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Jaillon, O.

Publications and source records attributed to Jaillon, O..

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Genomics-based quantitative biogeography of marine plankton

Marine plankton are key drivers of ocean productivity and global carbon cycling, yet their quantitative biogeography remains poorly characterized. Environmental genomic datasets are inherently compositional, restricting analyses to relative abundances and limiting their integration into ecological and biogeochemical models. Here we combine DNA mass measurements, filtered seawater volumes, and metagenomic relative abundances to generate absolute estimates of cell concentrations and carbon biomass of plankton across the global ocean. Leveraging thousands of samples, this approach provides quantitative estimates for hundreds of eukaryotic and thousands of prokaryotic environmental genomes, unveiling ecological associations not captured by compositional data. Using the psbO marker gene, we reconstruct quantitative biogeographies of photosynthetic lineages and, through global-scale modeling, project their distributions to generate quantitative maps of phytoplankton communities across the worlds ocean. By bridging genomic data with biogeochemical metrics, this study provides novel resources for integrating plankton at genomic resolution into next-generation biogeochemical models.

genomics↗

Deviation from Power-Law Distribution when Scaling the Distribution of Marine Plankton Folds from Genomes to Communities

At different scales of living systems, biological entities appear to follow scaling laws, such as power laws, which are often explained from stochastic mechanisms. This is the case for the number of species in a community and the number of genes or protein folds in a genome. Resulting from evolutionary processes combining gene family duplications and expansions with selective pressures, the distribution of protein folds systematically follows a power law in all individually observed genomes. A small number of folds are highly prevalent, while the majority of folds appear only once per genome. However, previous studies on fold occurrence have focused on individual genomes, isolated from their community contexts. In the oceans, plankton communities consist of complex assemblages of species, each exhibiting variable relative abundances. We investigated the consequences of this variability on the composition and distribution of folds by considering the relative abundance of species. By annotating folds to genes of environmental genomes of plankton collected by the Tara Oceans expedition, we show that the relative abundance of folds deviates from the classical power law and instead follows a Type II Pareto distribution. This model, typically observed in other complex organizations such as economics, allows us to classify different categories of folds that exhibit biogeographical differences. Our results show that scaling fold distributions from individual genomes to species communities lead to a deviation from the expected behavior of simple power-law relationship towards a more complex model. This phenomenon could be linked with the variable complexity of marine planktonic ecosystems.

genomics↗

Global population structure of a unicellular marine predator

Unicellular predators, especially marine heterotrophic flagellates (HFs), are fundamental to marine food webs, facilitating the flow of nutrients from bacteria and the smallest primary producers to upper trophic levels. Comprehending their distributions and diversity is essential for understanding the functioning of marine ecosystems. The uncultured MArine STramenopiles clade 4 (MAST-4) constitutes a crucial HF member of the ocean microbiome with a predatory (bacterivorous) lifestyle. Temperature gradients have influenced the evolution and biogeography of MAST-4 species. Yet, similarly to most uncultured microbes, there is limited information on the population diversity and structure within MAST-4 species. This information is key for better comprehending the ecological roles and adaptations of different MAST-4 species to specific ocean niches. Here, we investigate the population diversity and structure on the global scale of the MAST-4 species A, B, C, and E by combining metagenomics and single-cell genomics data from the Tara Oceans expedition. We found substantial population divergence in the abundant MAST-4A and C species, while lower levels of divergence were observed in species B and E. Temperature and salinity were the main drivers structuring the populations within the four MAST-4 species. The analysis of positively selected gene clusters within each MAST-4 species revealed genomic areas likely the basis of population adaptation to different niches. Overall, our results contribute to a better comprehension of the population diversity and structure of four species belonging to an important group of unicellular predators, offering insights into their ecological roles and adaptations in the global ocean. The results also contribute to understanding microbial populations, a dimension of diversity that remains poorly known for most wild species and is pivotal in global change.

ecology↗

Biological and genomic resources for the cosmopolitan phytoplankton Bathycoccus: Insights into genetic diversity and major structural variations

