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Phylogeny and Molecular Evolution of Green Algae

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Phylogeny and Molecular Evolution of Green Algae Phylogeny and molecular evolution of green algae Ellen Cocquyt Universiteit Gent Faculteit Wetenschappen, Vakgroep Biologie Onderzoeksgroep Algologie Phylogeny and molecular evolution of green algae Fylogenie en moleculaire evolutie van groenwieren Ellen Cocquyt Proefschrift voorgelegd tot het behalen van de graad van Doctor in de Wetenschappen: Biologie Academiejaar 2008-2009 Research Group C eM oFE miii UNIVERSITEIT GENT P h y c o lo g y Promotor: Prof. Dr. O. De Clerck (Universiteit Gent) Co-promotor: Dr. H. Verbruggen (Universiteit Gent) Leden van de leescommissie: Prof. Dr. K. Hoef-Emden (Universität zu Köln, Germany) Dr. P. Rouzé (Universiteit Gent) Prof. Dr. A. Vanderpoorten (Université de Liège) Overige leden van de examencommissie: Prof. Dr. K. Sabbe (Universiteit Gent) Prof. Dr. Erik Smets (Katholieke Universiteit Leuven and National Herbarium of the Nederlands) Prof. Dr. W. Vyverman (Universiteit Gent) Photographs cover: Frederik Leliaert and Heroen Verbruggen Photographs upper band, from left to right and from top to bottom: Boodlea, Phyllodictyon, Dictyosphaeria, Ulva, Cladophora and Valonia Photographs lower band, from left to right: Boergesenia, Codium, Halimeda, Dictyosphaeria and Cladophora Photographs at the back, from left to right and from top to bottom: Blastophysa, Trentepohlia, Ignatius and Chlamydomonas The research reported in this thesis was funded by the Special Research Fund (Ghent University, DOZA-01107605) and performed in the Research Group Phycology and the Center for Molecular Phylogenetics and Evolution, Biology Department, Ghent University, Krijgslaan 281-S8, B-9000, Ghent, Belgium, www.phvcoloqy.uqent.be Dankwoord Vooreerst zou ik mijn promotor Olivier willen bedanken. Bijna negen jaar geleden stapte ik op het vliegtuig richting Zuid-Afrika. Ik mocht gedurende 2 maanden wieren inzamelen langsheen de Zuid- Afrikaanse kust en zou leren 'kijken' naar roodwieren, samen met Olivier die daar toen gedurende een jaar aan de Universiteit van Kaapstad werkte. Op de luchthaven van Kaapstad aangekomen vroeg Olivier verwondert: "Is dat alles wat je mee hebt?", wijzend naar mijn klein rugzakje. Tja, er zat een rugby team op het vliegtuig en niet alle bagage was meegeraakt. De mijne stond nog in Londen, 't Is gelukkig allemaal goed gekomen en ik heb daar een fantastisch tijd gehad! Eenmaal ik mijn licentiaatdiploma behaalde, ging ik nog even langs het labo om goedendag te zeggen. Olivier stelde toen voor om met een Marie Curie beurs een tijdje bij Christine Maggs aan de Queen's University of Belfast te gaan werken. Hm, ik zou eigenlijk net gaan samenwonen met Toon. Uiteindelijk ben ik toch vertrokken voor een half jaartje. Daar heb ik voor het eerst DNA geëxtraheerd en PCR's gedaan, en eveneens een fantastisch tijd beleeft. Terug in België mocht ik onder voorwaarde dat ik een IWT beurs zou aanvragen, beginnen ais laborante bij onze onderzoeksgroep. Die IWT beurs werd niets, maar na anderhalf jaar kon ik dan toch beginnen aan een doctoraat met een BOF beurs. Het resultaat daarvan is dit doctoraat! Olivier, bedankt om me te begeleiden doorheen al die jaren. Ten tweede, zou ik mijn co-promotor Heroen willen bedanken. Ais laborante heb ik voor zijn doctoraat veel praktisch werk gedaan, maar het laatste anderhalf jaar heb ik ontzettend veel hulp van hem gekregen. Heroen, bedankt voor de hulp bij het analyseren van mijn gegevens en het snel en grondig nalezen en verbeteren van de teksten. Ten derde, zou ik Olivier, Heroen en Frederik willen bedanken om me te steunen. Zonder de talloze brainstormmomenten en de hulp van jullie alle drie bij het verwerken en uitschrijven van de resultaten, was ik nooit tot dit resultaat gekomen. Caroline, het was leuk om gedurende drie jaar bureau en labo met je te delen. Eveneens bedankt voor de hulp bij het praktisch werk. Andy en Renata, bedankt voor al het sequentiewerk. Kadriye thanks to help me with PCR's and cloning of some of the nuclear genes. It was often a frustrating job, with a lot of trial and error. Koen Sabbe, Ann Willems en Paul De Vos, bedankt voor de tijd die jullie hebben vrij gemaakt om, vooral in het begin, te luisteren naar mijn vorderingen en me met jullie suggesties telkens een stapje vooruit te helpen. Ook Steven Robbens en Yves van de Peer hielpen me door me in het begin de kans te geven over het nog niet gepubliceerde Ostreococcus genoom te beschikken. Klaus Valentin, thanks for the cDNA service. The generation of this cDNA library was a big step forward during this PhD study. The people from VERTIS Biotechnologie AG (Freising , Germany) also helped a lot to solve the problems I encountered during the screening of the cDNA library. Aan de mensen van de plantkunde