Fatty acid composition as biomarkers of freshwater microalgae: Analysis of 37 strains of microalgae in 22 genera and in seven classes

Aquatic Microbial Ecology

Volumn 71, Issue 2, 2013, Pages 165-178

  Taipale, Sami ^a   Strandberg, Ursula ^b   Peltomaa, Elina ^c   Galloway, Aaron W E ^d   Ojala, Anne ^c   Brett, Michael T ^e  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF WASHINGTON   (United States)

^e University of Washington   (United States)

Author keywords

Cryptomonads; Diatoms; Diet quality; Green algae; Lacustrine food web; Lipids; Omega 3 fatty acids

Indexed keywords

EID: 84892909318     PISSN: 09483055     EISSN: None     Source Type: Journal    
DOI: 10.3354/ame01671     Document Type: Article

References (69)

1. Ackman RG, Tocher CS, McLachlan J (1968) Marine phytoplankter fatty acids. J Fish Res Board Can 25:1603-1620
2. Ahlgren G, Gustafsson IB, Boberg M (1992) Fatty acid content and chemical composition of freshwater microalgae. J Phycol 28:37-50
3. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32-46
4. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245-253
5. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
6. Arts MT, Ackman RG, Holub BJ (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
7. Beakes GW, Canter HM, Jaworski G H M (1986) Zoospore ultrastructure of Zygorhizidium affluens and Z. planktonicum, two chytrids parasitizing the diatom Asterionella formosa. Can J Fish Aquat Sci 66:1054-1067
8. Boschker H T S, Kromkamp JC, Middelburg JJ (2005) Biomarker and carbon isotopic constraints on bacterial and algal community structure and functioning in a turbid, tidal estuary. Limnol Oceanogr 50:70-80
9. Bott TL, Kaplan LA (1985) Bacterial biomass, metabolic state and activity in stream sediments: relation to environmental variables and multiple assay comparisons. Appl Environ Microbiol 50:508-522
10. Bowman JP, Skerratt JH, Nichols PD, Sly LI (1991) Phospholipid fatty acid and lipopolysaccharide fatty acid signature lipids in methane-utilizing bacteria. FEMS Microbiol Lett 85:15-21
11. Brett MT, Müller-Navarra DC, Ballantyne AP, Ravet JL, Goldman CR (2006) Daphnia fatty acid composition reflects that of their diet. Limnol Oceanogr 51:2428-2437
12. Brett MT, Kainz MJ, Taipale SJ, Seshan H (2009a) Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci USA 106:21197-21201
13. Brett MT, Müller-Navarra DC, Persson J (2009b) Crustacean zooplankton fatty acid composition. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 115-146
14. Burns CW, Brett MT, Schallenberg M (2011) A comparison of the trophic transfer of fatty acids in freshwater plankton by cladocerans and calanoid copepods. Freshw Biol 56:889-903
15. Cagilari A, Margis R, Maraschin FS, Turchetto-Zolet AC, Loss G, Margis-Pinheiro M (2011) Biosynthesis of triacylglycerols (TAGs) in plants and algae. Int J Plant Biol 2, doi: 10.4081/pb.2011.e10
16. Canuel EA, Cloern JE, Ringelberg DB, Guckert JB, Rau GH (1995) Molecular and isotopic tracers used to examine sources of organic matter and its incorporation into the food webs of San Francisco Bay. Limnol Oceanogr 40:67-81
17. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth
18. Cranwell PA, Creighton ME, Jaworski G H M (1988) Lipids of four species of freshwater chrysophytes. Phytochemistry 27:1053-1059
19. Dalsgaard J, St John M, Kattner G, Müller-Navarra DC, Hagen HW (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar. Biol 46:225-340
20. De Mott WR (1986) The role of taste in food selection by freshwater zooplankton. Oecologia 69:334-340
