New evidence for morphological and genetic variation in the cosmopolitan coccolithophore emiliania huxleyi (prymnesiophyceae) from the cox1b-atp4 genes

Journal of Phycology

Volumn 47, Issue 5, 2011, Pages 1164-1176

  Hagino, Kyoko ^a,e   Bendif, El Mahdi ^b   Young, Jeremy R ^c,f   Kogame, Kazuhiro ^a   Probert, Ian ^b   Takano, Yoshihito ^d   Horiguchi, Takeo ^a   de Vargas, Colomban ^b   Okada, Hisatake ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^d NAGASAKI UNIVERSITY   (Japan)

^e OKAYAMA UNIVERSITY   (Japan)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Biogeography; Coccolithophore; Emiliania huxleyi; Mitochondrial DNA; Morphotype

Indexed keywords

EMILIANIA HUXLEYI; HAPTOPHYCEAE;

EID: 80053571861     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2011.01053.x     Document Type: Article

References (51)

1. Antonov, J., Locarnini, I. R. A., Boyer, T. P., Mishonov, A. V. & Garcia, H. E. 2006. World Ocean Atlas 2005, Volume 2: Salinity. In Levitus, S. [Ed.] NOAA Atlas NESDIS 62. U.S. Government Printing Office, Washington, D.C., 182 pp.
2. Boeckel, B. & Baumann, K.-H. 2008. Vertical and lateral variations in coccolithophore community structure across the subtropical frontal zone in the South Atlantic Ocean. Mar. Micropaleontol. 67:255-73.
3. Corstjens, P. L. A. M., van der Kooij, A., Linschooten, C., Brouwers, G.-J., Westbroek, P. & de Vrind-de Jong, E. W. 1998. GPA, a calcium-binding protein in the coccolithophorid Emiliania huxleyi (Prymnesiophyceae). J. Phycol. 34:622-30.
4. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-91.
5. Findlay, C. S. & Giraudeau, J. 2000. Extant calcareous nannoplankton in the Australian Sector of the Southern Ocean (austral summers 1994 and 1995). Mar. Micropaleontol. 40:417-39.
6. Fujiwara, S., Tsuzuki, M., Kawachi, M., Minaka, N. & Inouye, I. 2001. Molecular phylogeny of the Haptophyta based on the rbcL gene and sequence variation in the spacer region of the RUBISCO operon. J. Phycol. 37:121-9.
7. Garcia, H. E., Locarnini, R. A., Boyer, T. P. & Antonov, J. I. 2006a. World Ocean Atlas 2005, Volume 3: Dissolved Oxygen, Apparent Oxygen Utilization, and Oxygen Saturation. In Levitus, S. [Ed.] NOAA Atlas NESDIS 63. U.S. Government Printing Office, Washington, D.C., 342 pp.
8. Garcia, H. E., Locarnini, R. A., Boyer, T. P. & Antonov, J. I. 2006b. World Ocean Atlas 2005, Volume 4: Nutrients (phosphate, nitrate, silicate). In Levitus, S. [Ed.] NOAA Atlas NESDIS 64. U.S. Government Printing Office, Washington, D.C., 396 pp.
9. Gard, G. 1986. Calcareous nannofossil biostratigraphy of Late Quaternary Arctic sediments. Boreas 15:217-29.
10. Gard, G. 1989. Variations in coccolith assemblages during the last glacial cycle in the high and mid-latitude Atlantic and Indian Oceans. In Crux, J. A. & van Heck, S. E. [Eds.] Nannofossils and Their Applications. Ellis Horwood, Chichester, UK, pp. 108-21.
11. Hagino, K. & Okada, H. 2006. Intra- and infra-specific morphological variation in selected coccolithophore species in the equatorial and subequatorial Pacific Ocean. Mar. Micropaleontol. 58:184-206.
12. Hagino, K., Okada, H. & Matsuoka, H. 2000. Spatial dynamics of coccolithophore assemblages in the equatorial western-central Pacific Ocean. Mar. Micropaleontol. 39:53-72.
13. Hagino, K., Okada, H. & Matsuoka, H. 2005. Coccolithophore assemblages and morphotypes of Emiliania huxleyi in the boundary zone between the cold Oyashio and warm Kuroshio currents off the coast of Japan. Mar. Micropaleontol. 55:19-47.
