Disentangling the mechanisms shaping the surface ocean microbiota

BACKGROUND: The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here, we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore this, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S- and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans. RESULTS: We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts. CONCLUSIONS: The differential action of ecological mechanisms seems to cause contrasting biogeography, in the tropical and subtropical ocean, among the smallest surface plankton, prokaryotes and picoeukaryotes. This suggests that the idiosyncrasy of the main constituents of the ocean microbiota should be considered in order to understand its current and future configuration, which is especially relevant in a context of global change, where the reaction of surface ocean plankton to temperature increase is still unclear. Video Abstract

Global comparative analysis of prokaryotic and eukaryotic diversity contributing to oceanic photosynthesis using data from Tara Oceans and Malaspina expeditions

Trabajo final presentado por Laura Rubinat Ripoll para un Máster de la Universitat Pompeu Fabra (UPF), realizado bajo la dirección del Dr. Ramiro Logares del Institut de Ciències del Mar (ICM-CSIC)Peer Reviewe

Structure et diversité trophique des producteurs primaires picoeucaryotes dans l'océan global

Primary production is the synthesis of organic matter out of inorganic molecules, and in most ecosystems is achieved through photosynthesis. Eukaryotic microbial phototrophs and mixotrophs are main contributors to primary production in the global oligotrophic ocean, supporting processes of energy and biomass trophic transfer at a planetary scale. Despite the ecological value of these organisms, their wide taxonomic and functional diversity remains largely unknown. In this thesis, we use different types of molecular data obtained from the Tara Oceans circumglobal expedition to assess the composition and trophic diversity of picoeukaryotic primary producers in the oligotrophic ocean. In the first part of the thesis, we compare metagenomic and metabarcoding data to assess the evolutionary diversity and relative abundance of picophototrophic organisms. We identified phototrophic bacteria as three-fold more abundant and significantly less phylogenetically diverse than phototrophic picoeukayrotes. Prymnesiophyceae, Mamiellophyceae, Pelagophyceae and Dictiochophyceae appeared as the dominant groups of phototrophic picoeukaryotes in terms of relative richness and abundance. In the fourth chapter, we describe a predictive model to quantify the abundance of trophic groups in metagenomic samples. This taxonomy-free approach revealed the dominance of photo-trophic organisms across all ocean basins, while the contribution of phagomixo- and phago-trophs oscillated around 25% of the relative abundance in most samples. In the last study included in this thesis we assess the distribution of a collection of single-cell amplified genomes across all Tara Oceans samples. Our results argue that single-cell sequencing technique has the potential to recover the genome of dominant protists in the global oligotrophic ocean with a relatively low sampling effort. Overall, this work describes a number of approaches based on molecular data for the assessment of primary producers distribution and diversity in marine environments.La production primaire est la synthèse de matière organique à partir de molécules inorganiques et, dans la plupart des écosystèmes, elle est réalisée à travers de la photosynthèse. Les microbiens eucaryotes phototrophes et mixotrophes sont les principaux contributeurs à la production primaire dans l'océan oligotrophe global, soutenant les processus de transfert trophique d'énergie et de biomasse à l'échelle planétaire. Malgré la valeur écologique de ces organismes, leur grande diversité taxonomique et fonctionnelle reste largement inconnue. Dans cette thèse, nous utilisons différents types de données moléculaires obtenues à partir de l'expédition circumglobale de Tara Oceans pour évaluer la composition et la diversité trophique des producteurs primaires picoeucaryotes dans l'océan oligotrophique. Dans la première partie de la thèse, nous comparons les données métagénomiques et de métabarcodage pour évaluer la diversité évolutive et l'abondance relative des organismes picophototrophes. Nous avons identifié les bactéries phototrophes comme trois fois plus abondantes et significativement moins phylogénétiquement diversifiées que les picoeukayrotes phototrophes. Les Prymnesiophyceae, Mamiellophyceae, Pelagophyceae et Dictiochophyceae sont apparus comme les groupes dominants de picoeucaryotes phototrophes en termes de richesse relative et d'abondance. Dans le quatrième chapitre, nous décrivons un modèle prédictif pour quantifier l'abondance des groupes trophiques dans les échantillons métagénomiques. Cette approche, qui ne dépend pas de la attribution taxonomique, a révélé la dominance des organismes phototrophes dans tous les bassins océaniques, tandis que la contribution des phagomixo- et phago- trophées oscillait autour de 25% de l'abondance relative dans la plupart des échantillons. Dans la dernière étude incluse dans cette thèse, nous évaluons la distribution d'une collection de single-cell amplified genomes dans les échantillons de Tara Oceans. Nos résultats soutiennent que la technique de séquençage unicellulaire a le potentiel de récupérer le génome des protistes dominants dans l'océan oligotrophique global avec un effort d'échantillonnage relativement modeste. Dans l'ensemble, ce travail décrit un certain nombre d'approches basées sur des données moléculaires pour évaluer la distribution et la diversité des producteurs primaires dans les environnements marins