1.Population-scale genome sequencing has become essential for exploring genetic diversity and adaptation, particularly in land plants. In contrast, eukaryotic phytoplankton resources remain limited to model reference genomes or community-level metagenomics, leaving a gap in understanding intraspecific variation and evolutionary processes. To address this, we developed a comprehensive biological and genomic resource for the cosmopolitan and ecologically important genus Bathycoccus. Extensive metagenomic data from across the world Ocean are available for this genus, and previous studies have identified four Bathycoccus species and reconstructed 34 metagenome-assembled genomes. Here we report 28 high-quality strain genome sequences using a combination of Oxford Nanopore Technologies long reads and Illumina short reads and associated biological resources. These include 24 Bathycoccus prasinos strains spanning a latitudinal gradient from 40{degrees} to 78{degrees}N, a reference genome for Bathycoccus calidus, and three genomes of the recently identified B3 clade, which we propose as the Bathycoccus catiminus species. Comparative analyses of sequenced genomes with MAGs highlight the complementarity between resources: while MAGs capture environmental diversity and uncover uncultured taxa, the cultured strain genomes provide complete, non-chimeric high-quality assemblies that resolve structural variations and haplotype-level diversity not detected in MAGs. These include the large outlier chromosome (BOC), a putative sexual chromosome revealing a second mating type, and extensive variability in the small outlier chromosome (SOC), associated with viral resistance and genome plasticity. Together, these biological and genomic resources establish Bathycoccus prasinos as a powerful model for studying diversity, adaptation, and evolution of eukaryotic phytoplankton in the ocean, complementing existing global metagenomic datasets. 2. Significance statementEukaryotic phytoplankton are key to ocean ecosystems, yet their intraspecific genomic diversity is poorly understood. We present 28 high-quality genomes and their annotations of the cosmopolitan microalga Bathycoccus, revealing whole genome structural variations, chromosomal haplotype diversity linked to mating and viral resistance, and offering a genomic framework that complements metagenomic data to establish this picoalga as a model for functional and ecological studies.

genomics↗

Changes in functional composition and gene expression in eukaryotic plankton at the Atlantic-Arctic Polar front

In the Arctic Ocean, phytoplankton communities, dominated by eukaryotes, sustain the marine food web and influence biogeochemical cycles. While many are endemic, some are transported by currents from the Atlantic Ocean along an environmental gradient that steepens at the polar front. Despite these distinct biogeographies, the functional characteristics of these communities remain poorly characterized. Here, we analyzed twenty metatranscriptomes from a North Atlantic-Arctic environmental gradient considering ocean currents transport times. Functions related to the regulation of gene expression and cold acclimation were more abundant in Arctic metatranscriptomes. Using the PHATE dimensionality reduction algorithm, reconstructed transcriptomes of Bacillariophyta, Mamiellales, Pelagophyceae, and Phaeocystales revealed different gene expression patterns, including photosynthesis regulation. All groups showed upregulation of numerous key temperature-associated functions and a subset of shared functions, supporting a convergence in transcriptomic changes under polar conditions. This study, based on a new resource of reconstructed transcriptomes, addressed the functional differentiation of eukaryotic phytoplankton across the North Atlantic and Arctic Ocean. It evidenced both differential and convergent changes in gene expression across the polar front in widespread phytoplankton types. These results advance our understanding of the functional dynamics of phytoplankton along environmental gradients.

genomics↗

Global observation of plankton communities from space

Satellite remote sensing from space is a powerful way to monitor the global dynamics of marine plankton. Previous research has focused on developing models to predict the size or taxonomic groups of phytoplankton. Here we present an approach to identify representative communities from a global plankton network that included both zooplankton and phytoplankton and using global satellite observations to predict their biogeography. Six representative plankton communities were identified from a global co-occurrence network inferred using a novel rDNA 18S V4 planetary-scale eukaryotic metabarcoding dataset. Machine learning techniques were then applied to train a model that predicted these representative communities from satellite data. The model showed an overall 67% accuracy in the prediction of the representative communities. The prediction based on 17 satellite-derived parameters showed better performance than based only on temperature and/or the concentration of chlorophyll a. The trained model allowed to predict the global spatiotemporal distribution of communities over 19-years. Our model exhibited strong seasonal changes in the community compositions in the subarctic-subtropical boundary regions, which were consistent with previous field observations. This network-oriented approach can easily be extended to more comprehensive models including prokaryotes as well as viruses.

