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The Marine Diatom Phaeodactylum Tricornutum and the Green Algae Chlamydomonas Reinhardtii Serena Flori

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The Marine Diatom Phaeodactylum Tricornutum and the Green Algae Chlamydomonas Reinhardtii Serena Flori Light utilization in microalgae : the marine diatom Phaeodactylum tricornutum and the green algae Chlamydomonas reinhardtii Serena Flori To cite this version: Serena Flori. Light utilization in microalgae : the marine diatom Phaeodactylum tricornutum and the green algae Chlamydomonas reinhardtii. Agricultural sciences. Université Grenoble Alpes, 2016. English. NNT : 2016GREAV080. tel-01686353 HAL Id: tel-01686353 https://tel.archives-ouvertes.fr/tel-01686353 Submitted on 17 Jan 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. THÈSE Pour obtenir le grade de DOCTEUR DE LA COMMUNAUTE UNIVERSITE GRENOBLE ALPES Spécialité : Biologie Végétale Arrêté ministériel : 7 août 2006 Présentée par Serena FLORI Thèse dirigée par Giovanni FINAZZI et codirigée par Dimitris PETROUTSOS préparée au sein du Laboratoire de Physiologie Cellulaire et Végétale dans l'École Doctorale Chimie et Science du Vivant Light utilization in microalgae: the marine diatom Phaeodactylum tricornutum and the green algae Chlamydomonas reinhardtii. Thèse soutenue publiquement le 15 Septembre 2016 devant le jury composé de : Mme Christelle, BRETON Professeur à l’Université Grenoble Alpes (Président) Mme Claire, REMACLE Professeur à l’Université de Liège, Belgique (Rapporteur) M Maurizio, RIBERA D’ALCALA' Directeur de Recherche SZN, Italy (Rapporteur) Mme Xenie, JOHNSON Ingénieur CEA Cadarache (Examinateur) M Jun, MINAGAWA Professeur National Institute for Basic Biology, Japan (Examinateur) M Dimitris, PETROUTSOS CR1 CNRS Grenoble (Co-encadrant de thèse) M Giovanni, FINAZZI Directeur de Recherche CNRS Grenoble (Directeur de thèse) Pour ma famille… 1 2 Index 3 Summary English 6 Résumé Français 7 Chapter 1 9 1.1 Introduction 11 1.2 From light perception to light utilization 11 1.3 The photosynthetic process 12 1.4 “Too much of a good thing…” 16 1.5 Photoprotection 17 1.6 Short-term responses 18 1.6.1 Non-photochemical quenching 18 1.6.1.1 Energy-dependent quenching qE 18 1.6.1.1.1 Xanthophyll cycle and its variants 19 1.6.1.1.2 Light-harvesting complex protein superfamily and its variants 20 1.6.1.2 State transitions, qT 21 1.6.1.3 Energy spillover as photoprotective mechanism 22 1.6.1.4 Photoinhibition, qI 23 1.7 Long-term responses 23 1.8 AIM of the thesis 24 Chapter 2 25 2.1 Introduction 27 2.2 The chloroplast 27 2.2.1 Case of study Phaeodactylum tricornutum (Bohlin, 1897) 33 2.3 Energetic interactions between chloroplasts and mitochondria 36 2.3.1 Preface 36 2.3.2 Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms 37 2.3.2.1 Results 39 2.3.2.2 Conclusions 45 2.3.2.3 Materials and methods 55 2.3.3 Perspectives 61 2.4 Phaeodactylum periplastidial compartment 64 2.4.1 Preface 62 2.4.2 Ultrastructure of the periplastidial compartment of the diatom Phaeodactylum tricornutum 63 3 2.4.2.1 Results and discussion 68 2.4.2.2 Materials and methods 81 2.4.3 Perspectives 82 2.5 Ultrastructure of diatoms photosynthetic membranes 83 2.5.1 Preface 83 2.5.2 Chloroplast thylakoid architecture optimizes photosynthesis in diatoms 84 2.5.2.1 Results and discussion 85 2.5.2.2 Conclusions 92 2.5.2.3 Materials and methods 93 2.5.3 Perspectives 108 Chapter 3 111 3.1 Protocols 113 3.2 Electron microscopy samples preparation 113 3.2.1 Results and discussion 115 3.3 Immunolabeling protocol 116 3.3.1 Immunolabeling protocol through Tokuyasu technique 116 3.3.2 Results and discussion 118 3.4 Tomographic studies 119 3.4.1 The Gatan 3View2XP analysis 119 3.4.1.1 Results and discussion 120 3.4.2 Focused Ion Beam – Scanning Electron Microscopy (FIB-SEM) analysis 120 3.4.2.1 Results and discussion 121 3.5 Data processing and 3-Dimentional reconstruction 122 3.5.1 Results and discussion 122 3.6 Three-Dimentional analysis of the thylakoid membranes 123 3.6.1 Results and discussion 123 3.7 The Atomic Force Microscopy (AFM) 126 3.7.1 Thylakoid membranes preparation for AFM 127 3.7.2 Protocol for the purification of intact chloroplasts of P. tricornutum 128 3.7.3 Improved protocol of isolated thylakoid membranes preparation 129 3.7.4 Experimental procedure INSERM Marseille 130 3.7.4.1 Results and discussion 130 3.7.5 Experimental procedure SSL Grenoble 131 3.7.5.1 Results and discussion 131 4 Chapter 4 133 4.1 Introduction 135 4.2 Chlamydomonas reinhardtii 135 4.2.1 LHCSR 136 4.2.2 A facultative acetate flagellate 137 4.2.3 Photoreceptors 140 4.2.3.1 Phototropin 141 4.2.4 Okazaki large spectrograph 142 4.3 Blue light perception by phototropin mediates regulation of photosynthetic light harvesting 143 4.3.1 Preface 143 4.3.2 A