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Heterotrophic Cultivation of Microalgae As a Source of Docosahexaenoic Acid for Aquaculture

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Heterotrophic Cultivation of Microalgae As a Source of Docosahexaenoic Acid for Aquaculture Heterotrophic cultivation of microalgae as a source of docosahexaenoic acid for aquaculture ENEKO GANUZA TABERNA Grupo de Investigaci´onen Acuicultura Intituto Canario de Ciencias Marinas Universidad de Las Palmas de Gran Canaria (IUSA) Being a thesis submitted for the degree of Doctor of Phylosophy in the University of Las Palmas de Gran Canaria, 2008 Directors: Prof. Marisol Izquierdo & Prof. Colin Ratledge El haber nacido cerca del mar me gusta, me ha parecido siempre como un augurio de libertad y cambio... Pio Baroja Contents List of tables III List of figures V List of abbreviations VII Acknowledgements IX 1. General introduction1 1.1. Lipids and their role in living organisms............1 1.2. Lipid biochemistry........................3 1.3. Importance of HUFA for marine finfish.............6 1.4. Importance of HUFA for human health.............9 1.5. Fish oil as a source of HUFA................... 10 1.6. Single cell oils as source of HUFA................ 12 1.7. DHA-producing microorganisms................. 14 1.8. HUFA producing microorganisms in aquaculture........ 19 1.9. Gilthead seabream as a model to study the effect of hetero- trophic organisms as a source of HUFA............. 20 1.10. Objectives............................. 21 2. General materials and methods 39 2.1. Microbial cultures......................... 39 2.2. Rotifers.............................. 45 2.3. Experimental microdiets..................... 45 2.4. Gilthead seabream larviculture.................. 48 3. Lipid accumulation in Schizochytrium G13/2S produced in continuous culture 53 4. The influence of air supply on fatty acid production by Schi- zochytrium G13/2S and Crypthecodinium cohnii 67 5. Restriction in propionic acid precursors inhibits odd-chain fatty acid synthesis in Schizochytrium G13/2S 79 i Contents 6. High-cell-density cultivation of Schizochytrium G13/2S in an ammonium/pH-auxostat fed-batch system 87 7. Docosahexaenoic acid production by Crypthecodinium coh- nii grown in an ethanol fed-batch system 99 8. Crypthecodinium cohnii and Schizochytrium sp. as poten- tial substitutes to fisheries-derived oils in seabream (Sparus aurata) microdiets 109 9. General conclusions 127 10.Summary 129 10.1. Summary............................. 129 10.2. Resumen.............................. 130 10.3. Laburpena............................. 132 11.Resumen ampliado 135 11.1. Introducci´ongeneral....................... 135 11.2. Objetivos............................. 153 11.3. Materiales y m´etodos generales................. 154 11.4. Discusi´on............................. 154 List of publications 187 Curriculum vitae 189 II List of Tables 1.1. Fatty acid production by oleaginous microorganisms...... 13 3.1. Nitrogen source concentration in continuous culture...... 58 3.2. Carbon source concentration in continuous culture....... 60 3.3. Schizochytrium: batch vs. continuous culture.......... 63 4.1. Air supply in Schizochytrium G13/2S fatty acid profile.... 71 4.2. N2-atmosphere in Schizochytrium G13/2S fatty acid profile.. 72 4.3. Air supply in Crypthecodinium cohnii fatty acid profile.... 73 4.4. N2-atmosphere in Crypthecodinium cohnii fatty acid profile.. 74 5.1. Nitrogen source induces odd-chain fatty acid production... 82 6.1. Optimum ammonium concentration............... 91 6.2. Fatty acid profile in a NH4/pH-auxostat fermentation..... 94 7.1. Fatty acid profile in an ethanol fed-batch fermentation.... 105 7.2. C. cohnii: acetic acid vs. ethanol................ 106 8.1. Dietary formulation and proximate composition........ 112 8.2. Dietary fatty acid composition.................. 113 8.3. Larval fatty acid composition.................. 119 11.1. Fuentes microbianas de ´acidosgrasos.............. 147 11.2. Schizochytrium: cultivo tipo \batch" vs. continuo....... 156 11.3. C. cohnii: ´acidoac´etico vs. etanol................ 163 iii List of Tables IV List of Figures 1.1. Docosahexaenoic acid (DHA; 22:6 n-3).............2 1.2. DHA biosynthesis.........................5 1.3. Fish oil price........................... 11 1.4. Biochemistry of lipid accumulation............... 15 1.5. Fermentation facilities...................... 16 1.6. Microphotographs of DHA producing microorganisms..... 18 1.7. Gilthead seabream global production.............. 21 3.1. Growth-associated lipid accumulation in batch culture.... 57 3.2. Carbon source limited batch culture............... 59 3.3. Dilution rate in continuous culture............... 61 4.1. Anaerobic culture......................... 72 5.1. Fatty acid GC chromatograms.................. 83 6.1. Optimum glucose concentration................. 91 6.2. NH4/pH-auxostat fermentation................. 