Formation and Transfer of Fatty Acids in Aquatic Microbial Food Webs: Role of Heterotrophic Protists



The term protist was first coined by Haeckel in 1866 for diverse microorganisms including bacteria (Haeckel 1866). However, in 1925 in a paper on an amoeboid parasite of Daphnia, Chatton (1925) highlighted for the first time the fundamental difference between prokaryotic and eukaryotic organisms and the term protist to be now used to describe unicellular eukaryotes, which do not differentiate into tissues (see Adl et al. 2005).


Highly Unsaturated Fatty Acid Desaturase Gene Crustacean Zooplankton Trophic Transfer Heterotrophic Flagellate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Professor Gilles Bourdier for having invited us (some years ago) to collaborate on his research project. We thank Diane Stoecker, Evelyn and Barry Sherr for having provided useful information and many answers. We are grateful to Dr. Keith Joblin (AgResearch Ltd., Hamilton N.Z.) for his help in improving the text from a linguistic perspective.


  1. Adl, M., Simpson, A., Farmer, M.A., Andersen, R.A., Anderson, O.R., Barta, J.R., Bowser, S.S., Brugerolle, G., Fensome, R.A., Fredericq, S., James, T.Y., Karpov, S., Kugrens, P., Krug, J., Lane, C., Lewis, L., Lodge, J., Lynn, D.H., Mann, D.G., McCourt, R.M., Mendoza, L., Moestrup, O., Mozley-Standridge, S., Nerad, T., Shearer, C.A., Smirnov, A., Speigel, F.W., and Taylor, M.F.J.R. 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52:399–451.PubMedCrossRefGoogle Scholar
  2. Adolf, J.E., Place, A.R., Stoecker, D.K., and Harding Jr., L.W. 2007a. Modulation of polyunsaturated fatty acids in mixotrophic Karlodinium Veneficum (Dinophyceae) and its prey, Storeatula major (Cryptophyceae). J. Phycol. 43:1259–1270.CrossRefGoogle Scholar
  3. Adolf, J.E., Bachvaroff, T.R., Krupatkina, D.N., and Place, A.R. 2007b. Karlotoxin mediates grazing of Oxyrrhis marina on Karlodinium veneficum strains. Harmful Algae 6:400–412.CrossRefGoogle Scholar
  4. Ahlgren, G., Lundstedt, L., Brett, M.T., and Forsberg, C. 1990. Lipid composition and food quality of some freshwater phytoplankton for cladoceran zooplankters. J. Plankton Res. 12:809–818.CrossRefGoogle Scholar
  5. Arndt, H., Dietrich, D., Auer, B., Cleven, E., Gräfenhan, T., Weitere, M., and Mylnikov, A. 2000. Functional diversity of heterotrophic flagellates in aquatic ecosystems, pp. 240–268. In B.S.C. Leadbeater and J.C. Green (eds.), The flagellates unity, diversity and evolution. Taylor & Francis, London.Google Scholar
  6. Arts, M.T., Ackman, R.G., and Holub, B.G. 2001. “Essential fatty acids” in aquatic ecosystems: a crucial link between diet and human health and evolution. Can. J. Fish. Aquat. Sci. 58:122–137.CrossRefGoogle Scholar
  7. Avery, S.V., Lloyd, D., and Harwood, J. 1994. Changes in membrane fatty acid composition and delta 12-desaturase activity during growth of Acanthamoeba castellanii in batch culture. J. Eukaryot. Microbiol. 41:396–401.CrossRefGoogle Scholar
  8. Avery, S.V., Lloyd, D., and Harwood, J. 1995. Temperature dependent changes in the plasma lipid order and the phagocytotic activity of the amoeba Acanthamoeba castellanii are closely correlated. Biochem. J. 312:811–816.PubMedGoogle Scholar
  9. Avery, S.V., Harwood, J., Rutter, A.J., Lloyd, D., and Harwood, J. 1996. Oxygen dependent low temperature composition and delta12 desaturase induction and alteration of fatty acid composition in Acanthamoeba castellanii in batch culture. Microbiology 142:2213–2221.CrossRefGoogle Scholar
  10. Azam, F., Fenchel, T., Field, J.G., Gray, J.S., Meyer-Reil, L.A., and Thingstad, F. 1983. The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10:257–263.CrossRefGoogle Scholar
