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Light-Induced Changes in Fatty Acid Profiles of Specific Lipid Classes in Several Freshwater Phytoplankton Species

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Light-Induced Changes in Fatty Acid Profiles of Specific Lipid Classes in Several Freshwater Phytoplankton Species Light-induced changes in fatty acid profiles of specific lipid classes in several freshwater phytoplankton species Alexander Wacker1*, Maike Piepho2, John L. Harwood3, Irina A. Guschina3, Michael T. Arts4 1Institute of Biology and Biochemistry, University of Potsdam, Germany, 2Institute of 3 Aquatic Ecology, University of Rostock, Germany, School of Biosciences, Cardiff University, United Kingdom, 4Department of Chemistry and Biology, Ryerson University, Canada Submitted to Journal: Frontiers in Plant Science Specialty Section: Plant Metabolism and Chemodiversity ISSN: 1664-462X Article type: Original Research Article Received on: 23 Dec 2015 Accepted on: 19 Feb 2016 Provisional PDF published on: Provisional19 Feb 2016 Frontiers website link: www.frontiersin.org Citation: Wacker A, Piepho M, Harwood JL, Guschina IA and Arts MT(2016) Light-induced changes in fatty acid profiles of specific lipid classes in several freshwater phytoplankton species. Front. Plant Sci. 7:264. doi:10.3389/fpls.2016.00264 Copyright statement: © 2016 Wacker, Piepho, Harwood, Guschina and Arts. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. This Provisional PDF corresponds to the article as it appeared upon acceptance, after peer-review. Fully formatted PDF and full text (HTML) versions will be made available soon. Frontiers in Plant Science | www.frontiersin.org Provisional 1 Light-induced changes in fatty acid profiles of specific lipid classes in several 2 freshwater phytoplankton species 3 4 5 Alexander Wacker1*, Maike Piepho2, John L. Harwood3, Irina A. Guschina3, Michael T. 6 Arts4 1 7 Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany 2 8 Institute of Aquatic Ecology, University of Rostock, Rostock, Germany 3 9 School of Biosciences, Cardiff University, Cardiff, United Kingdom 4 10 Department of Chemistry and Biology, Ryerson University, Toronto, Ontario, Canada 11 * Correspondence: Alexander Wacker, Theoretical Aquatic Ecology and Ecophysiology, 12 University of Potsdam, Institute of Biochemistry and Biology, Am Neuen Palais 10, Potsdam, 13 14469 14 [email protected] 15 16 Keywords: freshwater algae, light adaptation, lipid classes, fatty acid changes 17 18 19 Abstract 20 We tested the influence of two light intensities [40 and 300 µmol PAR / (m² s)] on the fatty 21 acid composition of three distinct lipid classes in four freshwater phytoplankton species. We 22 chose species of different taxonomic classes in order to detect potentially similar reaction 23 characteristics that might also be present in natural phytoplankton communities. From 24 samples of the bacillariophyte Asterionella formosa, the chrysophyte Chromulina sp., the 25 cryptophyte Cryptomonas ovata and the zygnematophyte Cosmarium botrytis we first 26 separated glycolipids (monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and 27 sulfoquinovosyldiacylglycerol), phospholipids (phosphatidylcholine, phosphatidylethanol- 28 amine, phosphatidylglycerol, phosphatidylinositol, and phosphatidylserine) as well as non- 29 polar lipids (triacylglycerols), before analyzing the fatty acid composition of each lipid class. 30 HighProvisional variation in the fatty acid composition existed among different species. Individual fatty 31 acid compositions differed in their reaction to changing light intensities in the four species. 32 Although no generalizations could be made for species across taxonomic classes, individual 33 species showed clear but small responses in their ecologically-relevant omega-3 and omega-6 34 polyunsaturated fatty acids in terms of proportions and of per carbon quotas. Knowledge on 35 how lipids like fatty acids change with environmental or culture conditions is of great interest 36 in ecological food web studies, aquaculture and biotechnology, since algal lipids are the most 37 important sources of omega-3 long-chain polyunsaturated fatty acids for aquatic and 38 terrestrial consumers, including humans. 