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Polar Lipids Analysis of Cultured Phytoplankton Reveals Significant Inter-taxa Changes, Low Influence of Growth Stage, and Usefulness in Chemotaxonomy

  • Microbiology of Aquatic Systems
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Abstract

The high lipid diversity of microalgae has been used to taxonomically differentiate phytoplankton taxa at the class level. However, important lipids such as phospholipids (PL) and betaine lipids (BL) with potential chemotaxonomy application in phytoplankton ecology have been scarcely studied. The chemotaxonomy value of PL and BL depends on their intraspecific extent of variation as microalgae respond to external changing factors. To determine such effects, lipid class changes occurring at different growth stages in 15 microalgae from ten different classes were analyzed. BL occurred in 14 species and were the less affected lipids by growth stage with diacylglyceryl-hydroxymethyl-N,N,N-trimethyl-b-alanine (DGTA) showing the highest stability. PL were more influenced by growth stage with phosphatidylcholine (PC), phosphatidylglycerol (PG), and phosphatidyletanolamine (PE) declining towards older culture stages in some species. Glycolipids were the more common lipids, and no evident age-related variability pattern could be associated to taxonomic diversity. Selecting BL and PL as descriptor variables optimally distinguished microalgae taxonomic variability at all growth stages. Principal coordinate analysis arranged species through a main tendency from diacylglyceryl-hydroxymethyl-N,N,N-trimethyl-b-alanine (DGCC) containing species (mainly dinoflagellates and haptophytes) to DGTA or PC containing species (mainly cryptophytes). Two diatom classes with similar fatty acid profiles could be distinguished from their respective content in DGTA (Bacillariophyceae) or DGCC (Mediophyceae). In green lineage classes (Trebouxiophyceae, Porphyridophyceae, and Chlorodendrophyceae), PC was a better descriptor than BL. BL and PL explained a higher proportion of microalgae taxonomic variation than did fatty acids and played a complementary role as lipid markers.

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References

  1. Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45:160–186

    Article  CAS  PubMed  Google Scholar 

  2. Goss R, Wilhelm C (2009) Lipids in algae, lichens and mosses. In: Wada H, Murata N (eds) Lipids in photosynthesis: essential and regulatory functions. Springer, Dordrecht, pp 117–137

    Chapter  Google Scholar 

  3. Kumari P, Kumar M, Reddy CRK, Jha B (2013) Algal lipids, fatty acids and sterols. In: Functional Ingredients from Algae for Foods and Nutraceuticals. In: Dominguez H (ed) Woodhead Publishing Series in Food Science, Technology and Nutrition. Pp 87–134

  4. Volkman JK (2006) Lipid markers for marine organic matter. The handbook of environmental chemistry, vol 2N. Springer, Berlin, pp 27–70

    Google Scholar 

  5. 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 11:124–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Galloway AWE, Winder M (2015) Partitioning the relative importance of phylogeny and environmental conditions on phytoplankton fatty acids. PLoS One 10(6):e0130053. doi:10.1371/journal.pone.0130053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Taipale SJ, Hiltunen M, Vuorio K, Peltomaa E (2016) Suitability of phytosterols alongside fatty acids as chemotaxonomic biomarkers for phytoplankton. Front Plant Sci 7:212. doi:10.3389/fpls.2016.00212

    Article  PubMed  PubMed Central  Google Scholar 

  8. Volkman JK (2003) Sterols in microorganisms. Appl Microbiol Biotechnol 60:495–506

    Article  CAS  PubMed  Google Scholar 

  9. Wolhowe MD, Prahl FG, White AE, Popp BN, Rosas-Navarro A (2014) A biomarker perspective on coccolithophorid growth and export in a stratified sea. Prog Oceanogr 122:65–76

    Article  Google Scholar 

  10. Schubotz F, Wakeham SG, Lipp JS, Fredricks HF, Hinrichs KU (2009) Detection of microbial biomass by intact polar membrane lipid analysis in the water column and surface sediments of the Black Sea. Environ Microbiol 11:2720–2734

    Article  CAS  PubMed  Google Scholar 

  11. Van Mooy BAS, Fredricks HF (2010) Bacterial and eukaryotic intact polar lipids in the eastern subtropical South Pacific: water-column distribution, planktonic sources, and fatty acid composition. Geochim Cosmochim Acta 74(22):6499–6516