14. Hine, N. & Weaver, P. P. E. 1998. Quaternary. In Bown, P. [Ed.] Calcareous Nannofossil Biostratigraphy. Chapman & Hall, Cambridge, pp. 266-83.
15. Hiramatsu, C. & De Deckker, P. 1996. Distribution of calcareous nannoplankton near the subtropical convergence, south of Tasmania, Australia. Mar. Freshw. Res. 47:707-13.
16. Iglesias-Rodríguez, M. D., Sáez, A., Groben, R., Edwards, K. J., Batley, J., Medlin, L. & Hayes, P. K. 2002. Polymorphic microsatellite loci in global populations of the marine coccolithophorid Emiliania huxleyi. Mol. Ecol. Notes 2:495-7.
17. Iglesias-Rodríguez, M. D., Schfield, O. M., Batley, J., Medlin, L. K. & 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. 42:526-36.
18. Jordan, R. W., Zhao, M., Eglinton, G. & Weaver, P. P. E. 1996. Coccolith and alkenone stratigraphy and palaeoceanography at an upwelling site off NW Africa (ODP 658C) during the last 130, 000years. In Moguilevsky, A. & Whatley, R. [Eds.] Microfossils and Oceanic Environments. University of Wales, Aberystwyth - Press, Aberystwyth, UK, pp. 111-30.
19. Kimura, M. 1980. A simple method for estimating rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:111-20.
20. Locarnini, R. A., Mishonov, A. V., Antonov, J. I., Boyer, T. P. & Garcia, H. E. 2006. World Ocean Atlas 2005, Volume 1: Temperature. In Levitus, S. [Ed.] NOAA Atlas NESDIS 61, U.S. Government Printing Office, Washington, D.C., 182 pp.
21. Martínez-Martínez, J., Schroeder, D. C., Larsen, A., Bratbak, G. & Wilson, W. H. 2007. Molecular dynamics of Emiliania huxleyi and cooccurring viruses during two separate mesocosm studies. Appl. Environ. Microbiol. 73:554-62.
22. McIntyre, A. & Bé, A. 1967. Modern Coccolithophoridae of the Atlantic Ocean-I. Placoliths and cyrtoliths. Deep-Sea Res. 14:561-97.
23. Medlin, L. K., Barker, G. L. A., Campbell, L., Green, J. C., Hayes, P. K., Marie, D., Wrieden, S. & Vaulot, D. 1996. Genetic characterization of Emiliania huxleyi (Haptophyta). J. Mar. Syst. 9:13-31.
24. Noël, M.-H., Kawachi, M. & Inouye, I. 2004. Induced dimorphic life cycle of a coccolithophorid, Calyptrosphaera sphaeroidea (Prymnesiophyceae, Haptophyta). J. Phycol. 40:112-29.
25. Okada, H. & Honjo, S. 1973. The distribution of oceanic coccolithophorids in the Pacific. Deep-Sea Res. 20:355-74.
26. Okada, H. & McIntyre, A. 1977. Modern coccolithophores of the Pacific and North Atlantic Oceans. Micropaleontology 23:1-55.
27. Posada, M. A. & Crandall, K. A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-8.
28. Raffi, I., Backman, J., Fornaciari, E., Pälike, H., Rio, D., Lourens, L. & Hilgen, F. 2006. A review of calcareous nannofossil astrobiochronology encompassing the past 25 million years. Quat. Sci. Rev. 25:3113-37.
29. Reid, P. C., Johns, D. G., Edwards, M., Starr, M., Poulin, M. & Snoeijs, P. 2007. A biological consequence of reducing Arctic ice cover: arrival of the Pacific diatom Neodenticula seminae in the North Atlantic for the first time in 800, 000years. Glob. Change Biol. 13:1910-21.
30. Ripley, S. J., Baker, A. C., Miller, P. I., Walne, A. W. & Schroeder, D. C. 2008. Development and validation of a molecular technique for the analysis of archived formalin-preserved phytoplankton samples permits retrospective assessment of Emiliania huxleyi communities. J. Microbiol. Methods 73:118-24.
31. Ronquist, F. & Huelsenbeck, J. P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-4.
32. Rost, B. & Riebesell, U. 2004. Coccolithophores and the biological pump: responses to environmental changes. In Thierstein, H. R. & Young, J. R. [Eds.] Coccolithophores From Molecular Processes to Global Impact. Springer-Verlag, Berlin Heidelberg, Germany, pp. 99-125.
