Linking elements to biochemicals: Effects of nutrient supply ratios and growth rates on fatty acid composition of phytoplankton species

Journal of Phycology

Volumn 50, Issue 1, 2014, Pages 117-130

  Bi, Rong ^a   Arndt, Carmen ^a   Sommer, Ulrich ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

Author keywords

Algae; Cell quota; Dilution rate; Fatty acids; N:P ratio; Nutrient limitation; Semicontinuous culture

Indexed keywords

EID: 84894057969     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/jpy.12140     Document Type: Article

References (92)

1. Abdullahi, A. S., Underwood, G. J. C. & Gretz, M. R. 2006. Extracellular matrix assembly in diatoms (Bacillariophyceae). V. Environmental effects on polysaccharide synthesis in the model diatom, Phaeodactylum tricornutum. J. Phycol. 42:363-78.
2. Ahlgren, G. 1985. Growth of Oscillatoria agardhii in chemostat culture 3. Simultaneous limitation of nitrogen and phosphorus. Br. Phycol. J. 20:249-61.
3. Ahlgren, G. & Hyenstrand, P. 2003. Nitrogen limitation effects of different nitrogen sources on nutritional quality of two freshwater organisms, Scenedesmus quadricauda (Chlorophyceae) and Synechococcus sp. (Cyanophyceae). J. Phycol. 39:906-17.
4. Alonso, D. L., Belarbi, E.H., Rodríguez-Ruiz, J., Segura, C. I. & Giménez, A. 1998. Acyl lipids of three microalgae. Phytochemistry 47:1473-81.
5. Anderson, T. R., Boersma, M. & Raubenheimer, D. 2004. Stoichiometry: linking elements to biochemicals. Ecology 85:1193-202.
6. Anderson, M. J., Gorley, R. N. & Clarke, K. R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, 214 pp.
7. Arts, M. T., Ackman, R. G. & Holub, B. J. 2001. "Essential fatty acids" in aquatic ecosystems: a crucial link between diet and human health and evolution. Can. J. Fish. Aquat. Sci. 58:122-37.
8. Ben-Amotz, A., Tornabene, T. G. & Thomas, W. H. 1985. Chemical profile of selected species of microalgae with emphasis on lipids. J. Phycol. 21:72-81.
9. Bergé, J.P. & Barnathan, G. 2005. Fatty acids from lipids of marine organisms: molecular biodiversity, roles as biomarkers, biologically Active compounds, and economical aspects. Adv. Biochem. Eng. Biotechnol. 96:49-125.
10. Bi, R., Arndt, C. & Sommer, U. 2012. Stoichiometric responses of phytoplankton species to the interactive effect of nutrient supply ratios and growth rates. J. Phycol. 48:539-49.
11. Boersma, M., Schöps, C. & McCauley, E. 2001. Nutritional quality of seston for the freshwater herbivore Daphnia galeata × hyalina: biochemical versus mineral limitations. Oecologia 129:342-8.
12. Borowitzka, M. A. 1988. Fats, oils and hydrocarbons. In Borowitzka, M. A. & Borowitzka, L. J. [Eds.] Micro-algal Biotechnology. Cambridge University Press, Cambridge, pp. 257-87.
13. Brepohl, D. C. 2005. Fatty acids distribution in marine, brackish and freshwater plankton during mesocosm experiments. PhD dissertation, Christian-Albrechts-University Kiel, Kiel, Germany, 77 pp.
14. Brett, M. & Müller-Navarra, D. C. 1997. The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshw. Biol. 38:483-99.
15. Breuer, G., Lamers, P. P., Martens, D. E., Draaisma, R. B. & Wijffels, R. H. 2012. The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour. Technol. 124:217-26.
16. Broglio, E., Jónasdóttir, S. H., Calbet, A., Jakobsen, H. H. & 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. 31:267-78.
