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Metabarcoding in the Abyss: Uncovering Deep-Sea Biodiversity Through Environmental

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Metabarcoding in the Abyss: Uncovering Deep-Sea Biodiversity Through Environmental Metabarcoding in the abyss : uncovering deep-sea biodiversity through environmental DNA Miriam Isabelle Brandt To cite this version: Miriam Isabelle Brandt. Metabarcoding in the abyss : uncovering deep-sea biodiversity through environmental DNA. Agricultural sciences. Université Montpellier, 2020. English. NNT : 2020MONTG033. tel-03197842 HAL Id: tel-03197842 https://tel.archives-ouvertes.fr/tel-03197842 Submitted on 14 Apr 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. THÈSE POUR OBTENIR LE GRADE DE DOCTEUR DE L’UNIVERSITÉ DE M ONTPELLIER En Sciences de l'Évolution et de la Biodiversité École doctorale GAIA Unité mixte de recherche MARBEC Pourquoi Pas les Abysses ? L’ADN environnemental pour l’étude de la biodiversité des grands fonds marins Metabarcoding in the abyss: uncovering deep - sea biodiversity through environmental DNA Présentée par Miriam Isabelle BRANDT Le 10 juillet 2020 Sous la direction de Sophie ARNAUD-HAOND et Daniela ZEPPILLI Devant le jury composé de Sofie DERYCKE, Senior researcher/Professeur rang A, ILVO, Belgique Rapporteur Naiara RODRIGUEZ-EZPELETA, Senior researcher/ Chercheur rang B, AZTI, Espagne Rapporteur Jan PAWLOWSKI, Associate Professor/ Professeur rang A, Université de Genève Examinateur Anne CHENUIL, Directrice de recherche, CNRS IMBE Examinateur, Président du jury Frédérique VIARD, Directrice de recherche, CMRS UPMC Examinateur Sophie ARNAUD-HAOND, Cadre de recherche des EPIC, IFREMER MARBEC Directrice de thèse Daniela ZEPPILLI, Cadre de recherche des EPIC, IFREMER LEP Invitée et co-encadrante de thèse i eDNA METABARCODING IN THE DEEP-SEA Any intelligent fool can make things bigger, more complex, and more violent. It takes a touch of genius — and a lot of courage — to move in the opposite direction. Ernst Friedrich Schumacher i eDNA METABARCODING IN THE DEEP-SEA General abstract The abyssal seafloor covers more than half of planet Earth. It can host a large number of, mostly small and still undescribed, organisms (~50,000-5 million individuals/m 2), contributing to key ecosystem functions such as nutrient cycling, sediment stabilisation and transport, or secondary production. Technological developments in the past 30 years have allowed remarkable advances, yet due to the vastness and remoteness of deep-sea habitats, ecological studies have been limited to local or regional scales. Indeed, we have so far explored less than 1% of the deep seafloor, although the latter is under increased threat from a variety of anthropogenic pressures. This PhD aimed at bringing new perspectives for the study of biodiversity and biogeography in the deep-sea, to bridge this large knowledge gap, and advance toward the development of efficient biomonitoring protocols to preserve this vast and elusive backyard. We investigated the potential of multi-marker environmental DNA (eDNA) metabarcoding to assess the extent and distribution patterns of biodiversity in this remote ecosystem. Using mitochondrial and nuclear marker genes, this PhD aimed at producing and testing an optimized eDNA metabarcoding workflow for deep-sea sediments, on a bioinformatic, molecular, and sample processing level, applicable to multiple life compartments including bacteria, protists, and metazoans. Biodiversity assessment with eDNA is confronted with the difficulty in defining accurate “species -level” molecular Operational Taxonomic Units (OTUs), as numerous sources of error induce frequent overestimations. The first part of this thesis describes how newly developed bioinformatic tools can be combined in order to get access different levels of biotic diversity, and underline the advantages of clustering and LULU-curation for producing metazoan biodiversity inventories at the level of the morphospecies. Moreover, the accuracy of protocols based on eDNA in deep sea sediments still needs to be assessed, as results may be biased by ancient DNA, resulting in biodiversity assessments not targeting live organisms.This thesis assessed the potential bias of ancient DNA by 1) evaluating the effect of removing short DNA fragments, and 2) comparing communities revealed by co- extracted DNA and RNA in five deep-sea sites. Results indicated that short DNA fragments do not affect alpha and beta diversity, but that DNA obtained from 10g of sediment should be favoured over RNA for logistically realistic, repeatable, and reliable surveys. Results also ii eDNA METABARCODING IN THE