Structure et diversité trophique des producteurs primaires picoeucaryotes dans l'océan global

Primary production is the synthesis of organic matter out of inorganic molecules, and in most ecosystems is achieved through photosynthesis. Eukaryotic microbial phototrophs and mixotrophs are main contributors to primary production in the global oligotrophic ocean, supporting processes of energy and biomass trophic transfer at a planetary scale. Despite the ecological value of these organisms, their wide taxonomic and functional diversity remains largely unknown. In this thesis, we use different types of molecular data obtained from the Tara Oceans circumglobal expedition to assess the composition and trophic diversity of picoeukaryotic primary producers in the oligotrophic ocean. In the first part of the thesis, we compare metagenomic and metabarcoding data to assess the evolutionary diversity and relative abundance of picophototrophic organisms. We identified phototrophic bacteria as three-fold more abundant and significantly less phylogenetically diverse than phototrophic picoeukayrotes. Prymnesiophyceae, Mamiellophyceae, Pelagophyceae and Dictiochophyceae appeared as the dominant groups of phototrophic picoeukaryotes in terms of relative richness and abundance. In the fourth chapter, we describe a predictive model to quantify the abundance of trophic groups in metagenomic samples. This taxonomy-free approach revealed the dominance of photo-trophic organisms across all ocean basins, while the contribution of phagomixo- and phago-trophs oscillated around 25% of the relative abundance in most samples. In the last study included in this thesis we assess the distribution of a collection of single-cell amplified genomes across all Tara Oceans samples. Our results argue that single-cell sequencing technique has the potential to recover the genome of dominant protists in the global oligotrophic ocean with a relatively low sampling effort. Overall, this work describes a number of approaches based on molecular data for the assessment of primary producers distribution and diversity in marine environments.La production primaire est la synthèse de matière organique à partir de molécules inorganiques et, dans la plupart des écosystèmes, elle est réalisée à travers de la photosynthèse. Les microbiens eucaryotes phototrophes et mixotrophes sont les principaux contributeurs à la production primaire dans l'océan oligotrophe global, soutenant les processus de transfert trophique d'énergie et de biomasse à l'échelle planétaire. Malgré la valeur écologique de ces organismes, leur grande diversité taxonomique et fonctionnelle reste largement inconnue. Dans cette thèse, nous utilisons différents types de données moléculaires obtenues à partir de l'expédition circumglobale de Tara Oceans pour évaluer la composition et la diversité trophique des producteurs primaires picoeucaryotes dans l'océan oligotrophique. Dans la première partie de la thèse, nous comparons les données métagénomiques et de métabarcodage pour évaluer la diversité évolutive et l'abondance relative des organismes picophototrophes. Nous avons identifié les bactéries phototrophes comme trois fois plus abondantes et significativement moins phylogénétiquement diversifiées que les picoeukayrotes phototrophes. Les Prymnesiophyceae, Mamiellophyceae, Pelagophyceae et Dictiochophyceae sont apparus comme les groupes dominants de picoeucaryotes phototrophes en termes de richesse relative et d'abondance. Dans le quatrième chapitre, nous décrivons un modèle prédictif pour quantifier l'abondance des groupes trophiques dans les échantillons métagénomiques. Cette approche, qui ne dépend pas de la attribution taxonomique, a révélé la dominance des organismes phototrophes dans tous les bassins océaniques, tandis que la contribution des phagomixo- et phago- trophées oscillait autour de 25% de l'abondance relative dans la plupart des échantillons. Dans la dernière étude incluse dans cette thèse, nous évaluons la distribution d'une collection de single-cell amplified genomes dans les échantillons de Tara Oceans. Nos résultats soutiennent que la technique de séquençage unicellulaire a le potentiel de récupérer le génome des protistes dominants dans l'océan oligotrophique global avec un effort d'échantillonnage relativement modeste. Dans l'ensemble, ce travail décrit un certain nombre d'approches basées sur des données moléculaires pour évaluer la distribution et la diversité des producteurs primaires dans les environnements marins