in de Ledeganckstraat, het was altijd leuk en gezellig tijdens de middag of aan de koffietafel. Liesbeth, op het bankje aan het kleine vijvertje was het ook steeds gezellig vertoeven. Ik heb daar goeie herinneringen aan! Het laatste anderhalf jaar was het met de mensen van op de Sterre minstens even gezellig tijdens de middagen in de Resto. Katrien en Elke, bedankt voor het nalezen van een stukje Nederlandstalige tekst. Eric, al wist je nooit goed waar ik nu precies mee bezig was, toch zou ik je willen bedanken om me warm te maken voor de algologie, en om je vlucht naar Sri Lanka te verzetten zodat je aanwezig kunt zijn op mijn publieke verdediging. Ook mijn ouders en vrienden zou ik willen bedanken om me steeds te blijven steunen doorheen de jaren. En tenslotte, Toon die nu al bijna negen jaar lang mijn vriend is... nog vele fijne jaren voor ons! Ellen juni 2009 General introduction and thesis outline 1 Ancient relationships among green algae inferred from nuclear and 19 chloroplast genes Gain and loss of elongation factor genes in green algae 43 Complex phylogenetic distribution of a non-canonical genetic code in green 69 algae Codon usage bias and GC content in green algae 81 A multi-locus time-calibrated phylogeny of the siphonous green algae 91 Systematics of the marine microfilamentous green algae Uronema curvatum 115 and Urospora microscopica (Chlorophyta) General discussion 129 References 143 Summary 161 Samenvatting 165 Introduction Algae Algae are a large and diverse group of eukaryotic photosynthetic organisms occurring in almost every habitat. They exhibit a huge morphological diversity, ranging from tiny unicells to huge kelps over 50 m long. The first algal groups arose between 1 and 1.5 billion years ago (Douzery et al. 2004, Yoon et al. 2004) after the symbiogenesis of a heterotrophic eukaryotic organism with a photosynthetic cyanobacterium. This event gave rise to the primary plastids which are still present in the Glaucophyta, red algae and green lineages including land plants (Reyes-Prieto et al. 2007). These three lineages are collectively called Plantae or Archaeplastida (Cavalier-Smith 1981, Adi et al. 2005). The other photosynthetic protists arose through secondary endosymbiosis of either a green or a red alga. The euglenids and chlorarachniophytes are thought to have acquired their plastids from a green alga in two separate secondary endosymbiotic events, while molecular evidence suggests that the red algal plastid of cryptomonads, heterokonts, haptophytes, apicomplexans and dinoflagellates was acquired by a single secondary endosymbiosis in their common ancestor (Archibald 2005, Archibald 2008). This process of serial cell capture and subsequent enslavement explains the diversity of photosynthetic eukaryotes. Endosymbiosis forms the landmark evolutionary event, responsible for the spread of photosynthesis through the Eukaryotic tree of life. Photosynthesis occurs in four of the six supergroups: Archaeplastida (Glaucophyta, red algae, green plants), Chromalveolata (cryptophytes, Stramenopila or heterokonts including diatoms and brown algae, haptophytes and dinoflagallates), Rhizaria (Chlorarachniophyta) and Excavata (euglenoids) (Fig. 1). Figure 1. Eukaryotic tree of life. The first algae arose after the symbiogenesis of a heterotrophic eukaryotic organism with a photosynthetic cyanobacterium, giving rise to the Archaeplastida. The other photosynthetic protists arose through secondary endosymbiosis of either a green or a red alga and occur in four of six supergroups (marked with respectively Glaucophyta eugJenoicfs • green and red circles). The monophyly of the Archaeplastida is well-supported and j most recent evidence favours the h Glaucophyta as earliest diverging lineage within the Archaeplastida (modified after Baldauf 2008, Lane and Archibald 2008). 2 CHAPTER 1 Archaeplastida The monophyly of primary plastids has long been suggested by several features, such as a similar gene content of plastid genomes, the presence of plastid-specific gene clusters that are distinct from those found in Cyanobacteria, the conservation of the plastid-protein import machinery and protein- targeting signals, and phylogenies based on plastid and cyanobacteria! gene sequences (Palmer 2003). Nevertheless, several single-gene phylogenies and a few multigene phylogenies have challenged this hypothesis (e.g., Stiller et al. 2001, Nozaki et al. 2003a, Nozaki et al. 2003b, Stiller and Harrell 2005). Conclusive evidence for the monophyly of the Glaucophyta, red algae and green plants was provided only relatively recently by Rodriguez-Ezpeleta et al. (2005) based on: (1) chloroplast gene phylogenies showing the monophyly of primary plastid and (2) a phylogenomic dataset containing 143 nuclear genes, ca. 30,000 amino acid positions which show the monophyly of all organisms with a primary
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