In situ survey of life cycle phases of the coccolithophore Emiliania huxleyi (Haptophyta)

Environmental Microbiology

Volumn 14, Issue 6, 2012, Pages 1558-1569

  Frada, Miguel J ^a,b   Bidle, Kay D ^c   Probert, Ian ^a   de Vargas, Colomban ^a  

^a CNRS   (France)

^b UNIVERSITY OF LISBON   (Portugal)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; CELL CYCLE; DIPLOIDY; EUTROPHICATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; HAPLOIDY; HAPTOPHYTA; LIFE CYCLE STAGE; PHYSIOLOGY; PHYTOPLANKTON; VIROLOGY;

ANIMALS; CELL CYCLE; DIPLOIDY; EUTROPHICATION; HAPLOIDY; HAPTOPHYTA; IN SITU HYBRIDIZATION, FLUORESCENCE; LIFE CYCLE STAGES; PHYTOPLANKTON;

EMILIANIA HUXLEYI; HAPTOPHYCEAE; MASTIGOPHORA (FLAGELLATES);

EID: 84861925307     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02745.x     Document Type: Article

References (63)

1. Ameisen, J.C. (2002) On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ 9: 367-393.
2. Balestra, B., Ziveri, P., Monechi, S., and Troelstra, S. (2004) Coccolithophorids from the southeast Greenland margin (northern north atlantic): production ecology and the surface sediment record. J Nannoplankton Res 50: 23-34.
3. Bidle, K.D., and Vardi, A. (2011) chemical arms race at sea mediates algal host-virus interactions. Curr Opin Microbiol 14: 1-9.
4. Bidle, K.D., Haramaty, L., Ramos, J.B.E., and Falkowski, P. (2007) Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc Natl Acad Sci USA 104: 6049-6054.
5. Billard, C. (1994) Life cycles. In The Haptophyta Algae. Green, J.C., and Leadbeater, B.S.C. (eds). Oxford, UK: Clarendon Press, pp. 167-186.
6. Bratbak, G., Egge, J., and Heldal, M. (1993) Viral mortality of the marine alga Emiliania huxelyi (Haptophyceae) and the termination of the algal bloom. Mar Ecol Prog Ser 93: 39-48.
7. Brown, C.W., and Yoder, J.A. (1994) Coccolithophorid blooms in the global ocean. J Geophys Res 99: 7467-7482.
8. Campbell, L., Shapiro, L.P., and Haugen, E. (1994) Immunochemical characterization of eukaryotic ultraplankton from the Atlantic and Pacific Oceans. J Plankton Res 16: 35-51.
9. Charlson, R.J., Lovelock, J.E., Andreae, M.C., and Warren, S.G. (1987) Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate. Nature 326: 655-661.
10. Costas, E., and Varela, M. (1989) Circannual rhythm in cyst formation and growth rates in the dinoflagellate Scrippsiella trochoidea Stein. Chronobiologica 16: 265-270.
11. Cowart, L.A., Okamoto, Y., Lu, X., and Hannun, Y.A. (2006) Distinct roles for de novo versus hydrolytic pathways of sphingolipid biosynthesis in Saccharomyces cerevisiae. Biochem J 393: 733-740.
12. Cros, L. (2002) Planktonic Coccolithophores of the NW Mediterranean. Barcelona, Spain: Universitat de Barcelona.
13. von Dassow, P., Ogata, H., Probert, I., Wincker, P., Da Silva, C., Audic, S., etal. (2009) Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biol 10: R114.
14. 2 during experimental blooms of the coccolithophorid Emiliania huxleyi. Global Biogeochem Cycles 19: GB2023.
15. Egge, J.K., and Heimdal, B.R. (1994) Blooms of phytoplankton including Emiliania huxleyi (Haptophyta). Effects of nutrient supply in different N:P ratios. Sarsia 79: 333-348.
16. Evans, C., Malin, G., Mills, G.P., and Wilson, W.H. (2006) Viral infection of Emiliania huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J Phycol 42: 1040-1047.
17. 3 optical detection with fluorescent in situ hybridization: a new method to identify and quantify calcifying microorganisms from the oceans. J Phycol 42: 1162-1169.
18. Frada, M., Probert, I., Allen, A.E., Wilson, W.H., and de Vargas, C. (2008) The 'Cheshire Cat' escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc Natl Acad Sci USA 105: 15944-15949.
19. Frada, M., Young, J., Cachão, M., Lino, S., Martins, A., Narciso, A., etal. (2010) A guide to extant coccolithophores (Calcihaptophycidae, Haptophyta) using light microscopy. J Nannoplankton Res 31: 58-112.
20. Gayral, P., and Fresnel, J. (1983) Description, sexualité et cycle de développement d'une nouvelle Coccolithophoracée (Prymnesiophyceae): Pleurochrysis pseudoroscoffensis sp. nov. Protistologica 19: 245-261.
