The essential omega-3 fatty acid EPA affects expression of genes involved in the metabolism of omega-6-derived eicosanoids in Daphnia magna

  • Patrick Fink
  • Heidrun S. Windisch


Eicosanoids are an important class of signalling molecules derived from essential polyunsaturated fatty acids (PUFAs). Some recent research had started to investigate the eicosanoid pathway in Daphnia magna, but focussed mostly on the role of omega-6 PUFAs, rather than on the nutritionally important omega-3 PUFA eicosapentaenoic acid (EPA), which is known to determine the trophic transfer efficiency from phytoplankton to cladoceran zooplankton in freshwater foodwebs. To test for the relevance of EPA for the expression of genes in the eicosanoid pathway, we conducted highly controlled feeding experiments with D. magna under two temperature conditions and supplemented diets differing only in their EPA contents. Some, but not all genes previously reported to be related to the eicosanoid metabolism of D. magna, were significantly upregulated when EPA was available in the diet. Other genes from the eicosanoid pathway and two control genes not related to eicosanoid metabolism were unaffected by dietary EPA availability. Our data demonstrate that dietary omega-3 PUFA availability affects the expression of some genes typically considered to be part of the omega-6 PUFA-dependent eicosanoid metabolism. These findings may thus advance our understanding of the biochemical physiology of this essential dietary compound and its role for zooplankton nutrition.


Diet Eicosapentaenoic acid Food quality qPCR Polyunsaturated fatty acids Prostaglandins 



The authors thank Melina Meffert for her assistance in the laboratory and to Nina Schlotz and Dominik Martin-Creuzburg for their valuable comments on an earlier draft of this manuscript. This study was funded by the Heinrich-Heine-University of Duesseldorf and the German Research Foundation (DFG), under Grant FI 1548-6-1 to PF.

Supplementary material

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Supplementary material 1 (DOCX 27 kb)