  11. Bec, A., Desvilettes, C., Vera, A., Lemarchand, C., Fontvielle, D., and Bourdier, G. 2003a. Nutritional quality of a freshwater heterotrophic flagellate: trophic upgrading of its microalgal diet for Daphnia. Aquat. Microb. Ecol. 32:203–207.CrossRefGoogle Scholar
  12. Bec, A., Desvilettes, C., Vera, A., Fontvielle, D., and Bourdier, G. 2003b. Nutritional value of different food sources for the bennthic daphnidae Simocephalus vetulus: role of fatty acids. Arch. Hydrobiol. 156:145–163.CrossRefGoogle Scholar
  13. Bec, A., Martin-Creuzburg, D., and Von Elert, E. 2006. Trophic upgrading of autotrophic picoplankton by the heterotrophic flagellate Paraphysomonas sp. Limnol. Oceanogr. 51:1699–1707.CrossRefGoogle Scholar
  14. Behrouzian, B., Fauconnot, L., Daligault, F., Nugier-Chauvin, C., Patin, H., and Buist, P.H. 2001. Mechanism of fatty acid desaturation in the green alga Chlorella vulgaris. Eur. J. Biochem. 268:3545–3549.PubMedCrossRefGoogle Scholar
  15. Bettarel, Y., Sime-Ngando, T., Amblard, C., and Bouvy, M. 2005. Low consumption of virus-sized particles by heterotrophic nanoflagellates in two lakes of the French Massif Central. Aquat. Microb. Ecol. 39:205–209.CrossRefGoogle Scholar
  16. Bodyl, A. 2005. Do plastid-related characters support the chromalveolate hypothesis. J. Phycol. 41:712–719.CrossRefGoogle Scholar
  17. Boëchat, I.G. 2005. Biochemical composition of protists: dependence on diet and trophic mode and consequences for their nutritional quality. Ph.D. Thesis. Humboldt Universität zu Berlin, Berlin. 144 p.Google Scholar
  18. Boëchat, I.G. and Adrian, R. 2005. Biochemical composition of algivorous freshwater ciliates: you are not what you eat. FEMS Microbiol. Ecol. 53:393–400.PubMedCrossRefGoogle Scholar
  19. Boëchat, I.G., Weithoff, G., Krüger, A., Gücker, B., and Adrian, R. 2007. A biochemical explanation for the success of mixotrophy in the flagellate Ochromonas sp.. Limnol. Oceanogr. 52:1624–1632.CrossRefGoogle Scholar
  20. Bourdier, G. and Amblard, C. 1987. Evolution de la composition en acides gras du phytoplancton lacustre du (lac Pavin). Int. Revue Ges. Hydrobiol. 11:1201–1212.Google Scholar
  21. Brett, M.T. and Müller-Navarra, D.C. 1997. The role of highly unsaturated fatty acids in food web processes. Freshw Biol. 38:483–499.CrossRefGoogle Scholar
  22. Broglio, E., Jonasdottir, S.H., Calbet, A., Jakobsen, H.H., and Saiz, E. 2003. Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat. Microb. Ecol. 31:267–278.CrossRefGoogle Scholar
  23. Brugerolle, G. and Müller, M. 2000. Amitochondriate flagellates, pp. 166–189. In B.S.C. Leadbeater and J.C. Green (eds.), The flagellates. unity, diversity and evolution. Taylor & Francis, London.Google Scholar
  24. Burkholder, J.M. and Glasgow, H.B.J. 1997. Pfiesteria piscicida and other Pfiesteria-like dinoflagellates: behavior, impacts, and environmental controls. Limnol. Oceanogr. 42:1052–1075.CrossRefGoogle Scholar
  25. Calbet, A. and Landry, M.R. 2004. Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr. 49:51–57.CrossRefGoogle Scholar
  26. Callieri, C. and Stockner, J.G. 2002. Freshwater autotrophic picoplankton: a review. J. Limnol. 61:1–14.Google Scholar
  27. Caron, D.A., Goldman, J.C., and Dennett, M.R. 1990. Carbon utilization by the omnivorous flagellate Paraphysomonas imperforata. Limnol. Oceanogr. 35:192–201.CrossRefGoogle Scholar
  28. Carrias, J.-F., Quiblier-Lloberas, C., and Bourdier, G. 1998. Seasonal dynamics of free and attached heterotrophic nanoflagellates in an oligomesotrophic lake. Freshw. Biol. 39:91–101.CrossRefGoogle Scholar