Exploring the Ocean's biological dark matter using simple eukaryotik cell genomics and transcriptomics applied to world meta-omics datasets

Memoria de tesis doctoral presentada por Laura Rubinat Ripoll para obtener el título de Docteur en la Spécialité Écologie por la Sorbonne Université, realizada bajo la dirección del Dr. Ramiro Logares del Institut de Ciències del Mar (ICM-CSIC), del Dr. Colomban de Vargas y el Dr. Olivier Jaillon.-- 181 pages, figures, tables[EN] Primary production is the synthesis of organic matter out of inorganic molecules, and in most ecosystems is achieved through photosynthesis. Eukaryotic microbial phototrophs and mixotrophs are main contributors to primary production in the global oligotrophic ocean, supporting processes of energy and biomass trophic transfer at a planetary scale. Despite the ecological value of these organisms, their wide taxonomic and functional diversity remains largely unknown. In this thesis, we use different types of molecular data obtained from the Tara Oceans circumglobal expedition to assess the composition and trophic diversity of picoeukaryotic primary producers in the oligotrophic ocean. In the first part of the thesis, we compare metagenomic and metabarcoding data to assess the evolutionary diversity and relative abundance of picophototrophic organisms. We identified phototrophic bacteria as three-fold more abundant and significantly less phylogenetically diverse than phototrophic picoeukayrotes. Prymnesiophyceae, Mamiellophyceae, Pelagophyceae and Dictiochophyceae appeared as the dominant groups of phototrophic picoeukaryotes in terms of relative richness and abundance. In the fourth chapter, we describe a predictive model to quantify the abundance of trophic groups in metagenomic samples. This taxonomy-free approach revealed the dominance of photo-trophic organisms across all ocean basins, while the contribution of phagomixo- and phago-trophs oscillated around 25% of the relative abundance in most samples. In the last study included in this thesis we assess the distribution of a collection of single-cell amplified genomes across all Tara Oceans samples. Our results argue that single-cell sequencing technique has the potential to recover the genome of dominant protists in the global oligotrophic ocean with a relatively low sampling effort. Overall, this work describes a number of approaches based on molecular data for the assessment of primary producers distribution and diversity in marine environments[FR] La production primaire est la synthèse de matière organique à partir de molécules inorganiques et, dans la plupart des écosystèmes, elle est réalisée à travers de la photosynthèse. Les microbiens eucaryotes phototrophes et mixotrophes sont les principaux contributeurs à la production primaire dans l’océan oligotrophe global, soutenant les processus de transfert trophique d’énergie et de biomasse à l’échelle planétaire. [...

Structure et diversité trophique des producteurs primaires picoeucaryotes dans l'océan global