17. Brown, M. R., Dunstan, G. A., Norwood, S. J. & Miller, K. A. 1996. Effects of harvest stage and light on the biochemical composition of the diatom Thalassiosira pseudonana. J. Phycol. 32:64-73.
18. Brown, M. R., Jeffrey, S. W., Volkman, J. K. & Dunstan, G. A. 1997. Nutritional properties of microalgae for mariculture. Aquaculture 151:315-31.
19. Carvalho, A. P., Pontes, I., Gaspar, H. & Malcata, F. X. 2006. Metabolic relationships between macro- and micronutrients, and the eicosapentaenoic acid and docosahexaenoic acid contents of Pavlova lutheri. Enzyme Microb. Technol. 38:358-66.
20. Cavender-Bares, K. K., Karl, D. M. & Chisholm, S. W. 2001. Nutrient gradients in the western North Atlantic Ocean: relationship to microbial community structure and comparison to patterns in the Pacific Ocean. Deep-Sea Res. Part I Oceanogr. Res. Pap. 48:2373-95.
21. Chen, X., Wakeham, S. G. & Fisher, N. S. 2011. Influence of iron on fatty acid and sterol composition of marine phytoplankton and copepod consumers. Limnol. Oceanogr. 56:716-24.
22. Clarke, K. & Gorley, R. 2006. PRIMER v6: User Manual/tutorial. PRIMER-E, Plymouth, 190 pp.
23. Cohen, Z., Khozin-Goldberg, I., Adlerstein, D. & Bigogno, C. 2000. The role of triacylglycerol as a reservoir of polyunsaturated fatty acids for the rapid production of chloroplastic lipids in certain microalgae. Biochem. Soc. Trans. 28:740-3.
24. Cohen, Z., Vonshak, A. & Richmond, A. 1988. Effect of environmental conditions on fatty acid composition of the red alga Porphyridium cruentum: correlation to growth rate. J. Phycol. 24:328-32.
25. Conley, D. J., Paerl, H. W., Howarth, R. W., Boesch, D. F., Seitzinger, S. P., Havens, K. E., Lancelot, C. & Likens, G. E. 2009. Controlling eutrophication: nitrogen and phosphorus. Science 323:1014-5.
26. Dalsgaard, J., St. John, M., Kattner, G., Müller-Navarra, D. & Hagen, W. 2003. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46:225-340.
27. Dunstan, G. A., Volkman, J. K., Barrett, S. M. & Garland, C. D. 1993. Changes in the lipid composition and maximisation of the polyunsaturated fatty acid content of three microalgae grown in mass culture. J. Appl. Phycol. 5:71-83.
28. Elser, J. J., Bracken, M. E. S., Cleland, E. E., Gruner, D. S., Harpole, W. S., Hillebrand, H., Ngai, J. T., Seabloom, E. W., Shurin, J. B. & Smith, J. E. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10:1135-42.
29. Ferreira, M., Seixas, P., Coutinho, P., Fábregas, J. & Otero, A. 2011. Effect of the nutritional status of semi-continuous microalgal cultures on the productivity and biochemical composition of Brachionus plicatilis. Mar. Biotechnol. 13:1074-85.
30. Flynn, K. J., Davidson, K. & Leftley, J. W. 1994. Carbon-nitrogen relations at whole-cell and free-amino-acid levels during batch growth of Isochrysis galbana (Prymnesiophyceae) under conditions of alternating light and dark. Mar. Biol. 118:229-37.
31. Ford, B. I., Duncan, M. N. L., Annette, O. & Parviez, H. 2008. Nutrient recycling affects autotroph and ecosystem stoichiometry. Am. Nat. 171:511-23.
32. George, S. B., Fox, C. & Wakeham, S. 2008. Fatty acid composition of larvae of the sand dollar Dendraster excentricus (Echinodermata) might reflect FA composition of the diets. Aquaculture 285:167-73.
33. Gladyshev, M., Sushchik, N., Kolmakova, A., Kalachova, G., Kravchuk, E., Ivanova, E. & Makhutova, O. 2007. Seasonal correlations of elemental and ω3 PUFA composition of seston and dominant phytoplankton species in a eutrophic Siberian Reservoir. Aquat. Ecol. 41:9-23.