21. Dijkman NA, Kromkamp JC (2006) Phospholipid-derived fatty acids as chemotaxonomic markers for phytoplankton: application for inferring phytoplankton composition. Mar. Ecol Prog Ser 324:113-125
22. Dunstan GA, Volkman JK, Jeffrey SW, Barrett SM (1992) Biochemical composition of microalgae from green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acids. J Exp Mar. Biol Ecol 161:115-134
23. Dunstan GA, Volkman JK, Barrett SM, Leroi JM, Jeffrey SW (1993) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35:155-161
24. Dunstan GA, Brown MR, Volkman JK (2005) Cryptophyceae and Rhodophyceae; chemotaxonomy, phylogeny, and application. Phytochemistry 66:2557-2570
25. Ederington MC, McManus GB, Harvey HR (1995) Trophic transfer of fatty-acids, sterols, and a triterpenoid alcohol between bacteria, a ciliate, and the copepod Acartia tonsa. Limnol Oceanogr 40:860-867
26. Galloway A W E, Britton-Simmons KH, Duggins DO, Gabrielson PW, Brett MT (2012) Fatty acid signatures differentiate marine macrophytes at ordinal and family ranks. J Phycol 48:956-965
27. Gladyshev MI, Sushchik NN, Makhutova ON, Dubovskaya OP, Kravchuk ES, Kalachova GS, Khromechek EB (2010) Correlations between fatty acid composition of seston and zooplankton and effects of environmental parameters in a eutrophic Siberian reservoir. Limnologica 40:343-357
28. Guillard R R L (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chantey MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, NY, p 29-60
29. Guillard R R L, Lorenzen CJ (1972) Yellow-green algae with chlorophyllide c. J Phycol 8:10-14
30. Guschina IA, Harwood JL (2009) Algae lipids and effects of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 1-24
31. Hanson CE, Hyndes GA, Wang SF (2010) Differentiation of benthic marine primary producers using stable isotopes and fatty acids: implications to food web studies. Aquat Bot 93:114-22
32. Harwood JL, Guschina IA (2009) The versatility of algae and their lipid metabolism. Biochimie 91:679-684
33. Iverson SJ (2009) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 281-307
34. Jordan RW, Iwataki M (2012) Chrysophyceae and Synurophyceae. eLS, doi: 10.1002/9780470015902.a0023690
35. Kainz M, Arts MT, Mazumder A (2004) Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels. Limnol Oceanogr 49:1784-1793
36. Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomical significance. Microbiol Rev 55:288-302
37. Kankaala P, Taipale S, Grey J, Sonninen E, Arvola L, Jones RI (2006) Experimental 813C evidence for a contribution of methane to pelagic food webs in lakes. Limnol Oceanogr 51:2821-2827
38. Kattner G, Hagen W (2009) Lipids in marine copepods: latitudinal characteristics. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 257-280
39. Kattner G, Gercken G, Eberlein K (1983) Development of lipids during a spring plankton bloom in the northern North Sea. I. Particulate fatty acids. Mar. Chem 14:149-162
40. Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar. Ecol Prog Ser 446:1-22
41. Korn ED (1964) The fatty acids of Euglena gracilis. J Lipid Res 5:352-362
42. Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124
43. Lee RF, Nevenzel JC, Pfaffenhöfer GA (1971) Importance of wax esters and other lipids in the marine food chain: phytoplankton and copepods. Mar. Biol 9:99-108
44. Lindström K (1983) Selenium as a growth factor for plankton algae in laboratory experiments and in some Swedish lakes. Hydrobiologia 101:35-48
45. Marshall JA, Nichols PD, Hallegraeff GM (2002) Chemotaxonomic survey of sterols and fatty acids in six marine raphidophyte algae. J Appl Phycol 14:255-265
46. Martin-Creuzburg D, Sperfeld E, Wacker A (2009) Colimitation of a freshwater herbivore by sterols and polyunsaturated fatty acids. Proc R Soc Lond B Biol Sci 276:1805-1814