blue light photoreceptor mediates the feedback regulation of photosynthesis 144 4.3.2.1 Results and discussion 146 4.3.2.2 Conclusions 154 4.3.2.3 Materials and methods 155 4.3.3 Perspectives 164 4.4 Carbon metabolism controls photoprotection in Chlamydomonas via the light harvesting complex stress response protein LHCSR3 165 4.4.1 Introduction 165 4.4.2 Results 167 4.4.3 Materials and methods 176 4.4.4 Discussion 177 Chapter 5 181 5.1 Concluding remarks 183 5.2 List of acronyms 186 5.3 List of publications 199 5.4 List of figures 190 5.5 Supplemetary materials 210 5.6 References 211 5.7 Acknowledgements 242 5 Summary Light utilization in microalgae: the marine diatom Phaeodactylum tricornutum and the green algae Chlamydomonas reinhardtii. Microalgae have developed distinct approaches to modulate light absorption and utilization by their photosystems in response to environmental stimuli. In this Ph.D Thesis, I characterised different strategies employed by freshwater (Chlamydomonas reinhardtii) and marine algae (Phaeodactylum tricornutum) to optimise their acclimation to the environment. In the first part of this work, I used spectroscopic, biochemical, electron microscopy analysis and 3- dimentional reconstitution to produce a model of the entire cell of the marine diatom Phaeodactylum tricornutum. This model has been used to address the following questions: i. how the cellular organelles interact to optimise CO2 assimilation via ATP/NADPH exchanges? ii. how is a secondary chloroplast structured to facilitate exchanges with the cytosol via its four membranes envelope barrier? and iii. how have diatoms shaped their photosynthetic membranes to optimise light absorption and downstream electron flow? In the second part, I have focused on the regulation of light harvesting and dissipation in C. reinhardtii by studying the role of perception of light colour and metabolism on excess light dissipation via the Non-Photochemical Quenching of energy (NPQ). Using biochemical and spectroscopic approaches, a molecular link between photoreception, photosynthesis and photoprotection was found in C. reinhardtii via the role of the photoreceptor phototropin on excess absorbed energy dissipation (NPQ). I also demonstrated that besides light, downstream metabolism can also affect this acclimation process. Overall this Ph.D work reveals the existence and integration of different signal pathways in the regulation of photoprotective responses by microalgae living in the ocean and in the land. 6 Résumé L'utilisation de la lumière chez les microalgues : la diatomée marine Phaeodactylum tricornutum et l'algue verte Chlamydomonas reinhardtii. Les microalgues ont développé des approches distinctes pour moduler l'absorption de la lumière et son utilisation par leurs photosystèmes en réponse à des stimuli environnementaux. Dans ce rapport de Thèse je présente les différentes stratégies employées par une algue d'eau douce (Chlamydomonas reinhardtii) et une algue marine (Phaeodactylum tricornutum) pour optimiser leur acclimatation à l'environnement. Dans la première partie de ce rapport, je propose un modèle de cellules entières de la diatomée marine Phaeodactylum tricornutum obtenue par analyses spectroscopiques et biochimiques ainsi que par l’obtention d’images par microscopie électronique et reconstitution 3-D. Ce modèle a été utilisé pour répondre aux questions suivantes i. comment les chloroplastes et les mitochondries sont organisés pour optimiser l'assimilation du CO2 par échange ATP / NADPH ii. comment est structuré un chloroplaste secondaire pour faciliter les échanges avec le cytosol à travers les quatre membranes qui le délimitent et iii. comment sont structurées les membranes photosynthétiques afin d’optimiser l'absorption de lumière et le flux d'électrons. La deuxième partie de ce rapport porte sur la régulation de la lumière et de sa dissipation chez C. reinhardtii grâce à l'étude d'une part du rôle de la perception de la couleur de la lumière et d'autre part du métabolisme sur la dissipation de l'excès de lumière par quenching non photochimique (NPQ). En utilisant des approches biochimiques et spectroscopiques, on a mis en évidence un lien moléculaire entre la photoréception, la photosynthèse et la photoprotection chez C. reinhardtii via le rôle du photorécepteur phototropine, démontrant ainsi que le métabolisme, en plus de la lumière, peut aussi affecter ce processus d'acclimatation. En conclusion, ce travail de thèse révèle l'existence et l'intégration des différentes voies de signalisation dans la régulation des réponses photoprotectrices mises en place chez les microalgues marines et d'eau douce. 7 8 Chapter 1 9 10 1.1 Introduction I realized my Ph.D thanks to a Marie Curie ITN grant in the frame of the AccliPhot network.
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