    Article  CAS  Google Scholar 

  12. Popendorf KJ, Lomas MW, Van Mooy BAS (2011) Microbial sources of intact polar diacylglycerolipids in the Western North-Atlantic Ocean. Org Geochem 42(7):803–811

    Article  CAS  Google Scholar 

  13. Popendorf KJ, Tanaka T, Pujo-Pay M, Lagaria A, Courties C, Conan P, Oriol L, Sofen LE, Moutin T, Van Mooy BAS (2011) Gradients in intact polar diacylglycerolipids across the Mediterranean Sea are related to phosphate availability. Biogeosciences 8:3733–3745

    Article  CAS  Google Scholar 

  14. Brandsma J, Hopmans EC, Philippart JM, Veldhuis MJW, Schouten S, Sinninghe Damsté JS (2012) Low temporal variation in the intact polar lipid composition of North Sea coastal marine water reveals limited chemotaxonomic value. Biogeosciences 9:1073–1084

    Article  CAS  Google Scholar 

  15. Brandsma J, Hopmans EC, Brussaard CPD, Witte HJ, Schouten S, Damste JSS (2012) Spatial distribution of intact polar lipids in North Sea surface waters: relationship with environmental conditions and microbial community composition. Limnol Oceanogr 57(4):959–973

    Article  CAS  Google Scholar 

  16. Goutx M, Guigue C, Aritio D, Ghiglione JF, Pujo-Pay M, Raybaud V, Duflos M, Prieur L (2009) Short term summer to autumn variability of dissolved lipid classes in the Ligurian sea (NW Mediterranean). Biogeosciences 6:1229–1246

    Article  CAS  Google Scholar 

  17. Gasparovic B, Frka S, Koch BP, Zhu ZY, Bracher A, Lechtenfeld OJ, Neogi SB, Lara RJ, Kattner G (2014) Factors influencing particulate lipid production in the East Atlantic Ocean. Deep-Sea Res I Oceanogr Res Pap 89:56–67

    Article  CAS  Google Scholar 

  18. White DA, Widdicombe CE, Somerfield PJ, Airs RL, Tarran GA, Maud JL, Atkinson A (2015) The combined effects of seasonal community succession and adaptive algal physiology on lipid profiles of coastal phytoplankton in the Western English Channel. Mar Chem 177:638–652

    Article  CAS  Google Scholar 

  19. Volkman JK, Jeffrey SW, Nichols PD, Rogers GI, Garland CD (1989) Fatty acid and lipid composition of 10 species of microalgae used in mariculture. J Exp Mar Biol Ecol 128:219–240

    Article  CAS  Google Scholar 

  20. Dunstan GA, Volkman JK, Jeffrey SW, Barrett SM (1992) Biochemical composition of microalgae from the green algal classes Chlorophyceae and Prasinophyceae. 2. Lipid classes and fatty acids. J Exp Mar Biol Ecol 161:115–134

    Article  CAS  Google Scholar 

  21. Lombardi AT, Wangersky PJ (1995) Particulate lipid class composition of three marine phytoplankters Chaetoceros gracilis, Isochrysis galbana (Tahiti) and Dunaliella tertiolecta grown in batch culture. Hydrobiologia 306:1–6

    Article  CAS  Google Scholar 

  22. Guihéneuf F, Mimouni V, Ulmann L, Tremblin G (2009) Combined effects of irradiance level and carbon source on fatty acid and lipid class composition in the microalga Pavlova lutheri commonly used in mariculture. J Exp Mar Biol Ecol 369:136–143

    Article  CAS  Google Scholar 

  23. Miller MR, Quek SY, Staehler K, Nalder T, Packer MA (2014) Changes in oil content, lipid class and fatty acid composition of the microalga Chaetoceros calcitrans over different phases of batch culture. Aquac Res 45:1634–1647

    Article  CAS  Google Scholar 

  24. Guschina IA, Harwood JL (2009) Algal lipids and effect of the environment on their biochemistry. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, Dordrecht, pp 1–24

    Chapter  Google Scholar 

  25. Gong Y, Guo X, Wan X, Liang Z, Jiang M (2012) Triacylglycerol accumulation and change in fatty acid content of four marine oleaginous microalgae under nutrient limitation and at different culture ages. J Basic Microbiol 53:29–36