33. Saitou, N. & Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-25.
34. Sambrook, J., Fritsch, E. F. & Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, New York, 1659 pp.
35. Sánchez Puerta, V., Bachvaroff, T. R. & Delwiche, C. F. 2004. The complete mitochondrial genome sequence of the haptophyte Emiliania huxleyi and its relation to heterokonts. DNA Res. 11:1-10.
36. Sato, T., Saito, T., Yuguchi, S., Nakagawa, H., Kameo, K. & Takayama, T. 2002. Late Pliocene calcareous nannofossil palaeobiogeography of the Pacific Ocean: evidence for glaciation at 2.75Ma. Rev. Mexicana Cienc. Geol. 19:175-89.
37. Schroeder, D. C., Biggi, G. F., Hall, M., Davy, J., Martínez-Martínez, J., Richardson, A. J., Malin, G. & Wilson, W. H. 2005. Note: a genetic marker to separate Emiliania huxleyi (Prymnesiophyceae) morphotypes. J. Phycol. 41:874-9.
38. Schwaninger, H. R. 2008. Global mitochondrial DNA phylogeography and biogeographic history of the antitropically and longitudinally disjunct marine bryozoan Membranipora membranacea L. (Cheilostomata): another cryptic marine sibling species complex? Mol. Phylogenet. Evol. 49:893-908.
39. Swofford, D. L. 2002. PAUP*-Phylogenetic Analysis Using Parsimony (* and Other Methods), Version 4. Sinauer Associates, Sunderland, Massachusetts.
40. Tanimoto, M., Aizawa, C. & Jordan, R. W. 2003. Assemblages of living microplankton from the subarctic North Pacific and Bering Sea during July-August 1999. Cour. Forschungsinst. Senckenb. 244:83-103.
41. Thierstein, H. R., Geitzenauer, K. R. & Molfino, B. 1977. Global synchroneity of Late Quaternary coccolith datum levels: validation by oxygen isotope. Geology 5:400-4.
42. Tomczak, M. & Godfrey, J. S. 1994. Regional Oceanography: An Introduction. Pergamon, London, 422 pp.
43. Van Bleijswijk, J., van der Wal, P., Kempers, R., Veldhuis, M., Young, J. R., Muyzer, G., de Vrind-de Jong, E. & Westbroek, P. 1991. Distribution of two types of Emiliania huxleyi (Prymnesiophyceae) in the northeast Atlantic region as determined by immunofluorescence and coccolith morphology. J. Phycol. 27:566-70.
44. Verbeek, J. W. 1989. Recent calcareous nannoplankton in the southernmost Atlantic. Polarforschung 59:45-60.
45. Welch, B. L. 1947. The generalization of "Student's" problem when several different population variances are involved. Biometrika 34:28-35.
46. Winter, A. 1985. Distribution of living coccolithophore in the California Current system, southern California Borderland. Mar. Micropaleontol. 9:385-93.
47. Worsley, T. R. 1973. Calcareous nannofossils: Leg 19 of the Deep Sea Drilling Project. In Creager, J. S., Scholl, D. W., Boyce, R. E., Echols, R. J., Fullam, T. J., Grow, J. A., Koizumi, I., et al. [Eds.] Init. Repts. Deep Sea Drilling Project, 19. U.S. Govt. Printing Office, Washington, D.C., pp. 741-50.
48. Young, J. R. 1998. Neogene. In Bown, P. [Ed.] Calcareous Nannofossil Biostratigraphy. Champman & Hall, Cambridge, pp. 225-65.
49. Young, J. R., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I. & Ostergaard, J. 2003. A guide to extant coccolithophore taxonomy. J. Nannoplankton Res. Spec. Issue 1:1-125.
50. Young, J. R. & Westbroek, P. 1991. Genotypic variation in the coccolithophorid species Emiliania huxleyi. Mar. Micropaleontol. 18:5-23.
51. Zhu, H., Qu, F. & Zhu, L. H. 1993. Isolation of genomic DNAs from plants, fungi and bacteria using benzyl chloride. Nucleic Acids Res. 21:5279-80.