  1. Ahlgren, G., I. B. Gustafsson & M. Boberg, 1992. Fatty acid content and chemical composition of freshwater microalgae. Journal of Phycology 28: 37–50.CrossRefGoogle Scholar
  2. Becker, C. & M. Boersma, 2003. Resource quality effects on life histories of Daphnia. Limnology and Oceanography 48(2): 700–706.CrossRefGoogle Scholar
  3. Brzezinski, T. & E. von Elert, 2015. Predator evasion in zooplankton is suppressed by polyunsaturated fatty acid limitation. Oecologia 179(3): 687–697. Scholar
  4. Calder, P. C., 2010. Omega-3 fatty acids and inflammatory processes. Nutrients 2(3): 355.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chorus, I. & J. Bartram (eds), 1999. Toxic Cyanobacteria in Water – A Guide to Their Public Health Consequences, Monitoring and Management. E & FN Spoon, London.Google Scholar
  6. Cook, H. W. & C. R. McMaster, 2002. Chapter 7 Fatty Acid Desaturation and Chain Elongation in Eukaryotes New Comprehensive Biochemistry, Vol. 36. Elsevier, New York: 181–204.Google Scholar
  7. Fritsche, K., 2006. Fatty acids as modulators of the immune response. Annual Review of Nutrition 26(1): 45–73. Scholar
  8. Gygi, S. P., Y. Rochon, B. R. Franza & R. Aebersold, 1999. Correlation between protein and mRNA abundance in yeast. Molecular and Cellular Biology 19(3): 1720–1730. Scholar
  9. Hazel, J. R., 1995. Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annual Review Physiology 57: 19–42.CrossRefGoogle Scholar
  10. Heckmann, L. H., R. Connon, T. H. Hutchinson, S. J. Maund, R. M. Sibly & A. Callaghan, 2006. Expression of target and reference genes in Daphnia magna exposed to ibuprofen. BMC Genomics 7: 175.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Heckmann, L.-H., R. M. Sibly, R. Connon, H. L. Hooper, T. H. Hutchinson, S. J. Maund, C. J. Hill, A. Bouetard & A. Callaghan, 2008a. Systems biology meets stress ecology: linking molecular and organismal stress responses in Daphnia magna. Genome Biology 9(2): R40. Scholar
  12. Heckmann, L. H., R. M. Sibly, M. Timmermans & A. Callaghan, 2008b. Outlining eicosanoid biosynthesis in the crustacean Daphnia. Front Zool 5: 11.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Lampert, W., 2006. Daphnia: model herbivore, predator and prey. Polish Journal of Ecology 54(4): 607–620.Google Scholar
  14. Martin-Creuzburg, D., E. von Elert & K. H. Hoffmann, 2008. Nutritional constraints at the cyanobacteria-Daphnia magna interface: the role of sterols. Limnology and Oceanography 53(2): 456–468.CrossRefGoogle Scholar
  15. Martin-Creuzburg, D., A. Wacker & T. Basen, 2010. Interactions between limiting nutrients: consequences for somatic and population growth of Daphnia magna. Limnology and Oceanography 55(6): 2597–2607. Scholar
  16. Müller-Navarra, D., 1995. Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Archiv Fuer Hydrobiologie 132(3): 297–307.Google Scholar
  17. Müller-Navarra, D. C., 2008. Food web paradigms: the biochemical view on trophic interactions. International Review Hydrobiology 93(4–5): 489–505.CrossRefGoogle Scholar
  18. Nie, L., G. Wu & W. Zhang, 2006. Correlation between mRNA and protein abundance in Desulfovibrio vulgaris: a multiple regression to identify sources of variations. Biochemical Biophysical Research Communications 339(2): 603–610. Scholar
  19. Obata, T., T. Nagakura, T. Masaki, K. Maekawa & K. Yamashita, 1999. Eicosapentaenoic acid inhibits prostaglandin D2 generation by inhibiting cyclo-oxygenase-2 in cultured human mast cells. Clinical Experimental Allergy 29(8): 1129–1135.CrossRefPubMedGoogle Scholar
  20. Pajk, F., E. von Elert & P. Fink, 2012. Interaction of changes in food quality and temperature reveals maternal effects on fitness parameters of a keystone aquatic herbivore. Limnology and Oceanography 57(1): 281–292. Scholar
  21. Peters, R. H. & R. De Bernardi (eds), 1987. Daphnia. Istituto Italiano di Idrobiologia, Verbania Pallanza.Google Scholar
  22. R Core Team, 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  23. Schlotz, N., J. G. Sørensen & D. Martin-Creuzburg, 2012. The potential of dietary polyunsaturated fatty acids to modulate eicosanoid synthesis and reproduction in Daphnia magna: a gene expression approach. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 162(4): 449–454. Scholar
  24. Schlotz, N., D. Ebert & D. Martin-Creuzburg, 2013. Dietary supply with polyunsaturated fatty acids and resulting maternal effects influence host – parasite interactions. BMC Ecology 13: 41. Scholar
  25. Schlotz, N., M. Pester, H. M. Freese & D. Martin-Creuzburg, 2014. A dietary polyunsaturated fatty acid improves consumer performance during challenge with an opportunistic bacterial pathogen. Fems Microbiology Ecology 90(2): 467–477. Scholar
  26. Schlotz, N., A. Roulin, D. Ebert & D. Martin-Creuzburg, 2016. Combined effects of dietary polyunsaturated fatty acids and parasite exposure on eicosanoid-related gene expression in an invertebrate model. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 201(Supplement C): 115–123. Scholar
  27. Schmittgen, T. D. & K. J. Livak, 2008. Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3(6): 1101–1108.CrossRefPubMedGoogle Scholar
  28. Sinensky, M., 1974. Homeoviscous adaptation – a homeostatic process that regulates the viscosity of membrane lipids in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 71(2): 522–525.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Sperfeld, E. & A. Wacker, 2012. Temperature affects the limitation of Daphnia magna by eicosapentaenoic acid, and the fatty acid composition of body tissue and eggs. Freshwater Biology 57(3): 497–508. Scholar
  30. Stanley, D. W., 2000. Eicosanoids in Invertebrate Signal Transduction Systems. Princeton University Press, Princeton.Google Scholar
  31. Sterner, R. W. & J. J. Elser, 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton.Google Scholar
  32. Von Elert, E., 2002. Determination of limiting polyunsaturated fatty acids in Daphnia galeata using a new method to enrich food algae with single fatty acids. Limnology and Oceanography 47(6): 1764–1773.CrossRefGoogle Scholar
  33. Von Elert, E., 2004. Food quality constraints in Daphnia: interspecific differences in the response to the absence of a long chain polyunsaturated fatty acid in the food source. Hydrobiologia 526(1): 187–196.CrossRefGoogle Scholar
  34. Von Elert, E., D. Martin-Creuzburg & J. R. Le Coz, 2003. Absence of sterols constrains carbon transfer between cyanobacteria and a freshwater herbivore (Daphnia galeata). Proceedings of the Royal Society of London – Series B: Biological Sciences 270(1520): 1209–1214.CrossRefGoogle Scholar
  35. von Elert, E., L. Oberer, P. Merkel, T. Huhn & J. F. Blom, 2005. Cyanopeptolin 954, a chlorine-containing chymotrypsin inhibitor of Microcystis aeruginosa NIVA Cya 43. Journal of Natural Products 68(9): 1324–1327.CrossRefGoogle Scholar
  36. Wacker, A. & D. Martin-Creuzburg, 2007. Allocation of essential lipids in Daphnia magna during exposure to poor food quality. Functional Ecology 21(4): 738–747.CrossRefGoogle Scholar
  37. Wacker, A. & E. von Elert, 2001. Polyunsaturated fatty acids: evidence for non-substitutable biochemical resources in Daphnia galeata. Ecology 82(9): 2507–2520.CrossRefGoogle Scholar
  38. Wathes, D. C., D. R. E. Abayasekara & R. J. Aitken, 2007. Polyunsaturated fatty acids in male and female reproduction. Biology of Reproduction 77(2): 190–201. Scholar
  39. Windisch, H. S. & P. Fink, 2018. The molecular basis of essential fatty acid limitation in Daphnia magna: a transcriptomic approach. Molecular Ecology 27(4): 871–885. Scholar
  40. Yuan, D., Q. Zou, T. Yu, C. Song, S. Huang, S. Chen, Z. Ren & A. Xu, 2014. Ancestral genetic complexity of arachidonic acid metabolism in metazoa. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids 1841(9): 1272–1284. Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Workgroup Aquatic Chemical Ecology, Institute for ZoologyUniversity of CologneKoelnGermany
  2. 2.Institute for Zoology and Cell BiologyHeinrich-Heine-University of DuesseldorfDuesseldorfGermany
  3. 3.University of Cologne, Cologne BiocenterKoelnGermany

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