DEEP-SEA confirm that increasing the number of biological rather than technical replicates is important to infer robust ecological patterns. Sieving sediment to separate benthic size classes increased the number of detected meiofauna OTUs, but was not essential for achieving robust biodiversity estimates, and should be avoided if unicellular organisms are also of interest. More importantly, aboveground water and superficial sediment detected significantly different communities in all taxonomic compartments, even when large volumes of water were sampled, emphasising that eDNA metabarcoding of aboveground water samples is not suitable for benthic biodiversity surveys. Finally, this thesis applied the optimized eDNA metabarcoding protocols to investigate the influence of biotic and abiotic factors on the extent and distribution of deep-sea metazoan biodiversity on an East-West transect ranging from the Central Mediterranean to the Mid- Atlantic Ridge. Results, consistent to morphology-based studies, confirm that small-scale biotic and abiotic factors lead to significant vertical changes in metazoan richness and community structure within the sediment, and highlight that regional beta-diversity patterns result from a combined influence of past biogeography and present day processes. This thesis opens the way to large-scale eDNA-based studies in the deep-sea realm, thus contributing to a better understanding of biodiversity, biogeography, and ecosystem function in this vast and still poorly known biome. iii eDNA METABARCODING IN THE DEEP-SEA Résumé général Les fonds abyssaux couvrent plus de la moitié de la planète Terre. Ils peuvent héberger un grand nombre d'organismes (~ 50000 à 5 millions d'individus/m2), pour la plupart petits et encore non décrits, contribuant à des fonctions écosystémiques clés telles que le recyclage du carbone ou la productivité secondaire. Les développements technologiques ont permis des avancées remarquables, mais l'immensité et l'éloignement des habitats profonds ont restreints les études aux niveaux local et régional. Nous avons exploré moins de 1% des fonds marins, alors que ces-derniers forment l'un des plus grands biomes sur Terre et sont de plus en plus sous pression anthropique. Cette thèse vise à apporter de nouvelles perspectives pour l'étude de la biodiversité et de la biogéographie en environnements profonds, pour combler ce déficit de connaissances et permettre le développement de protocoles de biosurveillance efficaces. Nous avons étudié le potentiel du métabarcoding d’ ADN environnemental (ADNe) pour évaluer l'étendue et la distribution de la biodiversité en environnements profonds. À l'aide de gènes marqueurs mitochondriaux et nucléaires, cette thèse vise à produire un protocole de métabarcoding d’ADNe pour les sédiments des grands fonds, optimisé à un niveau de traitement bioinformatique, moléculaire et d'échantillonnage, et applicable à plusieurs compartiments du vivant. L'évaluation de la biodiversité avec l'ADNe est confrontée à la difficulté de définir des Unités Taxonomiques Opérationnelles (OTU) au niveau de «l'espèce», car de nombreuses sources d'erreur induisent de fréquentes surestimations. Le premier chapitre de cette thèse décrit comment des outils bioinformatiques nouvellement développés peuvent être combinés afin d’accéder à divers niveaux de diversité biotique , et soulignent les avantages du clustering et de l’outil LULU pour produire des inventaires de biodiversité métazoaire plus proches du niveau de l’espèce morphologique. De plus, la précision des protocoles basés sur l'ADNe dans les sédiments profonds devait être évaluée, car les résultats peuvent être biaisés par de l'ADN ancien archivé dans le sédiment, ce qui conduirait à des estimations de biodiversité passée plutôt que présente. Dans un second temps, nous avons donc estimé le biais de l'ADN ancien en 1) évaluant l'effet de l'élimination de courts fragments d'ADN, et 2) en comparant les communautés révélées par l'ADN et l'ARN co-extraits. Les résultats indiquent que les fragments d'ADN courts n'affectent pas la diversité iv eDNA METABARCODING IN THE DEEP-SEA alpha et bêta, que l'ADN obtenu à partir de 10 g de sédiments est plus approprié que l'ARN pour des études exhaustives logistiquement réalistes, et que les réplicas biologiques plutôt que techniques sont importants pour inférer des patrons écologiques fiables. Le tamisage des sédiments séparant les organismes benthiques par classe de taille a augmenté le nombre d'OTU métazoaires détectées, mais n'était pas essentiel pour obtenir des patrons écologiques robustes, et devrait être évité si des taxons unicellulaires
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