La production primaire est la synthèse de matière organique à partir de molécules inorganiques et, dans la plupart des écosystèmes, elle est réalisée à travers de la photosynthèse. Les microbiens eucaryotes phototrophes et mixotrophes sont les principaux contributeurs à la production primaire dans l'océan oligotrophe global, soutenant les processus de transfert trophique d'énergie et de biomasse à l'échelle planétaire. Malgré la valeur écologique de ces organismes, leur grande diversité taxonomique et fonctionnelle reste largement inconnue. Dans cette thèse, nous utilisons différents types de données moléculaires obtenues à partir de l'expédition circumglobale de Tara Oceans pour évaluer la composition et la diversité trophique des producteurs primaires picoeucaryotes dans l'océan oligotrophique. Dans la première partie de la thèse, nous comparons les données métagénomiques et de métabarcodage pour évaluer la diversité évolutive et l'abondance relative des organismes picophototrophes. Nous avons identifié les bactéries phototrophes comme trois fois plus abondantes et significativement moins phylogénétiquement diversifiées que les picoeukayrotes phototrophes. Les Prymnesiophyceae, Mamiellophyceae, Pelagophyceae et Dictiochophyceae sont apparus comme les groupes dominants de picoeucaryotes phototrophes en termes de richesse relative et d'abondance. Dans le quatrième chapitre, nous décrivons un modèle prédictif pour quantifier l'abondance des groupes trophiques dans les échantillons métagénomiques. Cette approche, qui ne dépend pas de la attribution taxonomique, a révélé la dominance des organismes phototrophes dans tous les bassins océaniques, tandis que la contribution des phagomixo- et phago- trophées oscillait autour de 25% de l'abondance relative dans la plupart des échantillons. Dans la dernière étude incluse dans cette thèse, nous évaluons la distribution d'une collection de single-cell amplified genomes dans les échantillons de Tara Oceans. Nos résultats soutiennent que la technique de séquençage unicellulaire a le potentiel de récupérer le génome des protistes dominants dans l'océan oligotrophique global avec un effort d'échantillonnage relativement modeste. Dans l'ensemble, ce travail décrit un certain nombre d'approches basées sur des données moléculaires pour évaluer la distribution et la diversité des producteurs primaires dans les environnements marins.Primary production is the synthesis of organic matter out of inorganic molecules, and in most ecosystems is achieved through photosynthesis. Eukaryotic microbial phototrophs and mixotrophs are main contributors to primary production in the global oligotrophic ocean, supporting processes of energy and biomass trophic transfer at a planetary scale. Despite the ecological value of these organisms, their wide taxonomic and functional diversity remains largely unknown. In this thesis, we use different types of molecular data obtained from the Tara Oceans circumglobal expedition to assess the composition and trophic diversity of picoeukaryotic primary producers in the oligotrophic ocean. In the first part of the thesis, we compare metagenomic and metabarcoding data to assess the evolutionary diversity and relative abundance of picophototrophic organisms. We identified phototrophic bacteria as three-fold more abundant and significantly less phylogenetically diverse than phototrophic picoeukayrotes. Prymnesiophyceae, Mamiellophyceae, Pelagophyceae and Dictiochophyceae appeared as the dominant groups of phototrophic picoeukaryotes in terms of relative richness and abundance. In the fourth chapter, we describe a predictive model to quantify the abundance of trophic groups in metagenomic samples. This taxonomy-free approach revealed the dominance of photo-trophic organisms across all ocean basins, while the contribution of phagomixo- and phago-trophs oscillated around 25% of the relative abundance in most samples. In the last study included in this thesis we assess the distribution of a collection of single-cell amplified genomes across all Tara Oceans samples. Our results argue that single-cell sequencing technique has the potential to recover the genome of dominant protists in the global oligotrophic ocean with a relatively low sampling effort. Overall, this work describes a number of approaches based on molecular data for the assessment of primary producers distribution and diversity in marine environments

Global comparative analysis of prokaryotic and eukaryotic diversity contributing to oceanic photosynthesis using data from Tara Oceans and Malaspina expeditions

15th International Congress of Protistology, International Society of Preotistologists (ISOP), 30 July - 4 August 2017 , Prague, Czech RepublicMotivation: Phototrophic picoeukaryotes or PPEs (organisms measuring ¿ 3¿m) contrib- ute to half of the oxygenic photosynthesis activity in open oceans and play key trophic roles for the functioning of these ecosystems. Despite their ecological value, the dynam- ics and taxonomic composition of these communities are poorly known at global scales, whereas the distribution of cyanobacteria (the only prokaryotes known to be capable of oxygenic photosynthesis) has been widely studied. Nowadays, molecular methods based on high-throughput technology allow us to do new valuable steps towards the compre- hension PPEs communities structure. In this study, we analyze 160 samples from surface waters (3m to 5m) collected along Tara Oceans and Malaspina circumglobal expeditions with PRC-based amplicons and metagenomic sequencing approaches for characterizing the global relative abundance and richness of PPEs and cyanobacteria. Results: We identify Chrysophyceae, Dictyochophyceae, Pelagophyceae, Prasinophyceae and Prymnesiophyceae as dominant PPE groups in the photosynthetic communities of global open ocean surface waters. Prymnesiophyceae, Prasinophyceae and Dictyocho- phyceae emerge as the classes with the highest diversity and abundance of plastidial se- quences. When comparing PPEs and cyanobacteria distribution, we observe that cyano- bacteria are more widely distributed and abundant. The evolutionary diversification of both communities has been described at class and genus level based on ribosomal DNA sequencing data obtained through two molecular approaches, (PCR-based amplicons and metagenomes), for which we report contradictory results and limitations in the quantification of cyanobacteria and PPE groupsPeer Reviewe