34. Goldman, J. C., McCarthy, J. J. & Peavey, D. G. 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279:210-5.
35. Graham, M. H. & Edwards, M. S. 2001. Statistical significance versus fit: estimating the importance of individual factors in ecological analysis of variance. Oikos 93:505-13.
36. Gulati, R. & DeMott, W. 1997. The role of food quality for zooplankton: remarks on the state-of-the-art, perspectives and priorities. Freshw. Biol. 38:753-68.
37. Guschina, I. A. & Harwood, J. L. 2006. Lipids and lipid metabolism in eukaryotic algae. Prog. Lipid Res. 45:160-86.
38. Guschina, I. A. & Harwood, J. L. 2009. Algal lipids and effect of the environment on their biochemistry. In Arts, M. T., Brett, M. T. & Kainz, M. J. [Eds.] Lipids in Aquatic Ecosystems. Springer, Heidelberg, pp. 1-24.
39. Hammer, A., Schumann, R. & Schubert, H. 2002. Light and temperature acclimation of Rhodomonas salina (Cryptophyceae): photosynthetic performance. Aquat. Microb. Ecol. 29:287-96.
40. Hansen, H. P. & Koroleff, F. 1999. Determination of nutrients. In Grasshoff, K., Kremling, K. & Ehrhardt, M. [Eds.] Methods of Seawater Analysis, 3rd ed. WILEY-VCH, Weinheim, pp. 159-228.
41. Harrison, P., Thompson, P. & Calderwood, G. 1990. Effects of nutrient and light limitation on the biochemical composition of phytoplankton. J. Appl. Phycol. 2:45-56.
42. Hartwich, M., Straile, D., Gaedke, U. & Wacker, A. 2012. Use of ciliate and phytoplankton taxonomic composition for the estimation of eicosapentaenoic acid concentration in lakes. Freshw. Biol. 57:1385-98.
43. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M. & Darzins, A. 2008. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 54:621-39.
44. Hughes, A. R. & Stachowicz, J. J. 2009. Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina. Ecology 90:1412-9.
45. Ismar, S. M. H., Hansen, T. & Sommer, U. 2008. Effect of food concentration and type of diet on Acartia survival and naupliar development. Mar. Biol. 154:335-43.
46. Jiang, H. & Gao, K. 2004. Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum (Bacillariophyceae). J. Phycol. 40:651-4.
47. Kainz, M., Arts, M. T. & Mazumder, A. 2004. Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol. Oceanogr. 49:1784-93.
48. Karl, D. M., Tien, G., Dore, J. & Winn, C. D. 1993. Total dissolved nitrogen and phosphorus concentrations at US-JGOFS station ALOHA: redfield reconciliation. Mar. Chem. 41:203-8.
49. Kelly, J. R. & Scheibling, R. E. 2012. Fatty acids as dietary tracers in benthic food webs. Mar. Ecol. Prog. Ser. 446:1-22.
50. Khozin-Goldberg, I., Bigogno, C., Shrestha, P. & Cohen, Z. 2002. Nitrogen starvation induces the accumulation of arachidonic acid in the freshwater green alga Parietochloris incisa (Trebuxiophyceae). J. Phycol. 38:991-4.
51. Lacour, T., Sciandra, A., Talec, A., Mayzaud, P. & Bernard, O. 2012. Diel variations of carbohydrates and neutral lipids in nitrogen-sufficient and nitrogen-starved cyclostat cultures of Isochrysis sp. J. Phycol. 48:966-75.
52. Lam, P. & Kuypers, M. M. M. 2011. Microbial nitrogen cycling processes in oxygen minimum zones. Annu. Rev. Mar. Sci. 3:317-45.
53. Lampert, W. 2009. Foreword. In Arts, M. T., Brett, M. T. & Kainz, M. J. [Eds.] Lipids in Aquatic Ecosystems. Springer, Heidelberg, pp. v-vi.
