Coccolithophores lipid and carbon isotope composition and their variability related to changes in seawater carbonate chemistry

Journal of Experimental Marine Biology and Ecology

Volumn 394, Issue 1-2, 2010, Pages 74-85

  Fiorini, Sarah ^a,b,c   Gattuso, Jean Pierre ^a,b   van Rijswijk, Pieter ^c   Middelburg, Jack ^c,d  

^a LABORATOIRE D OCÉANOGRAPHIE DE VILLEFRANCHE   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

Author keywords

13C; 13C discrimination; CO2 partial pressure; Coccolithophores; Phospholipids derived fatty acids; PLFA

Indexed keywords

ALGA; CARBON DIOXIDE; CARBON ISOTOPE; CARBONATE; FATTY ACID; GROWTH RATE; ISOTOPIC COMPOSITION; NITROGEN; ORGANIC ACID; ORGANIC CARBON; PHOSPHOLIPID; PHYTOPLANKTON; SEAWATER; WATER CHEMISTRY;

CALCIDISCUS LEPTOPORUS; EMILIANIA HUXLEYI; HAPTOPHYCEAE; SYRACOSPHAERA PULCHRA;

EID: 77956744757     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2010.07.020     Document Type: Article

References (88)

1. Albentosa M., Pérez-Camacho A., Labarta U., Beiras R., Fernandez-Reiriz M.J. Nutritional value of algal diets to clam spat Venerupis pullastra. Mar. Ecol. Prog. Ser. 1993, 97(3):261-269.
2. Alonso D.L., Delcastillo C.I.S., Sanchez J.L.G., Perez J.A.S. Quantitative genetics of fatty acids variation in Isochrysis galbana (Prymnesiophyceae) and Phaeodactylum tricornutum (Bacillarophyceae). J. Phycol. 1994, 30(3):553-558.
3. Anderson O.R., Spindler M., Bé A.W.H., Hemblen C.H. Trophic activity of planktonic foraminifera. J. Mar. Biol. Assoc. UK 1979, 59(3):791-799.
4. Bell M.V., Pond D. Lipid composition during growth of motile and coccolith forms of Emiliania huxleyi. Phytochemistry 1996, 41(2):465-471.
5. Ben-Amotz A., Tornabene T.G., Thomas W.H. Chemical profile of selected species of microalgae with emphasis on lipids. J. Phycol. 1985, 21(1):72-81.
6. Bendle J., Rosell-Mele A., Ziveri P. Variability of unusual distributions of alkenones in the surface waters of the Nordic seas. Paleoceanography 2005, 20(2):PA2001.
7. 2 concentration and primary production. Geochim. Cosmochim. Acta 2007, 71(6):1528-1541.
8. Bidigare R.R., Fluegge A., Freeman K.H., Hanson K.L., Hayes J.M., Hollander D., Jasper J.P., King L.L., Laws E.A., Milder J., Millero F.J., Pancost R., Popp B.N., Steinberg P.A., Wakeham S.G. Consistent fractionation of C-13 in nature and in the laboratory: growth-rate effects in some haptophyte algae. Glob. Biogeochem. Cycles 1997, 11(2):279-292.
9. Billard C., Inouye I. What is new in coccolithophores biology?. Coccolithophores from Molecular Processes to Global Impact 2004, 1-29. Springer. H.R. Thierstein, J. Young (Eds.).
10. Bligh E.G., Dyer W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 1959, 37(8):911-917.
11. Boschker H.T.S., de Brouwer J.F.C., Cappenberg T.E. The contribution of macrophyte-derived organic matter to microbial biomass in salt-marsh sediments: stable carbon isotope analysis of microbial biomarkers. Limnol. Oceanogr. 1999, 44(2):309-319.
12. Boschker H.T.S., Kromkamp J.C., Middelburg J.J. Biomarker and carbon isotopic constraints on bacterial and algal community structure and functioning in a turbid, tidal estuary. Limnol. Oceanogr. 2005, 50(1):70-80.