    Article  PubMed  CAS  Google Scholar 

  26. Su XL, Xu JL, Yan XJ, Zhao P, Chen JJ, Zhou CX, Zhao F, Li S (2013) Lipidomic changes during different growth stages of Nitzschia closterium f. minutissima. Metabolomics 9:300–310

    Article  CAS  Google Scholar 

  27. Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226

    Article  CAS  PubMed  Google Scholar 

  28. Klok AJ, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2014) Edible oils from microalgae: insights in TAG accumulation. Trends Biotechnol 32:521–528

    Article  CAS  PubMed  Google Scholar 

  29. Dembitsky VM (1996) Betaine ether-linked glycerolipids: chemistry and biology. Prog Lipid Res 35:1–51

    Article  CAS  PubMed  Google Scholar 

  30. Armada I, Hachero-Cruzado I, Mazuelos N, Ríos JL, Manchado M, Cañavate JP (2013) Differences in betaine lipids and fatty acids between Pseudoisochrysis paradoxa VLP and Diacronema vlkianum VLP isolates (Haptophyta). Phytochemistry 95:224–233

    Article  CAS  PubMed  Google Scholar 

  31. Banskota AH, Stefanova R, Sperker S, McGinn PJ (2013) New diacylglyceryltrimethylhomoserines from the marine microalga Nannochloropsis granulata and their nitric oxide inhibitory activity. J Appl Phycol 25:1513–1525

    Article  CAS  Google Scholar 

  32. Leblond JD, Dahmen AS, Dodson VJ, Dahmen JL (2013) Characterization of the Betaine Lipids, Diacylglyceryl-N, N, N-trimethylhomoserine (DGTS) and Diaclyglycerylhydroxymethyl-N, N, N-trimethyl-β-alanine (DGTA), in Brown-and Green-Pigmented Raphidophytes. Algol Stud 142:17–28

    Article  CAS  Google Scholar 

  33. Anesi A, Guella G (2015) A fast liquid chromatography-mass spectrometry methodology for membrane lipid profiling through hydrophilic interaction liquid chromatography. J Chromatogr A 1384:44–52

    Article  CAS  PubMed  Google Scholar 

  34. Canavate JP, Armada I, Ríos JL, Hachero-Cruzado I (2016) Exploring occurrence and molecular diversity of betaine lipids across taxonomy of marine microalgae. Phytochemistry 124:68–78

    Article  CAS  PubMed  Google Scholar 

  35. Martin P, Van Mooy BAS, Heithoff A, Dyhrman ST (2011) Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana. ISME J 5:1057–1060

    Article  CAS  PubMed  Google Scholar 

  36. Van Mooy BAS, Fredricks HF, Pedler BE, Dyhrman ST, Karl DM, Koblizek M, Lomas MW, Mincer TJ, Moore LR, Moutin T, Rappé MS, Webb EA (2009) Phytoplankton in the ocean use non-phosphorus lipids in response to phosphorus scarcity. Nature 458:69–72

    Article  PubMed  CAS  Google Scholar 

  37. Abida H, Dolch L-J, Meï C, Villanova V, Conte M, Block MA, Finazzi G, Bastien O, Tirichine L, Bowler C, Rébeillé F, Petroutsos D, Jouhet J, Maréchal E (2015) Membrane glycerolipid remodelling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol 167:118–136

    Article  CAS  PubMed  Google Scholar 

  38. Guiry MD (2012) How many species of algae are there? J Phycol 48:1057–1063

    Article  PubMed  Google Scholar 

  39. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Book Publ. Corp, New York, pp 29–60

    Chapter  Google Scholar 

  40. Nichols BW (1963) Separation of the lipids of photosynthetic tissues: improvements in analysis by thin layer chromatography. Biochim Biophys Acta 70:417–422

    Article  CAS  PubMed  Google Scholar 

  41. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  42. Mock T, Kroon BMA (2002) Photosynthetic energy conversion under extreme conditions. I. Important role of lipids as structural modulators and energy sink under N-limited growth in Antarctic sea ice diatoms. Phytochemistry 61:41–51