21. Green, J.C., Course, P.A., and Tarran, G.A. (1996) The life-cycle of Emiliania huxleyi: a brief review and a study of relative ploidy levels analysed by flow cytometry. J Mar Syst 9: 33-44.
22. Hagino, K., Bendif, E.M., Young, J., Kogame, K., Takano, Y., Probert, I., etal. (2011) New evidence for morphological and genetic variation in the cosmopolitan coccolithophore Emiliana huxleyi (Prymnesiophyceae) from the cox1b-ATP4 genes. J Phycol 47: 1164-1176.
23. Hayashi, M., Ohkuni, K., and Yamashita, I. (1998) An extracellular meiosis-promoting factor in Saccharomyces cerevisiae. Yeast 14: 617-622.
24. Holligan, P.M., Violler, M., Harbour, D.S., Camus, P., and Champagne-Philippe, M. (1983) Satellite and ship studies of coccolithophore production along a continental shelf edge. Nature 304: 339-342.
25. Houdan, A., Billard, C., Marie, D., Not, F., Saez, A., Young, G., and Probert, I. (2004) Holococcolithophores-heterococcolithophores (Haptophyta) life cycles: flow cytometry analysis of relative ploidy levels. System Biodivers 1: 453-465.
26. Houdan, A., Probert, I., Van Lenning, K., and Lefebvre, C. (2005) Comparison of photosynthetic responses in diploid and haploid life-cycle phases of Emiliania huxleyi (Prymnesiophyceae). Mar Ecol Prog Ser 292: 139-146.
27. Houdan, A., Probert, I., Zatylny, C., Véron, B., and Billard, C. (2006) Ecology of oceanic coccolithophores. I. nutritional preferences of the two stages in the life cycle of Coccolithus braarudii and Calcidiscus leptoporus. Aquat Microb Ecol 44: 291-301.
28. Iglesias-Rodriguez, M.D., Schofield, O.M., Batley, J., Medlin, L.K., and Hayes, P.K. (2006) Intraspecific genetic diversity in the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae): the use of microsatellite analysis in marine phytoplankton population studies. J Phycol 42: 526-536.
29. Jacquet, S., Heldal, M., Iglesias-Rodriguez, D., Larsen, A., Wilson, W., and Bratbak, G. (2001) Flow cytometric analysis of an Emiliana huxleyi bloom terminated by viral infection. Aquat Microb Ecol 27: 111-124.
30. Klaveness, D. (1972) Coccolithus huxleyi (Lohm.) Kamptn. II. The flagellate cell. aberrant cell types, vegetative propagation and life cycles. Br Phycol J 7: 309-318.
31. Laguna, R., Romo, J., Read, B.A., and Wahlund, T.M. (2001) Induction of phase variation events in the life cycle of the marine coccolithophorid Emiliania huxleyi. Appl Environ Microbiol 67: 3824-3831.
32. Leadbeater, B.S.C. (1971) Observations on the life history of the haptophyceaen alga Pleurochrysis scherffellii with special reference to the microanatomy of the different types of motile cells. Ann Bot 35: 429-439.
33. Liu, H., Aris-Brosou, S., Probert, I., and de Vargas, C. (2010) A timeline of the environmental genetics of the haptophytes. Mol Biol Evol 27: 171-176.
34. Lohmann, H. (1902) Die Coccolithophoridae, eine Monographie der Coccolithen bildenden flagellaten, zugleich ein beitrag zur kenntnis des mittelmeerauftriebs. Archiv für Protistenkunde 1: 89-165.
35. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., etal. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
36. Lüning, K., and Kadel, P. (1993) Daylength range for circannual rhythmicity in Pterygophora californica (Alariaceae, Phaeophyta) and synchronization of seasonal growth by daylength cycles in several other brown algae. Phycologia 32: 379-387.
37. Mable, B.K., and Otto, S.P. (1998) The evolution of life cycles with haploid and diploid phases. Bioessays 20: 453-462.
38. McIntyre, A., and Bé, A.W. (1967) Modern coccolithophoridae of the Atlantic Ocean. I. Placoliths and cyrtoliths. Deep Sea Res 4: 561-597.
39. Malin, G., and Steinke, M. (2004) Dimethyl sulfide production: what is the contribution of the coccolithophores? Coccolithophores: From the Molecular Processes to Global Impact. Thierstein, H.R., and Young, J.R. (eds). New York, USA: Springer Verlag, pp. 127-164.
40. Martinez-Martinez, J., Schroeder, D., Larsen, A., Bratbak, G., and Wilson, W. (2007) Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl Environ Microbiol 73: 554-562.
41. Medlin, L.K., Elwood, H.J., Stickel, S., and Sogin, M.L. (1988) The enzymatic characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71: 491-499.