13. Brassell S.C., Eglinton G., Marlowe I.T., Pflaumann U., Sarnthein M. Molecular stratigraphy: a new tool for climatic assessment. Nature 1986, 320(6058):129-133.
14. Brown C.W., Yoder J.A. Coccolithophorid blooms in the global ocean. J. Geophys. Res. 1994, 99(C4):7467-7482.
15. Budge S.M., Cooper M.H., Iverson S.J. Demonstration of the deposition and modification of dietary fatty acids in pinniped blubber using radiolabelled precursors. Physiol. Biochem. Zool. 2004, 77(4):682-687.
16. Buitenhuis E.T., Pangerc T., Franklin D.J., Le Quéré C., Malin G. Growth rates of six coccolithophorid strains as a function of temperature. Limnol. Oceanogr. 2008, 53(3):1181-1185.
17. 2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoplankton. Geochim. Cosmochim. Acta 1999, 63(22):3729-3741.
18. Caldeira K., Wickett M.E. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J. Geophys. Res. 2005, 110(C9):C09S04.
19. Chu F.L.E., Dupuy J.L., Webb K.L. Polysaccharide composition of 5 algal species used as food for larvae of the American oyster, Crassostrea virginica. Aquaculture 1982, 29(3-4):241-252.
20. Conte M.H., Thompson A., Eglinton G. Primary production of lipid biomarker compounds by Emiliania huxleyi: results from an experimental mesocosm study in fjords of southwestern Norway. Sarsia 1994, 79(4):319-331.
21. 13C measurements. Anal. Chem. 2006, 78(7):2439-2441.
22. 2 levels: a stable isotope labelling study. Biogeosci. Discuss. 2010, 7:3257-3295.
23. 2 Measurements 2007, PICES Special Publication.
24. Dijkman N.A., Kromkamp J.C. Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition. Mar. Ecol. Prog. Ser. 2006, 324:113-125.
25. Falk-Petersen S., Sargent J.R., Henderson J., Hegseth E.N., Hop H., Okolodkov Y.B. Lipids and fatty acids in ice algae and phytoplankton from the Marginal ice zone in the Barents Sea. Polar Biol. 1998, 20(1):41-47.
26. Fiorini S. "Effet de l'augmentation de la pression partielle du dioxyde de carbone et de la température sur le phytoplancton calcifiant (coccolithophoridés).". Ph.D. dissertation 2010, University of Paris VI, France.
27. Geider R.J., La Roche J. Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol. 2002, 37(1):1-17.
28. 2 and nitrogen supply on lipid class composition of Dunaliella viridis. J. Appl. Phycol. 1998, 10(2):135-144.
29. 2 and nitrogen supply on the biochemical composition of Ulva rigida with special emphasis on lipid class analysis. J. Plant Physiol. 2001, 158(3):367-373.
30. Harris R.P. Zooplankton grazing on the coccolithophore Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol. 1994, 119(3):431-439.
31. Holligan P.M., Fernandez E., Aiken J., Balch W.M., Boyd P., Burkill P.H., Finch M., Groom S.B., Malin G., Muller K., Purdie D.A., Robinson C., Trees C.C., Sm Turner, Vanderwal P. A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic. Glob. Biogeochem. Cycles 1993, 7(4):879-900.
32. Houdan A., Billard C., Marie D., Not F., Sàez A.G., Young J.R., Probert I. Holococcolithophore-heterococcolithophore (Haptophyta) life cycles: flow cytometry analysis of relative ploidy levels. Syst. Biodivers. 2004, 1:453-465.
33. Houdan A., Probert I., Zatylny C., Véron B., Billard C. Ecology of oceanic coccolithophores. Nutritional preferences of the two stages in the life cycles of Coccolithus brarudii and Calcidiscus leptoporus. Aquat. Microb. Ecol. 2006, 44(3):291-30.