ECCB2022: the 21st European Conference on Computational Biology

The ECCB2022 Organising Committee, the ECCB2022 Programme Committee, the ECCB2022 Steering Committee,This paper was published as part of a special issue financially supported by ECCB2022.Peer reviewe

Different processes shape prokaryotic and picoeukaryotic assemblages in the sunlit ocean microbiome

The smallest members of the sunlit-ocean microbiome (prokaryotes and picoeukaryotes) participate in a plethora of ecosystem functions with planetary-scale effects. Understanding the processes determining the spatial turnover of this assemblage can help us better comprehend the links between microbiome species composition and ecosystem function. Ecological theory predicts that selection, dispersal and drift are main drivers of species distributions, yet, the relative quantitative importance of these ecological processes in structuring the surface-ocean microbiome is barely known. Here we quantified the role of selection, dispersal and drift in structuring surface-ocean prokaryotic and picoeukaryotic assemblages by using community DNA-sequence data collected during the global Malaspina expedition. We found that dispersal limitation was the dominant process structuring picoeukaryotic communities, while a balanced combination of dispersal limitation, selection and drift shaped prokaryotic counterparts. Subsequently, we determined the agents exerting abiotic selection as well as the spatial patterns emerging from the action of different ecological processes. We found that selection exerted via temperature had a strong influence on the structure of prokaryotic communities, particularly on species co-occurrences, a pattern not observed among communities of picoeukaryotes. Other measured abiotic variables had limited selective effects on microbiome structure. Picoeukaryotes presented a higher differentiation between neighbouring communities and a higher distance-decay when compared to prokaryotes, agreeing with their higher dispersal limitation. Finally, drift seemed to have a limited role in structuring the sunlit-ocean microbiome. The different predominance of ecological processes acting on particular subsets of the ocean microbiome suggests uneven responses to environmental change

Disentangling the mechanisms shaping the surface ocean microbiota

Background: The ocean microbiota modulates global biogeochemical cycles and changes in its configuration may have large-scale consequences. Yet, the underlying ecological mechanisms structuring it are unclear. Here, we investigate how fundamental ecological mechanisms (selection, dispersal and ecological drift) shape the smallest members of the tropical and subtropical surface-ocean microbiota: prokaryotes and minute eukaryotes (picoeukaryotes). Furthermore, we investigate the agents exerting abiotic selection on this assemblage as well as the spatial patterns emerging from the action of ecological mechanisms. To explore this, we analysed the composition of surface-ocean prokaryotic and picoeukaryotic communities using DNA-sequence data (16S- and 18S-rRNA genes) collected during the circumglobal expeditions Malaspina-2010 and TARA-Oceans. Results: We found that the two main components of the tropical and subtropical surface-ocean microbiota, prokaryotes and picoeukaryotes, appear to be structured by different ecological mechanisms. Picoeukaryotic communities were predominantly structured by dispersal-limitation, while prokaryotic counterparts appeared to be shaped by the combined action of dispersal-limitation, selection and drift. Temperature-driven selection appeared as a major factor, out of a few selected factors, influencing species co-occurrence networks in prokaryotes but not in picoeukaryotes, indicating that association patterns may contribute to understand ocean microbiota structure and response to selection. Other measured abiotic variables seemed to have limited selective effects on community structure in the tropical and subtropical ocean. Picoeukaryotes displayed a higher spatial differentiation between communities and a higher distance decay when compared to prokaryotes, consistent with a scenario of higher dispersal limitation in the former after considering environmental heterogeneity. Lastly, random dynamics or drift seemed to have a more important role in structuring prokaryotic communities than picoeukaryotic counterparts. Conclusions: The differential action of ecological mechanisms seems to cause contrasting biogeography, in the tropical and subtropical ocean, among the smallest surface plankton, prokaryotes and picoeukaryotes. This suggests that the idiosyncrasy of the main constituents of the ocean microbiota should be considered in order to understand its current and future configuration, which is especially relevant in a context of global change, where the reaction of surface ocean plankton to temperature increase is still unclear.Science, Faculty ofNon UBCOceans and Fisheries, Institute for theReviewedFacult