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Genotypic and Phenotypic Variation in the Astaxanthin Producing Algal

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Genotypic and Phenotypic Variation in the Astaxanthin Producing Algal Dutch translation of the title Genotypische en fenotypische variatie in het astaxanthine producerende groenwier-genus Haematococcus Céline C. Allewaert Cover illustration Picutre taken by Charles Krebs, krebsmicro.com ISBN To refer to this work Allewaert, C., 2016. Genotypic and phenotypic variation in the astaxanthin producing green algal genus Haematococcus. Ghent University, pp. 255. PhD. dissertation. Ghent University, Ghent, Belgium. Publically defended on 22/02/2017 Copy The author and promotors give the authorization to consult and copy parts of this work for personal use only. Every other use is subject to the copyright laws. Permission to reproduce any material contained in this work should be obtained from the author. Members of the examination committee Prof. Dr. Wim Vyverman - Ghent University (Promotor)* Dr. Pieter Vanormelingen - Research Departement Natuurpunt, Mechelen (Co-promotor)* Prof. Dr. Annemieke Verbeken - Ghent University (Chairman) Prof. Dr. Koen Sabbe - Ghent University (Secretary) Dr. Luc Roef - Microalgae Innovation, Proviron Holding NV Prof. Dr. Koenraad Muylaert - KU Leuven, Kulak Dr. Josefin Sefbom - Ghent University Dr. Maike Lorenz - Experimentelle Phykologie und Sammlung von Algenkulturen der Universität Göttingen (EPSAG) * non-voting members Thesis defended in public Wednesday, 22 February 2017 at 16:00h Auditorium Valere Billet Campus Sterre Financial support This thesis was supported by Flanders Innovation & Entrepreneurship (IWT) Grant number: 121449 Table of contents Samenvatting 3 Summary 9 Chapter 1 Preface 15 Chapter 2 General introduction 23 Species diversity in European Haematococccus pluvialis 51 Chapter 3 (Chlorophyceae, Volvocales) Intraspecific variation in traits affecting astaxanthin 89 Chapter 4 productivity in two Haematococcus (Chlorophyceae) species Genotype by irradiance interactions in six 119 Chapter 5 Haematococcus strains (Chlorophyceae, Volvocales) during vegetative growth Genetic and life history determinants of the susceptibility 145 Chapter 6 of the blood alga Haematococcus to infection by Paraphysoderma sedebokerense (Blastocladiomycota) Chapter 7 General discussion and future perspectives 177 Cited literature 201 Acknowledgements 253 Notation index 18S Small subunit of the ribosomal operon 26S Large subunit of the ribosomal operon 5.8S rDNA Ribosomal DNA located between the SSU and LSU rDNA AIC Akaike Information Criterion ANOVA Analysis of variance BI Bayesian Inference BBM Bold Basal Medium BBM-3N Bold Basal Medium enriched with 3 fold the nitrate concentration BOLD Barcode of Life Data System bp Base pair(s) CBC Compensatory Base Change CCAP Culture Collection of Algae and Protozoa DGGE Denaturing Gradient Gel Electrophoresis DMSO Dimethylsulfoxide DNA Deoxyribonucleic Acid DW Dry Weight EFSA European Food Safety Authority FDA Food and Drug Administration G x E Genotype - Environment interaction GMYC Generalized Mixed Yule Coalescent method GWAS Genome-Wide Association Study HPLC High Performance Liquid Chromatography ISSR Inter Simple Sequence Repeat ITS Internal Transcribed Spacer ITS-1 Internal Transcribed Spacer region 1 located between SSU and 5.8S rDNA ITS-2 Internal Transcribed Spacer region 2 located between SSU and 5.8S rDNA LSU rDNA Large Subunit of the ribosomal operon ML Maximum Likelihood NIES Culture Collection at the National Institute for Environmental Studies OFAT One-Factor-at-A-Time approach P Statistical p-value obtained PAM Pulse Amplitude Modulation PCA Principal Component Analysis PDA Photodiode array detector pds Gene Phytoene Desaturase PCR Polymerase Chain Reaction PS Paraphysoderma sedebokerense PSII Photosystem II (or water-plastoquinone oxidoreductase) QTL Quantitative Trait Loci RAPD Random Amplified Polymorphic DNA rbcL RuBisCO large subunit rDNA Ribosomal DNA ROS Reactive Oxygen Species Rf Response factor SAG Sammlung von Algenkulturen der Universität Göttingen (Culture Collection of Algae at Göttingen University) SCCAP Scandinavian Culture Collection of Algae & Protozoa SD Standard Deviation SNV Single Nucleotide Variant SSU rDNA Small Subunit of the ribosomal operon tufA Translation Unstable Factor UTEX Culture collection of algae at the University of Texas at Austin WGA Wheat Germ Agglutinin, Lectin from Triticum vulgaris (wheat) SAMENVATTING Deze studie beoogt om tot een beter begrip te komen van de genotypische en fenotypische variatie in de astaxanthine producerende groenalg Haematococcus pluvialis. We wilden meer bepaald 1) onderzoeken of H. pluvialis één soort is of uit meerdere soorten bestaat door het analyseren van variatiepatronen in moleculaire merkers, morfologische kenmerken en ecofysiologische voorkeuren, 