39 --------------------------------------------------------------------------------------------------------------- 40 Abbreviations: 41 ALA, α-linolenic acid; DGDG, digalactosyldiacylglycerol; DHA, docosahexaenoic acid; 42 EPA, eicosapentaenoic acid; FA, fatty acid; FAME, fatty acid methyl ester; GL, glycolipid; 43 LHC, light harvesting complex; LNA, linoleic acid; MGDG, monogalactosyldiacylglycerol; 44 MUFA, monounsaturated fatty acid; NL, non-polar lipid; OD, optical density; PC, 45 phosphatidylcholine; PCA, principal component analysis; PC1, principal component one; 46 PC2, principal component two; PE, phosphatidylethanolamine; PG, phosphatidylglycerol; PI, 1 47 phosphatidylinositol; PL, phospholipid; POC, particulate organic carbon; PS, 48 phosphatidylserine; PUFA, polyunsaturated fatty acid; SFA, saturated fatty acid; SQDG, 49 sulfoquinovosyldiacylglycerol; TLC, thin-layer chromatography 50 Provisional 2 51 Introduction 52 53 Fatty acids (FA) are major components of most of the important lipids in eukaryotic 54 organisms. There are two major divisions of lipids: non-polar lipids and polar lipids. Non- 55 polar lipids (NL) for the most part consist of triacylglycerols and wax esters; the main energy 56 storage molecules of aquatic organisms. The most important polar lipids of phytoplankton are 57 structural components of cell membranes and include, phospholipids (PL), glycolipids (GL) 58 and betaine lipids. PL are predominantly found in non-chloroplast membranes (plasma 59 membrane, endoplasmic reticulum, etc.), whereas GL are typical constituents of chloroplast 60 thylakoid membranes (Guschina and Harwood 2009). Betaine lipids are common in algae and 61 lower plants and have been observed in plasma and chloroplast membranes (Sato 1992, Haigh 62 et al. 1996). Not much is known about their function, but, like PL, they seem to be structural 63 components of membranes and it has been tentatively suggested that, unlike PL, they might 64 not be affected by light intensity (Khotimchenko and Yakovleva 2004). Apart from their 65 structural role, FA and their associated lipids are also important functional molecules. For 66 example, they are involved in signal transduction (Sumida et al. 1993) and in photosynthesis 67 (SukenikProvisional et al. 1989; Harwood and Jones 1989; Jordan et al. 2001; Dörmann and Benning 68 2002; Jones 2007). FA composition of the different lipid classes varies with species and with 69 environmental conditions. These variations in biochemical composition allow algae to survive 70 as environmental conditions change. 71 It has been shown that the lipid structure of thylakoid membranes plays a central role 72 for the organisation of the light harvesting complex and the photosynthetic performance of 73 algae (Pronina et al. 1998; Goss and Wilhelm 2009; Schaller et al. 2011). In addition to the 74 lipid class itself, the FA composition within each lipid class is also important (Li et al. 2012); 75 polyunsaturated fatty acids (PUFA) are important in adjusting membrane fluidity and with it 3 76 the electron flow between electron acceptors of photosystem II (Horvath et al. 1987; Mock 77 and Kroon 2002; Guiheneuf et al. 2009). In photosynthetically active membranes, there are 78 two compositional responses (with respect to FA) to light that act in opposite directions. 79 Under low light acclimation higher proportions of PUFA reflect an increase in thylakoid 80 membrane stacking (see e.g. Richardson et al. 1983; Neal and Melis 1986; Sakshaug et al. 81 1997), whereas lower proportions of PUFA are associated with a decrease of proton leakage 82 to reduce metabolic costs (Raven et al. 2000; Quigg et al. 2006). 83 Elucidating the general mechanisms underlying the biochemical adaptations made by 84 algae in response to changing environmental conditions is important in order that we might be 85 in a better position to predict variation in algal food quantity and quality in aquatic food webs 86 experiencing extensive impacts of anthropogenic eutrophication (Schindler 2012) and climate 87 change (Fuschino et al. 2011). This is particularly important in estimating potential effects of 88 these global drivers on biodiversity because different phytoplankton species occupy distinct 89 physico-chemical niches allowing for higher resource use efficiency (Striebel et al. 2009). 90 Thereby species-specific responses of phytoplankton in response to fluctuations in their 91 immediate environment have to be quantified and characterized. For example, representatives 92 of theProvisional Chlorophyceae, Cryptophyceae and Mediophyceae, all of which are important 93 components of plankton communities in temperate lakes, showed different photosynthetic 94 acclimation strategies to changing abiotic environmental conditions such as phosphorus 95 availability and light intensity (Wacker et al. 2015a). Second, phytoplankton species have 96 been shown to be highly variable with respect to their FA composition and sterols when 97 nutrient concentration, light intensity and temperature fluctuate (Piepho et al. 2010, 2012ab). 98 Consequently, changing environmental conditions may cause alterations in relative 99 availabilities of mineral and biochemicals
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