93 7.1. Ethanol fed-batch fermentation................. 103 7.2. O2 enrichment in an ethanol fed-batch fermentation...... 104 8.1. Overall survival and survival to air-exposure of larvae..... 117 8.2. Larval growth........................... 118 v List of Figures VI List of abbreviations ABTS 2,2'-azino-bis(3-ethylbenzthiazoline-6-sulphonic acid) AMP Adenosine monophosphate ARA Arachidonic acid (20:4 n-6) ATP Adenosine triphosphate ATTC American type culture collection CCMP Culture collection marine phytoplankton CDW Cell dry weight D Dilution rate DGLA Dihomogammalinolenic acid (20:3 n-6) DHA Docosahexaenoic acid (22:6 n-3) DPA-3 Docosapentaenoic acid (22:5 n-3) DPA-6 Docosapentaenoic acid (22:5 n-6) EDTA Ethylenediamine tetraacetic acid EFA Essential fatty acids EPA Eicosapentaenoic acid (20:5 n-3) FA Fatty acid FAME Fatty acid methyl esters FAS Fatty acid synthase GC Gas cromatography GLA γ-linolenic acid (18:3 n-6) GRAS Generally recognized as safe HUFA Highly unsaturated fatty acids LA Linoleic acid LNA α-linolenic acid (18:3 n-3) MOPS 3-(N-morpholino)propanesulfonic acid NADH Nicotinamide adenine dinucleotide NADPH Nicotinamide adenine dinucleotide phosphate OA Oleic acid (19:1 n-9) OCFA Odd chain fatty acids PC Phosphatidylcholine PE Phosphatidylethanolamine PI Phosphatidylinositol PKS Polyketide synthase PUFA Polyunsaturated fatty acids List of abbreviations −1 −1 rCDW Biomass volumetric productivity (g l h ) −1 −1 rDHA DHA volumetric productivity (mg DHA l h ) −1 −1 rFA Fatty acid volumetric productivity (mg FA l h ) rpm Revolutions per minute SCO Single cell oils SEM Standard error of the mean TFA Total fatty acids TRIS Trishydroxymethylaminomethane −1 −1 µDHA Specific rate of DHA formation (mg DHA g CDW h ) µmax Maximum specific growth rate VIII Acknowledgements Acknowledgements The following PHD thesis was made un- der the financial support from Tom´asde Zarate scholarship from Cabildo de Gran Canaria. I would like to thank my supervisor, Prof Marisol Izquierdo, for making this possible, for her scientific, moral and professional support at all times. I am also very thankful my co-supervisor, Prof Colin Ratledge, for his scientific excellence, his comments and expertise taught to me through- out these years. To Dr Alistair Anderson I am especially grateful for initiating me on the scientific methodology. I am most grateful for the Britishness, along with many other valuable contributions made to the present thesis by my very friend Elisa. I am grateful to the Instituto Canario de Ciencias Marinas, Universidad de Las Palmas de Gran Canaria and The University of Hull for hosting me and nesting this research. Also, I would like to thank the staff of the Lipid Research Centre and Grupo de Investigaci´onen Acuicultura for their collaboration. In particular, Rachid and Orestes showed me how to calm down and channel my scientific restlessness. Eduardo opened in me a new interest in IT, including Latex and Mac refinement. Joaquin has made the elegant covers I was missing. Simon showed me the art of fermentation. I would like to thank Steven for the English corrections. Juan showed me how to write back in Span- ish. Gorka helped me with the bureaucratic matters. Ms. Watford, Carmen, Debbie and Val showed me how to hold the pipete. Nivedita, Cath, Veena, Isabel and The Neibor showed me to wisely wait for my results. Ms Kennedy helped me with the elementary analysis. Tibi and Eyad have been close to my fish larvae. Elena, Lorena, Tache, Luis, Noe, Chano, Javi, Egoi, Maite, Raphaele helped me by listening to the presentation of my results. I would like to thank different anonymous reviewers for opening a debate on the subject. I would also like to thank Geert, Guido and Guillermo and for the time they gave me to finish the dissertation. I would like to thank Lolke, Juan Luis, Arnaud, Hector, Ricardo for their comments to this thesis. Finally, my family showed me the Vito’s way and overall I am grateful to this place, the Canaries. Chapter 1 General introduction 1.1. Lipids and their role in living organisms Lipids are a group of organic compounds that are insoluble in water, but soluble in organic solvents. Although there is not a structural definition, many lipids, namely those saponifiable, contain fatty acids, hydrocarbon chains with a carboxylic group at one end and a terminal methyl group at the other (n or ! carbon). The acyl chain may be saturated or unsaturated. The fatty acids commonly found in biological tissues possess an even-numbered carbon chain of between 12 and 24 atoms and 0 to 6 methylene-interrupted double bonds or unsaturations. Being a heterogeneous and wide group of compounds, different classifi- cations of lipids are currently used. For instance, according to their degree of polarity, they are known as polar or neutral lipids. The latter include fatty acids and their derivative glycerolipids, sterols, waxes and tocopherols,
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