42. Montresor, M., and Lewis, J. (2006) Phases, stages, and shifts in the life cycles of marine phytoplankton. In Algal Cultures, Analogues of Blooms and Applications. Subba Rao, D. (ed.). Enfield, USA: Science Publishers, pp. 91-129.
43. Nedelcu, A.M. (2005) Sex as a response to oxidative stress: stress genes co-opted for sex. Proc R Soc Lond B Biol Sci 272: 1935-1940.
44. Nedelcu, A.M., Marcu, O., and Michod, R.E. (2004) Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. Proc R Soc Lond B Biol Sci 271: 1591-1596.
45. Noël, M.-H., Kawachi, M., and Inouye, I. (2004) Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J Phycol 40: 112-129.
46. Not, F., Simon, N., Biegala, I., and Vaulot, D. (2002) Application of fluorescent in situ hybridization coupled with tyramide signal amplification (FISH-TSA) to assess eukaryotic picoplankton composition. Aquat Microb Ecol 28: 157-166.
47. Okada, H., and McIntyre, A. (1977) Modern coccolithophores of the Pacific and North Atlantic Oceans. Micropaleontology 23: 1-55.
48. Paasche, E. (2001) A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification photosynthesis interactions. Phycologia 40: 503-529.
49. Pagarete, A., Allen, M.J., Wilson, W.H., Kimmance, S.A., and de Vargas, C. (2009) Host-virus shift of the sphingolipid pathway along an Emiliania huxleyi bloom: survival of the fattest. Environ Microbiol 11: 2840-2848.
50. Pagarete, A., Le Corguillé, G., Tiwari, B., Ogata, H., de Vargas, C., Wilson, W.H., and Allen, A.E. (2011) Unveiling the transcriptional features associated with coccolithvirus infection of natural Emiliania huxleyi blooms. FEMS Microbiol Ecol 78: 555-564.
51. Rhodes, L.L., Peake, B.M., MacKenzie, A.L., and Marwick, S. (1995) Coccolithophores Gephyrocapsa oceanica and Emiliania huxleyi (Prymnesiophyceae=Haptophyceae) in New Zealand's coastal waters: Characteristics of blooms and growth in laboratory culture. NZ J Mar Freshwater Res 29: 345-357.
52. 2 perturbation studies: from organism to community level. Biogeosciences 5: 1157-1164.
53. Rokitta, S.D., de Nooijer, L.J., Trimborn, S., de Vargas, C., Rost, B., and John, U. (2011) Transcriptome analyses reveal differential gene expression patterns between the life-cycle stages of Emiliania huxleyi (Haptophyta) and reflect specialization to different ecological niches. J Phycol 47: 829-838.
54. Rost, B., and Riebesell, U. (2004) Coccolithophores calcification and the biological pump: reponse to environmental changes. In Coccolithophores: From the Molecular Processes to Global Impact. Thierstein, H.R., and Young, J.R. (eds). New York, USA: Springer Verlag, pp. 99-125.
55. Shapiro, L.P., Campbell, L., and Haugen, E.M. (1989) Immunochemical recognition of phytoplankton species. Mar Ecol Prog Ser 57: 219-224.
56. Tyrrell, T., and Merico, A. (2004) Emiliania huxleyi: bloom observation and the conditions that induce them. In Coccolithophores: From the Molecular Processes to Global Impact. Thierstein, H.R., and Young, J.R. (eds). New York, USA: Springer Verlag, pp. 75-97.
57. Valero, M., Richerd, S., and Perrot, V. (1992) Evolution of alternation of haploid and diploid phases in life cycles. Trends Ecol Evol 7: 25-29.
58. 2 limitation and oxidative stress. Curr Biol 9: 1061-1064.
59. Vardi, A., Van Mooy, B.A.S., Fredricks, H.F., Popendorf, K.J., Ossolinski, J.E., Haramaty, L., and Bidle, K.D. (2009) Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 329: 861-865.
60. Westbroek, P., Brown, C.W., Van Bleijswijk, J., Brownlee, C., Brummer, G.J., Cote, M., etal. (1993) A model system approach to biological climate forcing: the example of Emiliania huxleyi. Glob Planet Change 8: 27-46.
61. Winter, A., Jordan, R.W., and Roth, P.H. (1994) Biogeography of Living Coccolithophores in Ocean Waters. Cambridge, UK: Cambridge University Press.
62. Young, J., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I., and Østergaard, J. (2003) A guide to extant coccolithophore taxonomy. J Nannoplankton Res Spec Issue 1: 125 pp.
63. Ziveri, P., Baumann, K.-H., Böckel, B., Bollmann, J., and Young, J.R. (2004) Biogeography of selected holocene coccoliths in the Atlantic Ocean. In Coccolithophores - From Molecular Processes to Global Impact. Thierstein, H.R., and Young, J.R. (eds). Berlin, Germany: Springer, pp. 403-428.