    Article  CAS  PubMed  Google Scholar 

  43. Olsen RE, Henderson RJ (1989) The rapid analysis of neutral and polar marine lipids using double-development HPTLC and scanning densitometry. J Exp Mar Biol Ecol 129:189–197

    Article  CAS  Google Scholar 

  44. Vieler A, Wilhelm C, Goss R, Süß R, Schiller J (2007) The lipid composition of the unicellular green alga Chlamydomonas reinhardtii and the diatom Cyclotella meneghiniana investigated by MALDI-TOF and TLC. Chem Phys Lipids 150:143–55

    Article  CAS  PubMed  Google Scholar 

  45. Christie WW (2003) Lipid analysis: isolation, separation, identification and structural analysis of lipids. In: Christie WW (ed) The Oily Press: Bridgewater, England

  46. Eltgroth ML, Watwood RL, Wolfe GV (2005) Production and cellular localization of neutral long-chain lipids in the Haptophyte algae Isochrysis galbana and Emiliania huxleyi. J Phycol 41:1000–1009

    Article  CAS  Google Scholar 

  47. Dittmer JC, Lester RL (1964) A simple specific spray for the detection of phospholipids on thin-layer chromatograms. J Lipid Res 5:126–127

    CAS  PubMed  Google Scholar 

  48. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  49. Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth, p 192

    Google Scholar 

  50. Clarke KR, Warwick RM (2001) Change in marine communities. An approach to statistical analyses and interpretation, 2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  51. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  52. Martin GJO, Hill DRA, Olmstead ILD, Bergamin A, Shears MJ, Dias DA, Kentish SE, Scales PJ, Botté CY, Callahan DL (2014) Lipid profile remodelling in response to nitrogen deprivation in the microalgae Chlorella sp. (Trebouxiophyceae) and Nannochloropsis sp. (Eustigmatophyceae). PLoS One 9(8):e103389. doi:10.1371/journal.pone.0103389

    Article  PubMed  PubMed Central  Google Scholar 

  53. Weber N, Bergenthal D, Kokate CK, Mangold HK (1989) Biologically active ether lipids: incorporation of long-chain precursors into 1(3),2-diacylglycero-3(1)-O-4′-(N, N, N- trimethyl)homoserines and other lipids of Chlorella fusca. J Lipid Mediat 1:37–48

    CAS  PubMed  Google Scholar 

  54. Li S, Xu J, Chen J, Chen JJ, Zhou C, Yan X (2014) The major lipid changes of some important diet microalgae during the entire growth phase. Aquaculture 428–429:104–110

    Article  CAS  Google Scholar 

  55. Bigogno C, Khozin-Goldberg I, Boussiba S, Vonshak A, Cohen Z (2002) Lipid and fatty acid composition of the green oleaginous alga Parietochloris incisa, the richest plant source of arachidonic acid. Phytochemistry 60:497–503

    Article  CAS  PubMed  Google Scholar 

  56. Kim SH, Liu KH, Lee SY, Hong SJ, Cho BK, Lee H, Lee CG, Choi HK (2013) Effects of light intensity and nitrogen starvation on glycerolipid, glycerophospholipid, and carotenoid composition in Dunaliella tertiolecta culture. PLoS One 8(9):e72415. doi:10.1371/journal.pone.0072415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Maat DS, Bale NJ, Hopmans EC, Damsté JSS, Schouten S, Brussaard CPD (2016) Increasing P-stress and viral infection impact lipid remodelling of the picophytoplankter Micromonas pusilla. Biogeosciences 13:1667–1676

    Article  Google Scholar 

  58. Pal D, Khozin-Goldberg I, Didi-Cohen S, Solovchenko A, Batushansky A, Kaye Y, Sikron N, Samani T, Fait A, Boussiba S (2013) Growth, lipid production and metabolic adjustments in the euryhaline eustigmatophyte Nannochloropsis oceanica CCALA 804 in response to osmotic downshift. Appl Microbiol Biotechnol 97:8291–8306

    Article  CAS  PubMed  Google Scholar 

  59. Haigh WG, Yoder TF, Ericson L, Pratum T, Winget RR (1996) The characterisation and cyclic production of a highly unsaturated homoserine lipid in Chlorella minutissima. Biochim Biophys Acta 1299:183–190

