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Diversity and Evolution of Nassellaria and Spumellaria (Radiolaria) Miguel Mendez Sandin

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Diversity and Evolution of Nassellaria and Spumellaria (Radiolaria) Miguel Mendez Sandin Diversity and Evolution of Nassellaria and Spumellaria (Radiolaria) Miguel Mendez Sandin To cite this version: Miguel Mendez Sandin. Diversity and Evolution of Nassellaria and Spumellaria (Radiolaria). Protis- tology. Sorbonne Université, 2019. English. NNT : 2019SORUS549. tel-03137926 HAL Id: tel-03137926 https://tel.archives-ouvertes.fr/tel-03137926 Submitted on 10 Feb 2021 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. Sorbonne Université École doctorale 227 : Sciences de la Nature et de l’Homme : Écologie et Évolution Station Biologique de Roscoff / Adaptation et diversité en milieu marin, UMR 7144 DIVERSITÉ ET ÉVOLUTION DES NASSELLAIRES ET SPUMELLAIRES (RADIOLAIRES) Par Miguel Méndez Sandín Thèse de doctorat d’Évolution et Diversité Moléculaire Dirigée par Fabrice Not Présentée et soutenue publiquement le 22 de Novembre de 2019 Devant un jury composé de : Linda Amaral-Zettler Rapportrice Senior Scientist, Netherlands Institute for Sea Research Fabien Burki Rapporteur Assistant professor, Uppsala University John Dolan Examinateur Research Director, Observatorie Océanologique de Villefranche-sur-Mer, Sorbonne Université, CNRS Spela Gorican Examinatrice Senior Researcher, Slovenian Academy of Sciences and Arts Nathalie Simon Examinatrice Associate professor, Station Biologique de Roscoff, Sorbonne Université, CNRS Cédric Berney Invité Associate Researcher, Station Biologique de Roscoff, Sorbonne Université, CNRS Fabrice Not Directeur de Thèse Research Director, Station Biologique de Roscoff, Sorbonne Université, CNRS I would like to thank the ANR grant IMPEKAB (15-CE02-0011) and the Brittany Region ARED (C16 1520A01), to have funded my PhD thesis and the experiments on it. To my grandfather: Suso, who gave me everything having nothing A mi abuelo: Suso, quien me dio todo sin tener nada À mon grand-père : Suso, qui m'a tout donné sans rien avoir. Summary Nassellaria and Spumellaria (Polycystines, Radiolaria) are planktonic amoeboid protists belonging to the Rhizaria lineage. They are widely distributed and abundant in the global ocean. Their silicified skeleton preserves very well in sediments, displaying an excellent and continuous fossil record dating back to the early Cambrian. Radiolarian fossil record is extremely valuable for paleo- environmental reconstruction studies. Radiolaria are difficult to maintain in culture preventing an accurate perception of their extant diversity and ecology in contemporary oceans, and most of it is inferred from the fossil record and sediment samples. Despite recent effort, their taxonomy and evolutionary history remains poorly known and controversial. Here I explored the diversity and evolutionary patterns of Nassellaria and Spumellaria, based on a single cell integrative classification obtained from taxonomic marker genes (18S and 28S ribosomal DNA) and morphological characteristics. Our phylogenetic analyses established a morpho- molecular framework partly agree with the latest classifications relying essentially on the overall symmetry of the skeleton at Superfamily and Family level. This comprehensive morpho-molecular framework was integrated with recent phylogenetic studies of Acantharia and Collodaria in order to reconstruct the most extensive rDNA phylogenetic analysis of Radiolaria to date. The integrative classification of Radiolaria established the Acantharia, with Strontium sulphate skeleton, a sister clade of the Taxopodida and the Polycystines, both with silicate skeletons. Radiolarian evolutionary patterns were explored using a fossil calibrated molecular clock dating an origin of Radiolaria in the Early Neoproterozoic. Two major events characterized their diversification, the development of the skeleton in the Early Paleozoic and the establishment of the symbiosis in the Middle to Upper Jurassic, when oligotrophy and anoxia governed the oceans. A large environmental diversity was found associated with basal nodes, that following the morpho-molecular framework and evolutionary patterns led to hypothesize a large skeleton-less diversity related to Taxopodida (Rad-B) at basal positions in the radiolarian phylogenetic tree. The intracellular genetic variability of Nassellaria and Spumellaria was explored finding an important taxonomic bias in both the variability and number of sequences when dealing with short read High-Throughput Sequencing (HTS) output. Sequencing platforms, such as Oxford Nanopore