34. Iglesias-Rodriguez M.D., Brown C.W., Doney S.C., Kleypas J., Kolber D., Kolber Z., Hayes P.K., Falkowski P. Representing key phytoplankton functional groups in ocean carbon cycle models: coccolithophorids. Glob. Biogeochem. Cycles 2002, 16(4):1100.
35. Iglesias-Rodriguez M.D., Schofield O.M., Batley J., Medlin L.K., Hayes P.K. Intraspecific genetic diversity in the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae): the use of the microsatellite analysis in marine phytoplankton population studies. J. Phycol. 2006, 42(3):526-536.
36. 2 world. Science 2008, 320(5874):336-340.
37. 13C discrimination by two marine phytoplankton. Mar. Ecol. Prog. Ser. 1996, 132(1-3):257-263.
38. Kanazawa A., Teshima S., Ono K. Relationship between essential fatty acid requirements of aquatic animals and their capacity for bioconversion of linoleic acid to highly unsaturated fatty acids. Comp. Biochem. Physiol. 1979, 63(3):295-298.
39. Keller M.D., Selvin R.C., Claus W., Guillard R.R.L. Media for the culture of oceanic ultraphytoplankton. J. Phycol. 1987, 23(4):633-638.
40. Langer G., Geisen M., Baumann K.-H., Klaas J., Riebesell U., Thoms S., Young J.R. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem. Geophys. Geosyst. 2006, 7:Q09006.
41. Langer G., Nehrke G., Probert I., Ly J., Ziveri P. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 2009, 6(11):2637-2646.
42. Lavigne H., Proye A., Gattuso J.-P. seacarb: calculates parameters of the seawater carbonate system http://www.obs-vlfr.fr/~gattuso/seacarb.php.
43. 2 concentration on carbon isotopic fractionation by the marine diatom Phaeodactylum tricornutum. Limnol. Oceanogr. 1997, 42(7):1552-1560.
44. Lecourt M., Muggli D.L., Harrison P.J. Comparison of growth and sinking rates of non-coccolith and coccolith-forming strains of Emiliania huxleyi (Prymnesiophyceae) grown under different irradiances and nitrogen sources. J. Phycol. 1996, 32(1):17-21.
45. Lombardi A.T., Wangersky P.J. Particulate lipid class composition of three marina phytoplanktoners Chaetoceros gracilis, Isochrysis galbana (Tahiti) and Dunaliella tertiolecta grown in batch culture. Hydrobiologia 1995, 306(1):1-6.
46. Malin G., Kirst G.O. Algal production of dimethyl sulfide and its atmospheric role. J. Phycol. 1997, 33(6):889-896.
47. Malinverno E., Prahl F.G., Popp B.N., Ziveri P. Alkenone abundance and its relationship to the coccolithophore assemblage in Gulf of California surface waters. Deep-Sea Res. I 2008, 55(9):1118-1130.
48. Marlowe I.T., Green J.C., Neal A.C., Brassell S.C., Eglinton G., Course P.A. Long chain (n-C37-C39) alkenones in the Prymnesiophyceae. Distribution of alkenones and other lipids and their taxonomic significance. Br. Phycol. J. 1984, 19(3):203-216.
49. Mayzaud P., Laureillard J., Merien D., Brinis A., Godard C., Razouls S., Labat J.-P. Zooplankton nutrition, storage and fecal lipid composition in different water masses associated with the Agulhas and Subtropical fronts. Mar. Chem. 2007, 107(2):202-213.
50. 13C-labeling study. Limnol. Oceanogr. 2000, 45(6):1224-1234.
51. Miyajima T., Yamada Y., Hanba Y.T., Yoshii K., Koitabashi T., Wada E. Determining the stable-isotope ratio of total dissolved inorganic carbon in lake water by GC/C/IRMS. Limnol. Oceanogr. 1995, 40(5):994-1000.