    Article  PubMed  Google Scholar 

  60. Gladu PK, Patterson GW, Wikfors GH, Smith BC (1995) Sterol, fatty acid, and pigment characteristics of Utex 2341, a marine Eustigmatophyte identified previously as Chlorella minutissima (Chlorophyceae). J Phycol 31:774–777

    Article  CAS  Google Scholar 

  61. Zhu CJ, Lee YK, Chao TM (1997) Effects of temperature and growth phase on lipid and biochemical composition of Isochrysis galbana TK1. J Appl Phycol 9:451–457

    Article  CAS  Google Scholar 

  62. Kato M, Sakai M, Adachi K, Ikemoto H, Sano H (1996) Distribution of betaine lipids in marine algae. Phytochemistry 42:1341–1345

    Article  CAS  Google Scholar 

  63. Eichenberger W, Gfeller H, Grel P, Gribi C, Henderson RJ (1996) Gas chromatographic-mass spectrometric identification of betaine lipids in Chroomonas salina. Phytochemistry 42:967–972

    Article  CAS  Google Scholar 

  64. Dyhrman ST, Jenkins BD, Rynearson TA, Saito MA, Mercier ML, Alexander H, Whitney LP, Drzewianowski A, Bulygin VV, Bertrand EM, Wu Z, Benitez-Nelson C, Heithoff A (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One 7(3):e33768. doi:10.1371/journal.pone.0033768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Flaim G, Obertegger U, Anesi A, Guella G (2014) Temperature-induced changes in lipid biomarkers and mycosporine-like amino acids in the psychrophilic dinoflagellate Peridinium aciculiferum. Freshw Biol 59:985–97

    Article  CAS  Google Scholar 

  66. Leblond JD, Khadka M, Duong L, Dahmen JL (2015) Squishy lipids: temperature effects on the betaine and galactolipid profiles of a C18/C18 peridinin-containing dinoflagellate, Symbiodinium microadriaticum (Dinophyceae), isolated from the mangrove jellyfish, Cassiopea xamachana. Phycol Res 63:219–230

    Article  CAS  Google Scholar 

  67. Guedes AC, Meireles LA, Amaro HM, Malcata FX (2010) Changes in lipid class and fatty acid composition of cultures of Pavlova lutheri, in response to right intensity. J Am Oil Chem Soc 87:791–801

    Article  CAS  Google Scholar 

  68. Eichenberger W, Gribi C (1997) Lipids of Pavlova lutheri: cellular site and metabolic role of DGCC. Phytochemistry 45:1561–1567

    Article  CAS  Google Scholar 

  69. Jouhet J, Maréhal E, Block MA (2007) Glycerolipid transfer for the building of membranes in plant cells. Prog Lipid Res 46:37–55

    Article  CAS  PubMed  Google Scholar 

  70. Boudière L, Michaud M, Petroutsos D, Rébeillé P, Falconet D, Bastien O, Roy S, Finazzi G, Rolland N, Jouhet J, Block MA, Maréchal E (2014) Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim Biophys Acta 1837:470–480

    Article  PubMed  CAS  Google Scholar 

  71. Petroutsos D, Amiar S, Abida H, Dolch LJ, Bastien O, Rébeillé F, Jouhet J, Falconet D, Block MA, McFadden GI, Bowler C, Botté C, Maréchal E (2014) Evolution of galactoglycerolipid biosynthetic pathways—from cyanobacteria to primary plastids and from primary to secondary plastids. Prog Lipid Res 54:68–85

    Article  CAS  PubMed  Google Scholar 

  72. Arakaki A, Iwama D, Liang Y, Murakami N, Ishikura M, Tanaka T, Matsunaga T (2013) Glycosylceramides from marine green microalga Tetraselmis sp. Phyochemistry 85:107–114

    Article  CAS  Google Scholar 

  73. Fulton JM, Fredricks HF, Bidle KD, Vardi A, Kendrick BJ, DiTullio GR, Van Moy BAS (2014) Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ Microbiol 16:1137–1149

    Article  CAS  PubMed  Google Scholar 

  74. Parrish CC, Wells JS, Yang Z, Dabinett P (1998) Growth and lipid composition of scallop juveniles, Placopecten magellanicus, fed the flagellate Isochrysis galbana with varying lipid composition and the diatom Chaetoceros muelleri. Mar Biol 133:461–471