  29. Chatton, E. 1925. Pansporella perplexa, amoebien à spores protégées, parasite des Daphnies. Réflexions sur la biologie et la phylogénie des Protozoaires. Ann. Sci. Nat. Zool. 8:5–84.Google Scholar
  30. Dunstan, G.A., Volkman, J.K., Barret, S.M., Leroi, J., and Jeffrey, S.W. 1994. Essential polyunsaturated fatty acids from 14 species of diatom. Phytochemistry 35:155–161.CrossRefGoogle Scholar
  31. Desvilettes, C., Bourdier, G., Amblard, C., and Barth, B. 1997. Use of fatty acids for the assessment of zooplankton grazing on bacteria, protozoan and microalgae. Freshw. Biol. 38:629–637.CrossRefGoogle Scholar
  32. Diez, B., Pedros-Alio, C., and Massana, R. 2001. Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl. Environ. Microbiol. 67:2932–2941.PubMedCrossRefGoogle Scholar
  33. Dolan, J.R. 1997. Phosphorus and ammonia excretion by planktonic protists. Mar. Geol. 139:109–122.CrossRefGoogle Scholar
  34. Domergue, F., Spiekermann, P., Lerchl, J., Beckmann, C., Kilian, O., Kroth, P., Boland, W., Zähringer, U., and Heinz, E. 2003. New insight into Phaeodactylum tricornutum fatty acid metabolism. Cloning and functional characterization of plastidial and microsomal delta 12 fatty acid desaturases. Plant Phycol. 131:1648–1660.CrossRefGoogle Scholar
  35. Erwin, J.A. 1973. Lipids and biomembranes of eukaryotic microorganisms, pp. 40–143. In J.A. Erwin (ed.), Comparative biochemistry of fatty acids in eukaryotic microorganisms. Academic, New York.Google Scholar
  36. Fauré-Fremiet, E. 1924. Contribution à la connaissance des Infusoires planctoniques. Suppl. Bull. Biol. Fr. Bel. 6:171.Google Scholar
  37. Fogg, G.E. 1995. Some comments on picoplankton and its importance in the pelagic ecosystem. Aquat. Microb. Ecol. 9:33–39.CrossRefGoogle Scholar
  38. Gifford, D.J. 1991. The protozoan-metazoan trophic link in pelagic ecosystems. J. Protozool. 38:81–86.Google Scholar
  39. Gockel, G. and Hachtel, W. 2000. Complete gene map of the plastid genome of the nonphotosynthetic euglenoid flagellate Astasia longa. Protist 151:347–351.PubMedCrossRefGoogle Scholar
  40. Haeckel, E. 1866. Generelle Morphologie der Organismen, Allgemeine Anatomie der Organismen Vol. I, Reimer, Berlin.Google Scholar
  41. Hashimoto, K., Yoshizawa, A., Saito, K., Yamada, T., and Kanehisa, M. 2006. The repertoire of desaturases for unsaturated fatty acid synthesis in 397 genomes. Genome Inform 17:173–183.PubMedGoogle Scholar
  42. Hessen, D. O.1990. Carbon, nitrogen and phosphorus status in Daphnia at varying food conditions. J. Plankton Res. 12:1239–1249.CrossRefGoogle Scholar
  43. Johnson, M.D., Oldach, D., Delwiche, C.F., and Stoecker, D.K. 2007. Retention of transcriptionally active cryptophyte nuclei by the ciliate Myrionecta rubra. Nature 445:426–428.PubMedCrossRefGoogle Scholar
  44. Kajikawa, K.T., Yamato, Y., Kohzu, S., Shoji, K., Matsui, Y., Tanaka, Y., and Fukuzawa, H. 2006. A front-end desaturase from Chlamydomonas reinhardtii produces pinolenic and coniferonic acids by ω13 desaturation in methylotrophic yeast and tobacco. Plant.Cell Physiol. 47:64–73.PubMedCrossRefGoogle Scholar
  45. Kaneshiro, E.S. 1980. Positional distribution of fatty acids in the major glycerophospholipids of Paramecium tetraurelia. J. Lipid Res. 21:559–570.PubMedGoogle Scholar
  46. Khozin-Goldberg, I., Didi-Cohen, S., Shayakhmetova, I., and Cohen, Z. 2002. Biosynthesis of EPA in the freshwater eustigmatophyte Monodus subterraneus. J. Phycol. 38:745–751.CrossRefGoogle Scholar
  47. Klein Breteler, W.C.M., Schogt, N., Baas, M., Schouten, S., and Kraay, G.W. 1999. Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar. Biol. 135:191–198.CrossRefGoogle Scholar