2) de genetisch gebaseerde component van fenotypische variatie op inter- en intraspecifiek niveau kwantificeren bij Haematococcus met nadruk op kenmerken gerelateerd aan de astaxanthine productiviteit, 3) ons een beeld vormen over de manier waarop responsen van verschillende stammen behorend tot verschillende genotypes kunnen uiteenlopen bij milieuveranderingen, meer bepaald bij variërende lichtintensiteit, 4) de gastheer-specificiteit van Paraphysoderma sedebokerense, een courant pathogeen van H. pluvialis beter begrijpen. Het eerste deel van dit proefschrift beoogde het genereren van een fylogenetisch kader voor verder vergelijkend onderzoek. In Hoofdstuk 3 werden genetische, morfologische en ecofysiologische patronen bestudeerd bij Europese Haematococcus stammen geïsoleerd uit 15 locaties verspreid over Europa om de mogelijke soortsniveau variatie te evalueren. Ter vergelijking werd de Europese verzameling aangevuld met geïsoleerde stammen uit Zuid-Amerika en stammen uit cultuurcollecties. De genetische differentiatie van de stammen werd onderzocht op basis van de volledige ITS1 rDNA regio (ITS1-5.8S-ITS2) en voor een selectie stammen ook het rbcL2 chloroplast gen. De aanwezigheid van CBCs3 in ITS1 en ITS2 werd ook geëvalueerd. Fylogenetische analyse resulteerde in zes duidelijke ITS clades - onderbouwd door zowel GMYC4 als statistische parsimonie netwerk analyse5 – waarvan er drie alle Europese stammen bevatten en het grootste deel van de cultuurcollectiestammen. De drie bijkomende clades aanwezig in Haematococcus, worden voorlopig Haematococcus sp. genoemd totdat hun taxonomie verder wordt uitgezocht. De rbcL groep vertoonde veel minder variatie dan de ITS, maar onderscheidde wel twee van de drie ITS groepen waar onze Europese stammen toe behoorden. We hebben drie CBCs gevonden bij elk van de drie Europese clades in de ITS1 secondaire structuur, terwijl er één CBC werd geïdentificeerd bij clades in de ITS2 secondaire structuur. Samen leidde deze resultaten tot het identificeren van drie soorten Haematococcus: een epitype werd voorgesteld voor H. pluvialis en we beschreven twee nieuwe soorten: H. rubicundus en H. rubens. 1 ITS Internal transcribed spacer, ITS regio’s uit het ribosomale cistron. 2 rbcL ribulose 1-2 bi-phosphate carboxylase Large subunit gene, chloroplast DNA. 3 CBC Compensatory Base Change, dubbelzijdige verandering van een nucleotide paar in een helix die deel uitmaakt van de secondaire structuur van het ITS. 4 GMYC Generalized Mixed Yule Coalescent method, statistische soortsafbakenings methode gebaseerd op het verkiezen van best passende vertakingsmodellen voor binnen en tussen soorten variatie om fylogenetische stambomen te reconstrueren. 5 Statistical parsimony network analysis, afbakening van soorten gebaseerd op het aansluiten van de meest nauw verwante knoopunten in een fylogenetische boom tot de maximale“parsimony” is bereikt. 3 SAMENVATTING Ook werd DGGE6 aangewend om deze drie soorten te onderscheiden zonder te moeten sequeneren. De aanwezigheid van bijkomende variatie in Haematococcus laat ons vermoeden dat verdere cryptische soortdiversiteit bestaat. We hebben verder de congruentie met morfologie en temperatuurvoorkeur bepaald voor een selectie stammen die deel uitmaakten van de drie beschreven soorten. Ondanks een grote intraspecifieke variatie en aanzienlijke overlap tussen kenmerken, vonden we significante verschillen in morfologie en groeisnelheid tussen de soorten, hetgeen onze soortafbakening ondersteunde. H. pluvialis en H. rubens hadden gemiddeld meer langwerpige cellen, duidelijkere cytoplasmatische strengen en peervormige protoplasten. De optimale groeitemperaturen waren gelijkaardig voor H. pluvialis, H. rubicundus en H. rubens, nl. variërend tussen 17 en 23 °C, maar H. pluvialis vertoonde gemiddeld een lagere maximale groeisnelheid dan H. rubicundus en H. rubens. In Hoofdstuk 4 werd de genetisch gebaseerde component van fenotypische variatie gekwantificeerd in een “common garden” experiment, waarbij de zes volgende fenotypische kenmerken van genetisch verschillende stammen werden vergeleken onder strikt identieke omgevingsomstandigheden: groeisnelheid, stationaire fase densiteit, percentage palmelloide cellen, post stress droog gewicht, astaxanthine inhoud en aplanospore biovolume. De verschillen in fenotype die overblijven wanneer alle omgevingsvariatie uitgeschakeld wordt, zijn dan te wijten aan genetische verschillen. Via deze methode hebben we de genetisch gebaseerde intra- en interspecifieke (co-) variatie onderzocht bij zes kenmerken gerelateerd aan astaxanthine productiviteit. Hiervoor werd een totaal van 30 stammen behorend tot H. pluvialis en H. rubicundus onderzocht. Naast 24 eigen stammen werden ook zes H. pluvialis stammen uit cultuurcollecties gebruikt. Dit gebeurde onder (pre-stress) groeivoorwaarden en onder voorwaarden waarbij astaxanthine productie
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