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Fatty Acid Oxidizing Enzymes in Lobosphaera Incisa Benjamin Djian

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Fatty Acid Oxidizing Enzymes in Lobosphaera Incisa Benjamin Djian Fatty acid oxidizing enzymes in Lobosphaera incisa Dissertation For the award of the degree “Doctor rerum naturalium” of the Georg-August Universität Göttingen Submitted by Benjamin Djian Born in Marseille Göttingen, 2017 Members of the Examination Board Reviewer 1 Prof. Dr. Ivo Feussner Department for Plant Biochemistry Albrecht-von-Haller-Institute for Plant Sciences University of Göttingen Reviewer 2 Prof. Dr. Ulf Diederichsen Institute of Inorganic Chemistry Department of Organic and Biomolecular Chemistry University of Göttingen Prof. Dr. Franc Meyer Department of Bioinorganic and Metallorganic Chemistry Institute of Inorganic Chemistry University of Göttingen Prof. Dr. Jörg Stülke Department of General Microbiology Institute for Microbiology and Genetics University of Göttingen Prof. Dr. Kai Tittmann Department of Molecular Enzymology Schwann-Schleiden-Forschungszentrum University of Göttingen Prof. Dr. Ralf Ficner Department of Molecular Structural Biology Institute for Microbiology and Genetics University of Göttingen Date of the oral examination: May 3, 2017 i Table of Contents 1. INTRODUCTION .................................................................................... 1 1.1. Some plants and algae accumulate neutral lipids under stress conditions ..................... 2 1.2. Lipids, lead actors of cell compartmenting .................................................................... 7 1.3. Lipoxygenase, a lipid oxidizing enzyme ....................................................................... 8 1.4. Aims of this study ........................................................................................................ 17 2. MATERIAL ............................................................................................ 18 2.1. Equipment .................................................................................................................... 19 2.2. Software ....................................................................................................................... 21 2.3. Medium, buffers and gels ............................................................................................ 22 2.4. Consumables ................................................................................................................ 29 2.5. Primers and vectors ...................................................................................................... 30 2.6. Strains .......................................................................................................................... 31 2.7. Commercially available crystal screens ....................................................................... 32 3. METHODS .............................................................................................. 33 3.1. Molecular biology ........................................................................................................ 34 3.2. Co-expression in onion cells and fluorescence microscopy ........................................ 39 3.3. LiLOX recombinant expression in E. coli and purification ......................................... 40 3.4. Protein Biochemistry ................................................................................................... 42 3.5. Lipid purification ......................................................................................................... 44 3.6. Treatments of LOX products ....................................................................................... 46 3.7. Lipid analysis ............................................................................................................... 47 3.8. Plants ............................................................................................................................ 54 3.9. Protein crystallography ................................................................................................ 56 4. RESULTS ................................................................................................ 58 4.1. Identification of a putative LOX sequence in the transcriptome of L. incisa .............. 59 ii Table of Contents 4.2. LiLOX is found to be upregulated under nitrogen starvation. ..................................... 64 4.3. LiLOX localizes in the plastids of onion epithelial cells. ............................................ 66 4.4. Heterologous expression of LiLOX ............................................................................. 67 4.5. Crystallography ............................................................................................................ 70 4.6. Activity of LiLOX towards FFA ................................................................................. 73 4.7. Analysis of LiLOX products by HPLC ....................................................................... 76 4.8. LiLOX used on L. incisa lysate shows oxidation towards complex lipids. ................. 80 4.9. Extraction and analysis of complex lipids from L. incisa ............................................ 86 4.10. LiLOX showed activity towards purified complex lipid fractions .............................. 91 4.11. Product analysis of the LiLOX reaction with complex lipid ....................................... 93 4.12. Oxidized LiMGDG molecular species harboring a conjugated diene system do not seem to be the final LiLOX product. ......................................................................... 101 4.13. Kinetic analysis of LiLOX oxidation products .......................................................... 103 4.14. Plastidic lipids from L. incisa are degraded after nitrogen starvation ....................... 105 4.15. LiLOX may be able to rescue the jasmonic acid pathway in wounded leaves of an A. thaliana 13-LOX-mutant. ...................................................................................... 108 4.16. LiLOX Mutations....................................................................................................... 110 5. DISCUSSION ........................................................................................ 116 5.1. LiLOX, a model for plastidic LOXs .......................................................................... 117 5.2. LiLOX and mutants ................................................................................................... 119 5.3. LiLOX is the first LOX shown to metabolize MGDG .............................................. 124 5.4. End product of the LiLOX reaction ........................................................................... 130 5.5. Speculations about the role of LiLOX in L. incisa, and conclusion .......................... 133 6. CITATIONS .......................................................................................... 137 7. LIST OF ABREVIATIONS ................................................................. 146 8. SUPLEMENTAL DATA ..................................................................... 148 iii INTRODUCTION 1. INTRODUCTION 1 INTRODUCTION 1.1. Some plants and algae accumulate neutral lipids under stress conditions The primary endosymbiosis is believed to have happened between an archaebacterium and a cyanobacterium over 1.5 Billion years ago (Yoon et al., 2004). It is widely accepted that this gave rise to eukaryotic algae, the first organisms to possess a cytosolic chloroplast. Shortly afterwards, a split separated red algae from green algae. The latter are estimated to be the precursor of all higher plants (Archibald, 2015). As photoautotrophic organisms, they are able to fix atmospheric CO2, and obtain their energy from the light via photosynthesis. During day light, photons are an unlimited source of energy and H2O as well as CO2 are available in quasi unlimited amounts as well. With these resources as well as nitrogen, phosphate and other inorganic compounds, green algae are able to build all the biomolecules needed throughout the cell cycle. Moreover algae, like other organisms, developed ways throughout evolution to store energy and carbon in different forms such as starch and neutral lipids. The most studied phenotype is their capacity to accumulate lipids in the form of Triacylglycerol (TAG) under stress. In this regard, it was repeatedly reported that the accumulation of this neutral lipid reaches a climax during a shortage of nitrogen or phosphate (Khozin‐Goldberg et al., 2002; Li et al., 2014; Merchant et al., 2012), two important nutrients that are not needed in the biosynthesis of neutral lipids. From an industrial point of view, TAG is of interest as it can be used pure as 1st generation biodiesel or as 2nd generation biodiesel after transesterification. Furthermore, because photosynthetic organisms are building neutral lipids from the consumption of atmospheric CO2, such an industrial production would be carbon neutral (Hu et al., 2008). This ability of algae and plants has made them a primordial model in biotechnology (Du & Benning, 2016). 1.1.1. Lobosphaera incisa, a model green microalga for the accumulation of polyunsaturated fatty acids The human population is known to face an unprecedented growth, expected to reach over 9 billion by 2050 (Godfray et al., 2010; Lee, 2011; Roberts, 2011). Due to this, cultivable lands are reaching a saturation, and alternative alimentation will only be sustainable if it does not require more land (Erb et al., 2016). Since microalgae can be cultivated even in a desert landscape, a high production would not be competing with plants and livestock for cultivable land. Moreover,
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