Technologies, provided interesting results for the full rDNA sequences, despite their high error rate. Our analyses allowed a better understanding of the global biodiversity and biogeography of Radiolaria, that was later explored through a metabarcoding approach across samples collected globally during Tara Oceans and Malaspina expeditions and regionally compared with the MOOSE-GE cruises in the western Mediterranean-sea. Radiolaria contributed about 9% of the total eukaryotic reads in the studied datasets. The colonial Collodaria was the group more abundant in large size fractions, adapted to oligotrophic and surface waters. Acantharia took the leading role in smaller size fractions and more productive waters. Spumellaria dominated the mesopelagic and bathypelagic followed by a big importance of environmental diversity believed to be associated to the skeleton-less Radiolaria. This work brings a new comprehensive perspective of the evolutionary relationships and diversity of extant Radiolaria, highlighting their important planktonic role in both contemporary and past oceans. Résumé Les Nassellaires et les Spumellaires (Polycystines, Radiolaires) sont des protistes planctoniques amiboïdes appartenant au super-groupe des Rhizaires. Ils sont abondants et largement distribués dans l’océan. Leur squelette silicifié se conserve très bien dans les sédiments et présente un excellent enregistrement fossile remontant jusqu’au début du Cambrien. Les fossils de Radiolaires sont extrêmement précieux pour les études de reconstruction paléo-environnementales. Les Radiolaires sont difficiles à maintenir en culture, ce qui limite nos connaissances sur leur diversité et leur écologie dans les océans actuels, qui reposent essentiellement sur les données fossiles et les échantillons de sédiments. Malgré des efforts récents, leur taxinomie et leur histoire évolutive demeurent peu connues et controversées. Pendant mon doctorat, j’ai exploré la diversité et l’évolution des Nassellaires et des Spumellaires sur la base d’une classification intégrative obtenue à partir de gènes marqueurs taxinomiques (ADN ribosomal 18S et 28S) et de caractéristiques morphologiques issues de cellules uniques isolées depuis l’environnement. Nos analyses phylogénétiques ont permit de mettre en evidence un cadre morpho-moléculaire correspondant partiellement aux classifications les plus récentes reposant largement sur la symétrie globale du squelette pour les Superfamilles et Familles. Nos nouvelles données morpho-moléculaires ont été intégrée aux études précédentes sur les Acanthaires et des Collodaires afin de reconstruire la phylogénie des Radiolaires la plus complete à ce jour. Cette nouvelle classification intégrée des Radiolaires établit les Acanthaires, avec leur squelette en sulfate de strontium, comme le groupe frère des Taxopodida et des Polycystines, tous deux dotés d’un squelette en silicate. Associé à ces phylogenies, l’utilisation d’horloges moléculaires nous a permis de dater l'origine des Radiolaires au Néoprotérozoïque. Mais également de metre en evidence deux événements majeurs caractérisent leur diversification : le développement du squelette au Paléozoïque ancien et l’établissement de la symbiose dans le Jurassique moyen à supérieur, lorsque les eaux oligotrophes et anoxiques dominaient les océans. La grande diversité environnementale trouvée aux nœuds basaux de nos phylogenies nous conduit à émettre l'hypothèse de l’existence d’une grande diversité de Radiolaires sans squelette associée aux Taxopodida (Rad-B). La variabilité génétique intracellulaire des Nassellaires et des Spumellaires a été étudiée et a révélé un biais taxinomique important dans la variabilité et le nombre de séquences obtenues par différentes méthodes de séquençage à haut débit (HTS). Cependant, le séquençage par Oxford Nanopore Technologies, a fourni des résultats intéressants pour le séquençage complet des ADNr, malgré son taux d'erreur élevé. L’ensemble de ces analyses a permis de mieux comprendre la biodiversité et la biogéographie des Radiolaires, qui ont été étudiées selon une approche de metabarcoding sur des échantillons collectés a travers le monde au cours des expéditions Tara Oceans et Malaspina puis comparés à l’échelle régionale avec les campagnes océanographiques MOOSE-GE en Méditerranée Occidentale. Les Radiolaires contribuent pour environ 9% du total des séquences eucaryotes dans les jeux de données étudiés. Les Collodaires coloniaux représentent le groupe le plus abondant dans les grandes fractions de taille, ils sont adaptés aux eaux oligotrophes et de surface. Les Acanthaires dominent les fractions de plus petites tailles
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