47. Nichols PD, Guckert JB, White DC (1986) Determination of monounsaturated fatty acid double-bond position and geometry for microbial monocultures and complex consortia by capillary GC-MS of their dimethyl disulphide adducts. J Microbiol Methods 5:49-55
48. Nichols PD, Volkman JK, Hallegraeff GM, Blackburn SI (1987) Sterols and fatty acids of the red tide flagellates Heterosigma akashiwo and Chattonella antiqua (Raphidophyceae). Phytochemistry 26:2537-2541
49. Parrish CC (2009) Essential fatty acids in aquatic food webs. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, NY, p 309-326
50. Ratledge C, Wilkinson SG (1988) Microbial lipids, Vol 1. Academic Press, London
51. Ravet JL, Brett MT (2006) Phytoplankton essential fatty acid and phosphorus content constraints on Daphnia somatic growth and reproduction. Limnol Oceanogr 51:2438-2452
52. Ravet JL, Brett MT, Arhonditsis GB (2010) The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA. Ecology 91:180-190
53. Rengefors K, Pålsson C, Hansson LA, Heiberg L (2008) Cell lysis of competitors and osmotrophy enhance growth of the bloom-forming alga Gonyostomum semen. Aquat Microb Ecol 51:87-96
54. Sargent J, Bell G, McEvoy GL, Tocher LD, Estevez DA (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191-199
55. Smoot JC, Findlay RH (2001) Spatial and seasonal variation in a reservoir sedimentary microbial community as determined by phospholipid analysis. Microb Ecol 42:350-358
56. Stemberger RS (1981) A general approach to the culture of planktonic rotifers. Can J Fish Aquat Sci 38:721-724
57. Stott AW, Davies E, Evershed RP, Tuross NR (1997) Monitoring the routing of dietary and biosynthesised lipids through compound-specific stable isotope (d13C) measurements at natural abundance. Naturwissenschaften 84:82-86
58. Taipale S, Kankaala P, Hämäläinen H, Jones RI (2009) Seasonal shifts in the diet of lake zooplankton revealed by phospholipid fatty acid analysis. Freshw Biol 54:90-104
59. Taipale SJ, Kainz MJ, Brett MT (2011) Diet-switching experiments show rapid accumulation and preferential retention of highly unsaturated fatty acids in Daphnia. Oikos 120:1674-1682
60. Taipale SJ, Brett M, Pulkkinen K, Kainz MJ (2012) The influence of bacteria-dominated diets on Daphnia magna somatic growth, reproduction, and lipid composition. FEMS Microbiol Ecol 82:50-62
61. Taipale SJ, Brett MT, Hahn MW, Martin-Creuzburg D and others (in press) Differing Daphnia magna assimilation efficiencies for terrestrial, bacterial and algal carbon and fatty acids. Ecology, doi: 10.1890/13-0650.1
62. Tatsuzawa H, Takizawa E (1995) Changes in lipid and fatty acid composition of Pavlova lutheri. Phytochemistry 40:397-400
63. Viso AC, Marty JC (1993) Fatty acids from 28 marine microalgae. Phytochemistry 34:1521-1533
64. 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. Limnol Oceanogr 47:1764-1773
65. Wakeham GS (1995) Lipid biomarkers for heterotrophic alteration of suspended particulate organic matter in oxygenated and anoxic water columns of the ocean. Deep-Sea Res I 142:1749-1771
66. Watanabe MM, Kawachi M, Hiroki M, Kasai F (eds) (2000) NIES collection list of strains, 6th edn. National Institute for Environmental Studies, Tsukuba
67. Watanabe T (1993) Importance of docosahexaenoic acid in marine larval fish. J World Aquacult Soc 24:152-161
68. White DC, Davis WM, Nickels JS, King JD, Robbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40:51-62
69. Wilson RP (2003) Amino acids and proteins. In: Halver JE, Hardy RW (eds) Fish nutrition. Academic Press, San Diego, CA, p 143-179