    Article  Google Scholar 

  75. Epstein BL, D’Hondt S, Hargraves PE (2001) The possible metabolic role of C37 alkenones in Emiliania huxleyi. Org Geochem 32:867–875

    Article  CAS  Google Scholar 

  76. Fábregas J, Arán J, Morales ED, Lamela T, Otero A (1997) Modification of sterol concentration in marine microalgae. Phytochemistry 46:1189–1191

    Article  Google Scholar 

  77. Ballantine JA, Lavis A, Morris RJ (1979) Sterols of phytoplankton-effects of illumination and growth stage. Phytochemistry 18:1459–66

    Article  CAS  Google Scholar 

  78. Mansour MP, Volkman JK, Blackburn SI (2003) The effect of growth phase on the lipid class, fatty acid and sterol composition in the marine dinoflagellate, Gymnodinium sp. in batch culture. Phytochemistry 63:145–153

    Article  CAS  PubMed  Google Scholar 

  79. Piepho M, Martin-Creuzburg D, Wacker A (2010) Simultaneous effects of light intensity and phosphorus supply on the sterol content of phytoplankton. PLoS One 5(12):e15828. doi:10.1371/journal.pone.0015828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Xu Z, Yan X, Pei L, Luo Q, Xu J (2008) Changes in fatty acids and sterols during batch growth of Pavlova viridis in photobioreactor. J Appl Phycol 20:237–243

    Article  CAS  Google Scholar 

  81. Ahmed F, Zhou W, Schenk PM (2015) Pavlova lutheri is a high-level producer of phytosterols. Algal Res 10:210–217

    Article  Google Scholar 

  82. Véron B, Dauguet JC, Billard C (1998) Sterolic biomarkers in marine phytoplankton. II. Free and conjugated sterols of seven species used in mariculture. J Phycol 34:273–279

    Article  Google Scholar 

  83. López-Alonso D, Belarbi EH, Fernandez-Sevilla JM, Rodriguez-Ruiz J, Molina-Grima E (2000) Acyl lipid composition variation related to culture age and nitrogen concentration in continuous culture of the microalga Phaeodactylum tricornutum. Phytochemistry 54:461–471

    Article  Google Scholar 

  84. 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 54:621–639

    Article  CAS  PubMed  Google Scholar 

  85. Van Mooy BAS, Moutin T, Duhamel S, Rimmelin P, Van Wambeke F (2008) Phospholipid synthesis rates in the eastern subtropical South Pacific Ocean. Biogeosciences 5:133–139

    Article  Google Scholar 

  86. Sato N (1992) Betaine lipids. J Plant Res 105:185–197

    CAS  Google Scholar 

  87. Sakurai K, Mori N, Sato N (2014) Detection and characterization of phosphatidylcholine in various strains of the genus Chlamydomonas (Volvocales, Chlorophyceae). J Plant Res 127:641–650

    Article  CAS  PubMed  Google Scholar 

  88. Schneider JC, Roessler P (1994) Radiolabeling studies of lipids and fatty acids in Nannochloropsis (Eustigmatophyceae), an oleaginous marine alga. J Phycol 30:594–598

    Article  CAS  Google Scholar 

  89. Llewellyn CA, Sommer U, Dupont CL, Allen AE, Viant MR (2015) Using community metabolomics as a new approach to discriminate marine microbial particulate organic matter in the western English Channel. Prog Oceanogr 137:421–433

    Article  Google Scholar 

  90. Theriot EC, Ashworth M, Ruck E, Nakov T, Jansen RK (2010) A preliminary multigene phylogeny of the diatoms (Bacillariophyta): challenges for future research. Plant Ecol Evol 143:278–296

    Article  Google Scholar 

  91. Smith SR, Abbriano RM, Hildebrand M (2012) Comparative analysis of diatom genomes reveals substantial differences in the organization of carbon partitioning pathways. Algal Res 1:2–16