  48. Klein Breteler, W.C.M., Koski, M., and Rampen, S. 2002. Role of essential lipids in copepod nutrition: no evidence for trophic upgrading of food quality by a marine ciliate. Mar. Ecol. Prog. Ser. 274:199–208.CrossRefGoogle Scholar
  49. Landry, M.R. and Calbet, A. 2004. Microzoplankton production in the oceans. ICES J. Mar. Sci. 61:501–507.CrossRefGoogle Scholar
  50. Laybourn-Parry, J. and Parry, J. 2000. Flagellates and the microbial loop, pp. 216–239. In B.S.C. Leadbeater and J.C. Green (eds.), The flagellates. unity, diversity and evolution. Taylor & Francis, London.Google Scholar
  51. Lefèvre, E., Bardot, C., Noël, C., Carrias, J-F., Viscogliosi, E., Amblard, C., and SimeNgando, T. 2007. Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ. Microbiol. 9:61–71.Google Scholar
  52. Li, W.K.W., Subba Rao, D.V., Harrison, W.C., Smith, J.C., Cullen, J.J., Irwin, B., and Platt, T. 1983. Autotrophic picoplankton in the tropical ocean. Science 219:292–295.PubMedCrossRefGoogle Scholar
  53. Mansour, M.P., Volkman, J.K., Holdsworth, D.G., Jackson, A.E., and Blackburn, S.I. 1999. Very-long-chain (C28) highly unsaturated fatty acids in marine dinoflagellates. Phytochemistry 50:541–548.CrossRefGoogle Scholar
  54. Martin-Creuzburg, D., Bec, A., and Von Elert, E. 2005. Trophic upgrading of picocyanobacterial carbon by ciliates for nutrition of Daphnia magna. Aquat. Microb. Ecol. 41:271–280.CrossRefGoogle Scholar
  55. Martin-Creuzburg, D., Bec, A., and Von Elert, E. 2006. Supplementation with sterols improves food quality of a ciliate for Daphnia magna. Protist 157:477–486.PubMedCrossRefGoogle Scholar
  56. McManus, G.B. 1991. Flow analysis of a planktonic microbial food web model. Mar. Microb. Food Webs 5:145–160.Google Scholar
  57. Metz, J.G., Roessler, P., Facciotti, D., Levering, C., Dittrich, F., Lassner, M., Valentine, R., Kathryn Lardizabal, K., Frederic Domergue, F., Yamada, A., Yazawa, K., Knauf, V., and John Browse, J. 2001. Production of polyunsaturated fatty acids by polyketide synthases in both prokaryotes and eukaryotes. Science 293:290–293.PubMedCrossRefGoogle Scholar
  58. Meyer, A., Cirpus, P., Ott, C., Schlecker, R., Zähringer, U., and Heinz, E. 2003. Biosynthesis of docosahexaenoic acid in Euglena gracilis: biochemical and molecular evidence for the involvement of a Δ4-fatty acyl group desaturase. Biochemistry 42:9779–9788.PubMedCrossRefGoogle Scholar
  59. Mignot, J-P. 1977. Etude ultrastructurale d’un flagellé du genre SpumellaChrysomonadine leucoplastidié. Protistologica 13:219–231.Google Scholar
  60. Nakashima, S., Zhao, Y., and Nozawa, Y. 1996. Molecular cloning of delta 9 fatty acid desaturase from the protozoan Tetrahymena thermophila and its mRNA expression during thermal membrane adaptation. Biochem. J. 317:29–34.PubMedGoogle Scholar
  61. Nichols, B.W. and Appleby, R.S. 1969. The distribution and biosynthesis of arachidonic acid in algae. Phytochemistry 8:1907–1915.CrossRefGoogle Scholar
  62. Nozawa, Y. and Thompson, G.A. 1979. Lipids and membrane organization in Tetrahymena, pp.276–335. In M. Levandowski and S.H. Hutner (eds.), Biochemistry and Physiology of Protozoa. Academic, New York.Google Scholar
  63. Park, J.S., Simpson, A.G.B., Lee, W.J., and Cho, B.C. 2007. Ultrastructure and phylogenetic placement within Heterolobosea of the previously unclassified, extremely halophilic heterotrophic flagellate Pleurostomum flabellatum (Ruinen 1938). Protist 158:397–413.PubMedCrossRefGoogle Scholar
  64. Parrish, C.C., Whiticar, M., and Puvanendran, V. 2007. Is ω6 docosapentaenoic acid an essential fatty acid during early ontogeny in marine fauna? Limnol. Oceanogr. 53:478–479.Google Scholar
