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Barely Visible but Highly Unique: the Ostreococcus Genome Unveils Its Secrets

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Barely Visible but Highly Unique: the Ostreococcus Genome Unveils Its Secrets Ghent University Faculty of Sciences Department of Molecular Genetics VIB Department of Plant Systems Biology Bioinformatics and Evolutionary Genomics Barely visible but highly unique: the Ostreococcus genome unveils its secrets Steven Robbens Promotor: Prof. Dr. Yves Van de Peer December 2007 Dissertation submitted in fulfillment of the requirements for the degree of Doctor (PhD) in Sciences, Biotechnology Examination committee Prof. Dr. Ann Depicker (chairwoman) - Faculty of Sciences, University Ghent Prof. Dr. Yves Van de Peer (promotor) - Faculty of Sciences, University Ghent Prof. Dr. Hervé Moreau - CNRS, France Pierre Rouzé - Faculty of Sciences, University Ghent Dr. Pieter De Bleser- Faculty of Sciences, University Ghent Prof. Dr. Dirk Inzé - Faculty of Sciences, University Ghent Dr. Lieven De Veylder - Faculty of Sciences, University Ghent Dr. Martin Kuiper - Faculty of Sciences, University Ghent Dr. Olivier De Clerck - Faculty of Sciences, University Ghent Thanks to ... Working in this lab has been really exciting for me, not only for the work I was able to perform, but even more in particular because of the people I worked with. So this page is meant for them… As it always goes, I also would first like to thank my “boss” Yves. Not because this is the first person you should thank, but because he made my 5 years here really worth it. He gave me all the freedom, and if necessary the knowledge, I needed to finish this PhD. Most of all I appreciate you for not being a “bossy boss”: paintball, karting, ice skating, playstation, … you joint all these activities. Good luck in the future with your group!! Going a bit down in the official hierarchy, but that’s really all it means, I bump into Pierre. As we both worked together a lot unveiling all the secrets of Ostreococcus, I was, and still am, amazed by your never-ending interest in science. Discovering one “special” gene could make you so enthusiastic, that we only could follow your stream of enthusiasm. Going a bit away from Gent, I would like to thank Hervé and his team for introducing me to our tiny green friend. In the beginning, Banyuls seemed a remote place to go and to do science, but the beach, the sun, and more in particular the really nice people changed this view completely. Merci beaucoup! Finally, I return to the people I spent almost 1800 days with, my colleagues. Following the time course of my PhD, many thanks to Klaas for introducing me to bioinformatics, Jan, Jeroen, Stefanie and Tineke for being real members and Lieven for being an ad interim member of the number one island of the bioinformatics room. Many thanks to all the other BEGers for the many laughs, lunches, scientific discussions and most of all the nice atmosphere you created here. Cool place to work!! Working in this combined wet/dry lab also gave me to opportunity to leave my pc once and a while to interact with wet lab people, especially our Cuban Doctorandus (and his wife). Thanks for the nice talks in the lab and the many moves during one of the many parties. Finally I would like to thank my parents, my brother and his wife, all my friends and of course Sofie for all the support during this nice period of my life. Thanks. Table of contents Chapter 1 - Introduction ........................................................................... 09 Chapter 2 - The first green lineage cdc25 dual-specificity phosphatase ........ 29 Chapter 3 - Genome-wide analysis of core cell cycle genes in the unicellular green alga Ostreococcus tauri ................................................ 49 Chapter 4 - Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features ........................................ 71 Chapter 5 - The complete chloroplast and mitochondrial DNA sequence of Ostreococcus tauri: organelle genomes of the smallest eukaryote are examples of compaction ................................................... 93 Chapter 6 - Unique Regulation of the Calvin Cycle in the ultrasmall green alga Ostreococcus ....................................................................... 123 Chapter 7 - The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation ........................................ 137 Chapter 8 - Marine algae and vertebrates share the FTO gene implicated in human obesity ........................................................................ 161 Chapter 9 - Discussion/Future perspectives .............................................. 173 Summary - Samenvatting ...................................................... 183 Bibliography .......................................................................... 