54. Liang, Y., Beardall, J. & Heraud, P. 2006. Changes in growth, chlorophyll fluorescence and fatty acid composition with culture age in batch cultures of Phaeodactylum tricornutum and Chaetoceros muelleri (Bacillariophyceae). Bot. Mar. 49:165-73.
55. Lindeman, R. L. 1942. The trophic-dynamic aspect of ecology. Ecology 23:399-417.
56. Lynn, S. G., Kilham, S. S., Kreeger, D. A. & Interlandi, S. J. 2000. Effect of nutrient availability on the biochemical and elemental stoichiometry in the freshwater diatom Stephanodiscus minutulus (Bacillariophyceae). J. Phycol. 36:510-22.
57. Malzahn, A. M., Hantzsche, F., Schoo, K. L., Boersma, M. & Aberle, N. 2010. Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers. Oecologia 162:35-48.
58. Moore, C. M., Mills, M. M., Arrigo, K. R., Berman-Frank, I., Bopp, L., Boyd, P. W., Galbraith, E. D. et al. 2013. Processes and patterns of oceanic nutrient limitation. Nat. Geosci. 6:701-10.
59. Mourente, G., Lubián, L. M. & Odriozola, J. M. 1990. Total fatty acid composition as a taxonomic index of some marine microalgae used as food in marine aquaculture. Hydrobiologia 203:147-54.
60. Müller-Navarra, D. C. 1995. Biochemical versus mineral limitation in Daphnia. Limnol. Oceanogr. 40:1209-14.
61. Müller-Navarra, D. C. 2008. Food web paradigms: the biochemical view on trophic interactions. Int. Rev. Hydrobiol. 93:489-505.
62. Otero, A. & Fábregas, J. 1997. Changes in the nutrient composition of Tetraselmis suecica cultured semicontinuously with different nutrient concentrations and renewal rates. Aquaculture 159:111-23.
63. Palmucci, M., Ratti, S. & Giordano, M. 2011. Ecological and evolutionary implications of carbon allocation in marine phytoplankton as a function of nitrogen availability: a fourier transform infrared spectroscopy approach. J. Phycol. 47:313-23.
64. Parke, M. 1949. Studies on marine flagellates. J. Mar. Biol. Assoc. U. K. 28:255-86.
65. Parrish, C. C. 2009. Essential fatty acids in aquatic food webs. In Arts, M. T., Brett, M. T. & Kainz, M. J. [Eds.] Lipids in Aquatic Ecosystems. Springer, Heidelberg, pp. 309-26.
66. Parrish, C. C., French, V. M. & Whiticar, M. J. 2012. Lipid class and fatty acid composition of copepods (Calanus finmarchicus, C. glacialis, Pseudocalanus sp., Tisbe furcata and Nitokra lacustris) fed various combinations of autotrophic and heterotrophic protists. J. Plankton Res. 34:356-75.
67. Patil, V., Källqvist, T., Olsen, E., Vogt, G. & Gislerød, H. 2007. Fatty acid composition of 12 microalgae for possible use in aquaculture feed. Aquacult. Int. 15:1-9.
68. Piepho, M., Arts, M. T. & Wacker, A. 2012. Species-specific variation in fatty acid concentrations of four phytoplankton species: does phosphorus supply influence the effect of light intensity or temperature? J. Phycol. 48:64-73.
69. Piorreck, M. & Pohl, P. 1984. Formation of biomass, total protein, chlorophylls, lipids and fatty acids in green and blue-green algae during one growth phase. Phytochemistry 23:217-23.
70. Provasoli, L. 1963. Growing marine seaweeds. In De Virville, A. D. & Feldmann, J. [Eds.] Proc. 4th Internatl. Seaweed Symp. Pergamon Press, Oxford, pp. 9-17.
71. Reitan, K., Jose, R. R. & Yngvar, O. 1994. Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J. Phycol. 30:972-9.
72. Renaud, S. M., Thinh, L.V., Lambrinidis, G. & Parry, D. L. 2002. Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195-214.
73. Reuss, N. R. & Poulsen, L. P. 2002. 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. 141:423-34.