  65. Poerschmann, J., Spijkerman, E., and Langer, U. 2004. Fatty acid patterns in Chlamydomonas sp. as a marker for nutritional regimes and temperature under extremely acidic conditions. Microb. Ecol. 48:78–89.PubMedCrossRefGoogle Scholar
  66. Pomeroy, L.R. 1974. The ocean’s food web, a changing paradigm. Bioscience. 24:499–504.CrossRefGoogle Scholar
  67. Ratledge, C. 2004. Fatty acid biosynthesis in microorganisms being used for single cell oil production. Biochimie 86:807–815.PubMedCrossRefGoogle Scholar
  68. Riekhof, W.R., Sears, B.B., and Benning, C. 2005. Annotation of genes involved in glycerolipid biosynthesis in Chlamydomonas reinhardtii: discovery of the betaine lipid synthase. Eukaryot. Cell. 4:242–252.PubMedCrossRefGoogle Scholar
  69. Rivkin, R.B. and Legendre, L. 2001. Biogenic carbon cycling in the upper ocean: effects of microbial respiration. Science 291:2398–2400.PubMedCrossRefGoogle Scholar
  70. Sanchez-Puerta, M.V., Lippmeier, J.C., Apt, K.E., and Delwiche, C.F. 2007. Plastid genes in a non-photosynthetic dinoflagellate. Protist 158:105–117.PubMedCrossRefGoogle Scholar
  71. Sanders, R.W. and Wickham, S.A. 1993. Planktonic protozoa and metazoa: predation, food quality and population control. Mar. Microb. Food Webs 7:197–223.Google Scholar
  72. Sanders, R.W., Williamson, C.E., Stutsman, P.L., Moeller, R.E., Goulden, C.E., and Aoki-Goldsmith, R. 1996. Reproductive success of “herbivorous” zooplankton fed algal and non algal food resources. Limnol. Oceanogr. 41:1295–1305.CrossRefGoogle Scholar
  73. Sargent, J.R., Bell, M.V., and Henderson, R.J. 1995. Protists as sources of (n-3) polyunsaturated fatty acids for vertebrate development, pp. 54–64. In G. Brugerolle and J. P. Mignot (eds.), Protistological actualities. Proceedings of the 2nd European Conference on Protistology and the 8th European Conference on Ciliate Biology, Aubiere Cedex, France.Google Scholar
  74. Sayanova, O., Haslam, R., Guschina, I., Lloyd, D., Christie, W.W., Harwood, J.L., and Napier, J.A. 2006. A bifunctional ∆z12, ∆15 desaturase from Acanthamoeba castellanii directs the synthesis of highly unusual n-1 series unsaturated fatty acids. J. Biol. Biochem. 281:36533–36541.Google Scholar
  75. Scott, F.J., Davidson, A.T., and MArchant, H.J. 2001. Grazing by the antarctic sea ice ciliate Pseudocohnolembus. Polar Biol. 24:127–131.CrossRefGoogle Scholar
  76. Sekiguchi, H., Moriya, M., Nakayama, T., and Inouye, I. 2001. Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae).aProtist153:157–167.CrossRefGoogle Scholar
  77. Sherr, E.B. and Sherr, B.F. 1988. Role of microbes in pelagic food webs: a revised concept. Limnol. Oceanogr. 33:225–1227.CrossRefGoogle Scholar
  78. Sherr, E.B. and Sherr, B.F. 2002. Significance of predation by protists in aquatic microbial food webs. Anton. Leeuw. Int. J. G. 81:293–308.CrossRefGoogle Scholar
  79. Sherr, E.B. and Sherr, B.F. 2007. Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar. Ecol. Prog. Ser. 352:187–197.CrossRefGoogle Scholar
  80. Sherr, E.B., Sherr, B.F., and Paffenhöffer, G.A. 1986. Phagotrophic protozoa as food for metazoans: a ‘missing’ trophic link in marine pelagic food webs? Mar. Microb. Food Webs 1:61–80.Google Scholar
  81. Sherr, B.F., Sherr, E.B., and Albright, L.J. 1987. Bacteria: link or sink? Science 235:88–89.CrossRefGoogle Scholar
  82. Stockner, J.G. and Antia, N.J. 1986. Algal picoplankton from marine and freshwater ecosystems: a multidisciplinary perspective. Can. J. Fish. Aquat. Sci. 43:2472–2503.CrossRefGoogle Scholar
