M. Chan, and M. T. Cottrell. 1990. Infection of phytoplankton by viruses and reduction of primary productivity. Nature 347:467-469.
41. Suttle, C. A., and C. Feng. 1992. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58:3721-3729.
42. Thingstad, T. F. 2000. Elements of a theory for the mechanisms controlling abundance, diversity, and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnol. Oceanogr. 45:1320-1328.
43. Weinbauer, M. G., and F. Rassoulzadegan. 2004. Are viruses driving microbial diversification and diversity? Environ. Microbiol. 6:1-11.
44. Weinbauer, M. G., S. W. Wilhelm, C. A. Suttle, R. J. Pledger, and D. L. Mitchell. 1999. Sunlight-induced DNA damage and resistance in natural viral communities. Aquat. Microb. Ecol. 17:111-120.
45. Wilhelm, S. W., and C. A. Suttle. 1999. Viruses and nutrient cycles in the sea-viruses play critical roles in the structure and function of aquatic food webs. BioScience 49:781-788.
46. Wilson, W. H., G. Tarran, and M. V. Zubkov. 2002. Virus dynamics in a coccolithophore-dominated bloom in the North Sea. Deep-Sea Res. Part II Top. Stud. Oceanogr. 49:2951-2963.
47. Wilson, W. H., G. A. Tarran, D. Schroeder, M. Cox, J. Oke, and G. Malin. 2002. Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. U.K. 82:369-377.
48. Wilson, W. H., S. Turner, and N. H. Mann. 1998. Population dynamics of phytoplankton and viruses in a phosphate-limited mesocosm and their effect on DMSP and DMS production. Estuar. Coast. Shelf Sci. 46:49-59.
49. 48a. Wilson, W. H., D. C. Schroeder, M. J. Allen, M. T. G. Holden, J. Parkhill, B. G. Barrell, C. Churcher, N. Hamlin, K. Mungall, H. Norbertczak, M. A. Quail, C. Price, E. Rabbinowitsch, D. Walker, M. Craigon, D. Roy, and P. Ghazal. 2005. Complete genomic sequence and lytic phase transcription profile of a coccolithovirus. Science 309:1090-1092.
50. Wommack, K. E., R. T. Hill, M. Kessel, E. Russekcohen, and R. R. Colwell. 1992. Distribution of viruses in the Chesapeake Bay. Appl. Environ. Microbiol. 58:2965-2970.
51. 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.
52. Ziveri, P., A. T. C. Broerse, J. E. van Hinte, P. Westbroek, and S. Honjo. 2000. The fate of coccoliths at 48 degrees N 21 degrees W, northeastern Atlantic. Deep-Sea Res. Part II Top. Stud. Oceanogr. 47:1853-1875.