74. Rhee, G. Y. 1978. Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnol. Oceanogr. 23:10-25.
75. Roessler, P. G. 1990. Environmental control of glycerolipid metabolism in microalgae: commercial implications and future research directions. J. Phycol. 26:393-9.
76. Roleda, M. Y., Slocombe, S. P., Leakey, R. J. G., Day, J. G., Bell, E. M. & Stanley, M. S. 2013. Effects of temperature and nutrient regimes on biomass and lipid production by six oleaginous microalgae in batch culture employing a two-phase cultivation strategy. Bioresour. Technol. 129:439-49.
77. Schlüter, L., Møhlenberg, F., Havskum, H. & Larsen, S. 2000. The use of phytoplankton pigments for identifying and quantifying phytoplankton groups in coastal areas: testing the influence of light and nutrients on pigment/chlorophyll a ratios. Mar. Ecol. Prog. Ser. 192:49-63.
78. Sharp, J. 1974. Improved analysis for particulate organic carbon and nitrogen from seawater. Limnol. Oceanogr. 19:984-9.
79. Siron, R., Giusti, G. & Berland, B. 1989. Changes in the fatty acid composition of Phaeodactylum tricornutum and Dunaliella tertiolecta during growth and under phosphorus deficiency. Mar. Ecol. Prog. Ser. 55:95-100.
80. Sommer, U., Adrian, R., De Senerpont Domis, L., Elser, J. J., Gaedke, U., Ibelings, B., Jeppesen, E. et al. 2012. Beyond the Plankton Ecology Group (PEG) Model: mechanisms driving plankton succession. Annu. Rev. Ecol. Evol. Syst. 43:429-48.
81. Spijkerman, E. & Wacker, A. 2011. Interactions between P-limitation and different C conditions on the fatty acid composition of an extremophile microalga. Extremophiles 15:597-609.
82. Sterner, R. W. & Hessen, D. O. 1994. Algal nutrient limitation and the nutrition of aquatic herbivores. Annu. Rev. Ecol. Syst. 25:1-29.
83. Sterner, R. & Schulz, K. 1998. Zooplankton nutrition: recent progress and a reality check. Aquat. Ecol. 32:261-79.
84. Terry, K. L., Hirata, J. & Laws, E. A. 1985. Light-, nitrogen-, and phosphorus-limited growth of Phaeodactylum tricornutum Bohlin strain TFX-1: chemical composition, carbon partitioning, and the diel periodicity of physiological processes. J. Exp. Mar. Biol. Ecol. 86:85-100.
85. Thompson, G. A. 1996. Lipids and membrane function in green algae. Biochim. Biophys. Acta 1302:17-45.
86. Thompson, P. A., Harrison, P. J. & Whyte, J. N. C. 1990. Influence of irradiance on the fatty acid composition of phytoplankton. J. Phycol. 26:278-88.
87. Tonon, T., Harvey, D., Larson, T. R. & Graham, I. A. 2002. Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae. Phytochemistry 61:15-24.
88. Twomey, L. & Thompson, P. 2001. Nutrient limitation of phytoplankton in a seasonally open bar-built estuary: Wilson Inlet, Western Australia. J. Phycol. 37:16-29.
89. Van Mooy, B. A. S. & Fredricks, H. F. 2010. Bacterial and eukaryotic intact polar lipids in the eastern subtropical South Pacific: water-column distribution, planktonic sources, and fatty acid composition. Geochim. Cosmochim. Ac. 74:6499-516.
90. Van Mooy, B. A. S., Fredricks, H. F., Pedler, B. E., Dyhrman, S. T., Karl, D. M., Koblizek, M., Lomas, M. W. et al. 2009. Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69-72.
91. Van Mooy, B. A. S., Rocap, G., Fredricks, H. F., Evans, C. T. & Devol, A. H. 2006. Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc. Natl. Acad. Sci. UA 103:8607-12.
92. Veloza, A., Chu, F.L. & Tang, K. 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. 148:779-88.