52. Montagnes D.J.S., Berges J.A., Harrison P.J., Taylor F.J.R. Estimating carbon, nitrogen, protein, and chlorophyll a from volume in marine phytoplankton. Limnol. Oceanogr. 1994, 39(5):1044-1060.
53. Mook W.G., Bommerson J.C., Staverman W.H. Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Planet. Sci. Lett. 1974, 22(2):169-176.
54. Morales-Loo M.R., Goutx M. Effects of water-soluble fraction of the Mexican crude oil «Isthmus Cactus» on growth, cellular content of chlorophyll a, and lipid composition of planktonic microalgae. Mar. Biol. 1990, 104(3):503-509.
55. Napolitano G.E., Pollero R., Gayoso A.M., Macdonald B.A., Thomps R. Fatty acids as trophic markers of phytoplankton blooms in the Bahia Blanca estuary (Buenos Aires, Argentina) and in Trinity Bay (Newfoundland, Canada). Biochem. Syst. Ecol. 1997, 25(80):739-755.
56. Neal A.C., Prahl F.G., Englinton G. Lipid changes during a planktonic feeding sequence involving unicellular algae. Elminius nauplii and adult Calanus. J. Mar. Biol. Assoc. UK 1986, 66(1):1-13.
57. Nieuwenhuize J., Maas Y.E.M., Middelburg J.J. Rapid analysis of organic carbon and nitrogen in particulate materials. Mar. Chem. 1994, 45(3):217-224.
58. Okuyama H., Morita N., Kogome K. Occurence of octadecapentaenoic acid in lipids of a cold stenothermic alga, prymnesiophyte strain-B. J. Phycol. 1992, 28(4):465-472.
59. Parrish C.C., Bodennec G., Gentien P. Time courses of intracellular and extracellular lipid classes in batch cultures of the toxic dinoflagellate, Gymnodium cf. nagasakiense. Mar. Chem. 1994, 48(1):71-82.
60. Peeler T.C., Thompson G.A. Effects of light on phospholipid metabolism in Dunaliella salina. Physiol. Plant. 1990, 78(3):324-330.
61. Pohl P., Zurheide F. Fatty acids and lipids of marine algae and the control of their biosynthesis by environmental factors. Marine Algae in Pharmaceutical Science 1979, 473-523. Gruyter, Berlin. H.A. Hoppe, T. Levring, Y. Tanaka (Eds.).
62. Pond D.W., Harris R.P. The lipid composition of the coccolithophore Emiliania huxleyi and its possible ecophysiological significance. J. Mar. Biol. Assoc. UK 1996, 76(3):579-594.
63. Popp B.N., Kenig F., Wakeham S.G., Laws E.A., Bidigare R.R. Does growth rate affect ketone unsaturation and intracellular carbon isotopic variability in Emiliania huxleyi?. Paleoceanography 1998, 13(1):35-41.
64. 2-concentrating mechanism. Russ. J. Plant Physiol. 1998, 45(4):447-455.
65. 2 and productivity in past oceans. Nature 1989, 341(6242):516-518.
66. 2 uptake. Mar. Ecol. Prog. Ser. 1996, 133(1-3):275-285.
67. Reuss N., Poulsen L.K. Evaluation of fatty acids as biomarkers for a natural plankton community. A field study of a spring bloom and a post-bloom period off West Greenland. Mar. Biol. 2002, 141(3):423-434.
68. Riebesell U., Wolf-Gladrow D., Smetacek V. Carbon dioxide limitation of marine phytoplankton growth rates. Nature 1993, 361(6409):249-251.
69. 2. Nature 2000, 407(6802):364-367.
70. 2 concentration on lipid composition and carbon isotope fractionation in Emiliania huxleyi. Geochim. Cosmochim. Acta 2000, 64(24):4179-4192.
71. Rost B., Zondervan I., Riebesell U. Light-dependent carbon isotope fractionation in the coccolithophorid Emiliania huxleyi. Limnol. Oceanogr. 2002, 47(1):120-128.