195 Appendix ............................................................................... 221 7 Introduction Introduction Introduction: algae (Graham and Wilcox, 1999) When talking about algae, we all think of these green, slimy plants attached to the surface of a swimming pool; or of the brown seaweeds covering rocks and beaches across the shoreline of the sea. Asian people see algae as an important source of food as they harbour many essential vitamins and irons. Finally, especially women get in touch with algae when they follow a therapy using algae to clean and heal the skin of their body, because algae contain many minerals which feed our skin. So everybody has been in touch with these plants, but not many people are aware of the variety that is present among these algae. Figure 1. Morphological differences among algae: a) unicellular green alga containing two flagella; b) unbranched, single celled filament; c) spherical colony; d,e) branched filament; f) plant like structure; g) brown kelp 11 Chapter 1 Algae can range in size from tiny single-celled organisms of only 1 micron in diameter to the 65 meter long giant brown kelps, forming underwater forests (fig. 1). In between these two extreme life forms lies a huge morphological diversity. Many algae occur as a unicellular organism, having a simple body plan, while other individual cells aggregate, forming a colony of non-specialized cells. These colonies can consist of a bunch of loosely packed cells, while others are formed in a highly organized fashion, thereby containing a fixed number and arrangement of cells throughout their life cycle. Some of these unicellular algae possess a flagellum which enables them to move around. Besides these unicellular algae, a common growth form among algae is the filament, where a chain of cells is formed after cell division, thereby sharing their cell wall. Filaments can form simple, unbranched structures, composed of a single series of cells; or they can grow into complex structures with many branches and containing multiple rows of cells next to each other. However, parenchymatous algae have the most complex body plan: they possess plant tissue (thallus) composed of undifferentiated cells, providing them with analogous structures as seen in vascular plants (roots, leaves and stems). Although these thalli are undifferentiated, visible differences and functions can be noticed. A nice example within the world of the algae is the kelp, which is a large brown seaweed which can form underwater forests. Their thallus can be divided into three parts: the holdfast, which serves as an anchor; a stipe which supports the blades; and the blades itself, providing them with a vascular leaf-like structure. The huge morphological differences found between algae can be linked to their presence in virtually every ecosystem in the biosphere. Depending on the environment (marine water, fresh water or even terrestrial), the algae have adapted themselves to survive in every circumstance. Algae capture light energy to convert inorganic substances into organic matter through oxygenic photosynthesis. Therefore, the green pigment chlorophyll a, which is the only pigment able to convert light energy into the high energy bonds of organic molecules, is universally present among algae. However, despite the presence of chlorophyll a, not all algae have a green colour. This is caused by the presence of accessory pigments, which are essential for the survival of photosynthetic organisms in both low- and high irradiance habitats: in low-irradiance habitats (the depth record for algae lies around 250 meters, where the light intensity is 12 Introduction only 0.0005% of the surface light) these accessory pigments help in the collection of light which is not completely absorbed by chlorophyll a; in high-irradiance places they help in protecting the algae against photodamage. Depending on the amount and composition of these pigments, eukaryotic algae can be roughly subdivided into different groups: the red algae (Rhodophyta), the brown algae (Phaeophyta) and the green algae (Ben Ali et al, 2001). Rhodophyta: the 4,000-6,000 members of the red algae can occur as unicells, simple filaments, or complex filamentous aggregations. Besides chlorophyll a, they harbour accessory phycobilins and carotenoids (for protection against photodamage). Members of the light-harvesting phycobili-protein family are extremely efficient in harvesting blue and green lights in subtidal habitats. This explains the abundance of red algae in the greater depths of the oceans. Another unique characteristic among all red algae is the absence of a flagellum, making them immobile. The oldest fossil record was found in arctic Canada and is estimated to be around 750-1,250 million years old. Molecular measurements estimated the split of the red and green algae to have occurred
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