  83. Stockner, J.G. and Shortreed, K.S. 1989. Algal picoplancton production and contribution to food webs in oligotrophic British Columbia lakes. Hydrobiologia 173:151–166.CrossRefGoogle Scholar
  84. Stoecker, D.K. 1998. Conceptual models of mixotrophy in planktonic protists and some ecological and evolutionary implications. Eur. J. Protistol. 34:281–290.Google Scholar
  85. Stoecker, D.K. and McDowell Capuzzo, J. 1990. Predation on protozoa: its importance to zooplankton. J. Plankton Res. 12:891–908.CrossRefGoogle Scholar
  86. Straile, D. 1997. Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator-prey weight ratio, and taxonomic group. Limnol. Oceanogr. 42:1375–1385.CrossRefGoogle Scholar
  87. Sul, D. and Erwin, J.A. 1997. The membrane lipids of the marine ciliated protozoan Parauronema acutum. Biochim. Biophys. Acta 1345:162–171.PubMedGoogle Scholar
  88. Tonon, T., Harvey, D., Larson, T.R., and Graham, I.A. 2003. Identification of a very long chain polyunsaturated fatty acid ∆4-desaturase from the microalga Pavlova lutheri. FEBS Lett. 553:440–450.PubMedCrossRefGoogle Scholar
  89. Tripodi, K., Buttigliero, L., Altabe, S., and Uttaro, A. 2005. Functional characterization of front-end desaturase from trypanosomatids depicts the first PUFA biosynthetic pathway from a parasitic protozoan. FEBS Lett. 273:271–280.Google Scholar
  90. Van Pelt , C.K., Huang , M.C., Tschanz , C.L., and Brenna , J.T . 1999. An octaene fatty acid, 4,7,10,13,16,19,22,25-octacosaoctaenoic acid (28:8n-3) found in marine oils. J. Lipid Res. 40:1501–1505.PubMedGoogle Scholar
  91. Veloza, A.J., Chu, F-L.E., and Tang, K.W. 2006. Trophic modification of essential fatty acids by heterotrophic protists and its effects on the fatty acid composition of the copepod Acartia tonsa. Mar. Biol. 148:779–788.CrossRefGoogle Scholar
  92. Venegas-Calerón , M., Beaudoin, F., Sayanova, O., and Napier, J.A. 2007. Co-transcribed genes for long chain polyunsaturated fatty acid biosynthesis in the protozoon Perkinsus marinus include a plant-like FAE1 3-ketoacyl coenzyme A synthase. Biol. Chem. 282:2996–3003.Google Scholar
  93. Vera, A., Desvilettes, C., Bec, A., and Bourdier, G. 2001. Fatty acid composition of freshwater heterotrophic flagellates: an experimental study. Aquat. Microb. Ecol. 25:271–279.CrossRefGoogle Scholar
  94. Volkman, J.K., Jeffrey, S.W., Nichols, P.D., Rogers, G.I., and Garland, C.D. 1989. Fatty acid and lipid composition of 10 species of microalgae used in aquaculture. J. Exp. Mar. Biol. Ecol. 128:219–240.CrossRefGoogle Scholar
  95. Vørs, N., Buck, K.R., Chavez, F.P., Eikrem, W., Hansen, L., Østergaard, J.B., and Thomsen, H. 1995. Nanoplankton of the equatorial Pacific with emphasis on the heterotrophic protists. Deep-Sea Res. II 42:585–602.CrossRefGoogle Scholar
  96. Wallis, J.G. and Browse, J. 1999. The Δ8 desaturase of Euglena gracilis: an alternate pathway for synthesis of 20-carbon polyunsaturated fatty acids. Archiv. Biochem. Biophys. 365:307–316.CrossRefGoogle Scholar
  97. Weisse, T. 1993. Dynamics of autotrophic picoplankton in marine and freshwater ecosystems. Adv. Microb. Ecol. 13:327–369.Google Scholar
  98. Wieltschnig, C., Kirschner, A.K.T., Steitz, A., and Velimirov, B. 2001. Weak coupling between heterotrophic nanoflagellates and bacteria in a eutrophic freshwater environment. Microb. Ecol. 42:159–167.PubMedGoogle Scholar
  99. Zhukova, N.V. and Kharlamenko, V.I. 1999. Sources of essential fatty acids in the marine microbial loop. Aquat. Microb. Ecol. 17:153–157.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Laboratoire de Biologie des ProtistesUniversité Blaise PascalAubièreFrance

Personalised recommendations