72. Saliot A., Laurelliard J., Scribe P., Sicre M.A. Evolutionary trends in the lipid biomarker approach for investigating the biogeochemistry of organic matter in marine environment. Mar. Chem. 1991, 36(1-4):233-248.
73. Saoudi-Helis L., Dubacq J.P., Marty Y., Samadin J.F., Gudin C. Influence of growth rate on pigment and lipid composition of the microalga Isochrysis Aff Galbana clone T-Iso. J. Appl. Phycol. 1994, 6(3):315-322.
74. Sargent J.H. The structure, metabolism and function of lipids in marine organisms. Biochemical and Biophysical Perspectives in Marine Biology 1976, 149-212. Academic Press, New York. D. Malins, J.R. Sargent (Eds.).
75. Solomon S., Qin D., Manning M., Chen Z., Marquis M., Averyt K.B., Tignor M., Miller H.L. Climate Change 2007: the Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change 2007, Cambridge University Press, Cambridge. U.K.
76. Sukenik A., Whanon R. Biochemical quality of marine unicellular algae with special emphasis on lipid composition. 1. Isochrysis galbana. Aquaculture 1991, 97(1):61-72.
77. Thompson P.A., Clavert S.E. Carbon isotope fractionation by a marine diatom. The influence of irradiance, daylength, pH, and nitrogen source. Limnol. Oceanogr. 1994, 39(8):1835-1844.
78. Tolosa I., Vescovali I., LeBlond N., Marty J.-C., de Mora S., Prieur L. Distribution of pigments and fatty acid biomarkers in particulate organic matter from frontal structure of the Alboran Sea (SW Mediterranean Sea). Mar. Chem. 2004, 88(3-4):103-125.
79. van Bleijswijk J.D.L., Kempers R.S., Veldhuis M.J., Westbroek P. Cell and growth characteristics of Type A and Type B of Emiliania huxleyi (Prymnesiophyceae) as determined by flow cytometry and chemical analyses. J. Phycol. 1994, 30(2):230-241.
80. 13C tracer experiment. Limnol. Oceanogr. 2004, 49(3):862-878.
81. Viso A.C., Marty J.C. Fatty acids from 28 marine microalgae. Phytochemistry 1993, 34(6):1521-1533.
82. Volkman J.K., Eglinton G., Corner E.D.S., Forsberg T.E.V. Long chain alkenes and alkenones in the marine coccolithophorid Emiliania huxleyi. Phytochemistry 1980, 19(12):2619-2622.
83. Volkman J.K., Jeffrey S.W., Nichols P.D., Rogers G.I., Garland C.D. Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J. Exp. Mar. Biol. Ecol. 1989, 128(3):219-240.
84. Werner R.A., Brand W.A. Referencing strategies and techniques in stable isotope ratio analysis. Rapid Commun. Mass Spectrom. 2001, 15(7):501-519.
85. Westbroek P., Brown C.W., Vanbleijswijk J., Brownlee C., Brummer G.J., Conte M., Egge J., Fernandez E., Jordan R., Knappertsbusch M., Stefels J., Veldhuis M., Vanderwal P., Young J. A model system approach to biological climate forcing. The example of Emiliania huxleyi. Global Planet. Change 1993, 8(1-2):27-46.
86. Ziveri P., Thunell R.C. Coccolithophore export production in Guaymas Basin, Gulf of California: response to climate forcing. Deep-Sea Res. II 2000, 47(9-11):2073-2100.
87. Ziveri P., De Bernardi B., Bauman K.-H., Stoll H.M., Mortyn P.G. Sinking of coccolith carbonate and potential contribution to organic carbon ballasting in the deep ocean. Deep-Sea Res. II 2007, 54(5-7):659-675.
88. 2 concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limiting conditions and different daylengths. J. Exp. Mar. Biol. Ecol. 2002, 272(1):55-70.