    Article  CAS  Google Scholar 

  92. Parker MS, Mock T, Armbrust EV (2008) Genomic insights into marine microalgae. Annu Rev Genet 42:619–645

    Article  CAS  PubMed  Google Scholar 

  93. Wang D, Ning K, Li J, Hu J, Han D, Wang H, Zeng X, Jing X, Zhou Q, Su X, Chang X, Wang A, Wang W, Jia J, Wei L, Xin Y, Qiao Y, Huang R, Chen J, Han B, Yoon K, Hill RT, Zohar Y, Chen F, Hu Q, Xu J (2014) Nannochloropsis genomes reveal evolution of microalgal oleaginous traits. PLoS Genet 10(1):e1004094. doi:10.1371/journal.pgen.1004094

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Fang J, Barcelona MJ, Alvarez PJJ (2000) A direct comparison between fatty acid analysis and intact phospholipid profiling for microbial identification. Org Geochem 31:881–887

    Article  CAS  Google Scholar 

  95. Strandberg U, Taipale SJ, Hiltunen M, Galloway AWE, Brett MT, Kankaala P (2015) Inferring phytoplankton community composition with a fatty acid mixing model. Ecosphere 6:1–18. doi:10.1890/ES14-00382.1

    Article  Google Scholar 

  96. Wright SW, Jeffrey SW (2006) Pigment markers for phytoplankton production. Handb Environ Chem 2:71–104, Part N

    CAS  Google Scholar 

  97. Latasa M (2007) Improving estimations of phytoplankton class abundances using CHEMTAX. Mar Ecol Prog Ser 329:13–21

    Article  Google Scholar 

  98. Mackey MD, Mackey DJ, Higgins HW, Wright SW (1996) CHEMTAX-a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar Ecol Prog Ser 144:265–83

    Article  CAS  Google Scholar 

  99. Carvalho CCR, Caramujo MJ (2014) Fatty acids as a tool to understand microbial diversity and their role in food webs of Mediterranean temporary ponds. Molecules 19:5570–5598

    Article  PubMed  CAS  Google Scholar 

  100. Christodoulou S, Marty JC, Miquel JC, Volkman JK, Rontani JF (2009) Use of lipids and their degradation products as biomarkers for carbon cycling in the northwestern Mediterranean Sea. Mar Chem 113:25–40

    Article  CAS  Google Scholar 

  101. Harvey HR, Macko SA (1997) Kinetics of phytoplankton decay during simulated sedimentation: changes in lipids under oxic and anoxic conditions. Org Geochem 27:129–140

    Article  CAS  Google Scholar 

  102. 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

    Article  Google Scholar 

  103. Higgins HW, Wright SW, Schlüter L (2011) Quantitative interpretation of chemotaxonomic pigment data. In: Roy S, Llewellyn C, Egeland ES, Johnsen G (eds) Phytoplankton pigments-characterization, chemotaxonomy and applications in oceanography. Cambridge University Press, Cambridge, pp 257–313

    Chapter  Google Scholar 

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Acknowledgements

This research was supported by projects “Sustainable and environmentally friendly aquaculture for the Atlantic Region of Europe” (SEAFARE), funded by the European Union Atlantic Area 670 Transnational Programme (2007–2013) through grant no 2009-1/123. I. Hachero-Cruzado was supported by an INIA post-doctoral contract.

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Correspondence to José Pedro Cañavate.

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Figure S1

Summary of HPTLC methods employed for lipid class identification in the studied microalgae. (PDF 2346 kb)

Table S1

Sphingolipid (SL) and glycolipids (SQDG, DGDG, MGDG) content (mg g−1 dry weight) of studied microalgae during exponential (E), late exponential (L) and stationary growth phase in culture. nd: non detected lipid class. (DOCX 118 kb)

Table S2

Neutral lipids (ST, TG, MK, EK, SE) content (mg g−1 dry weight) of studied microalgae during exponential (E), late exponential (L) and stationary growth phase in culture. nd: non detected lipid class. (DOCX 121 kb)

Table S3

Fatty acid content (per cent of total fatty acids) of microalgae harvested during late exponential growth. Values are means ± standard deviation (n = 3). (XLSX 53 kb)

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Cañavate, J.P., Armada, I. & Hachero-Cruzado, I. Polar Lipids Analysis of Cultured Phytoplankton Reveals Significant Inter-taxa Changes, Low Influence of Growth Stage, and Usefulness in Chemotaxonomy. Microb Ecol 73, 755–774 (2017). https://doi.org/10.1007/s00248-016-0893-7

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  • DOI: https://doi.org/10.1007/s00248-016-0893-7

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