ecology↗

Unveiling hidden eukaryotes: diversity of Endomyxa (Rhizaria) in coastal marine habitats

Nucleic acid based studies of marine biodiversity often focus on Kingdom-level diversity. Such approaches often largely miss diversity of less studied groups, likely to harbour many unknown lineages which are likely playing significant ecological roles. Among these elusive groups are Endomyxa (Rhizaria), a ubiquitous, but understudied lineage comprising parasites (e.g. Ascetosporea, Phytomyxea), free-living amoebae (e.g. Vampyrellida, Gromia, Filoreta), flagellates (e.g. Tremula, Aquavolon), and unknown environmental lineages. Using Endomyxa-biased primers targeting the hypervariable region V4 of the 18S rRNA gene, we explored the diversity of Endomyxa in marine samples from European coastal sites and compared it to that found in pan-eukaryote V4 libraries of the same samples. In total 458 endomyxan OTUs were identified, of which 38% were only detected by the specific primers. Most are distinct from published sequences, and include novel diversity within known clades, and putative novel lineages. The data revealed variations in endomyxan assemblages related to habitat (benthic vs. pelagic, sampling site), mode of nutrition (parasitic vs. free-living) and nucleic acid type (DNA vs. RNA). Overall, the vast majority of endomyxan diversity occurs in sediments (including Vampyrellida, Reticulosida, and the environmental "Novel Clade 12") where they form diverse and active communities including many uncharacterised lineages.

microbiology↗

Discovery of a class of giant virus relatives displaying unusual functional traits and prevalent within plankton: the Mirusviricetes

DNA viruses have a major influence on the ecology and evolution of cellular organisms, but their overall diversity and evolutionary trajectories remain elusive. Here, we performed a phylogeny-guided genome-resolved metagenomic survey of the sunlit oceans and discovered plankton-infecting relatives of herpesviruses that form a putative new phylum dubbed Mirusviricota. The virion morphogenesis module of this large monophyletic clade is typical of viruses from the realm Duplodnaviria, with the major capsid protein fold being a likely structural intermediate between the capsid proteins of Caudoviricetes (tailed phages) and Herpesvirales (animal-infecting viruses). Yet, a substantial fraction of Mirusviricota genes, including hallmark transcription machinery genes missing in herpesviruses, are closely related homologs of large and giant eukaryotic DNA viruses from another viral realm. The remarkable chimeric attributes of Mirusviricota provide missing links in the evolution of both herpesviruses and giant viruses. Furthermore, mirusviruses are widespread and transcriptionally active from pole to pole, encoding complex functional traits used during the infection of microbial eukaryotes. The Mirusviricota prevalence, functional activity, diversification, and atypical evolutionary traits point to a lasting role of mirusviruses in the ecology of marine ecosystems that might have not only predated but also contributed to the emergence of herpesviruses and giant viruses.

evolutionary biology↗

Equatorial to Polar genomic variability of the microalgae Bathycoccus prasinos

Phytoplankton plays a fundamental role in the ecology of ocean systems and is the key player in the global carbon cycle. At a time of global warming, understanding the mechanisms of its adaptation to temperature is therefore of paramount importance. Cosmopolitan planktonic species abundant in different marine environments provide both a unique opportunity and an efficient methodological tool to study the genomic bases of their adaptation. This is the case for the eukaryotic picoalga Bathycoccus prasinos, whose genomic variability we chose to study in temperate and polar oceanic waters. Using multiple metagenomic datasets, we found that ~5% of B. prasinos genomic positions are variable, with an overwhelming majority of biallelic motifs. Cold and temperate waters are clearly associated with changes in variant frequencies, whereas in transitional waters we found more balanced polymorphism at most of these positions. Mesophilic and psychrophilic gene variants are distinguished by only a few amino acid changes located at positions critical for physical and functional protein properties. These results provide new information on the genomic diversity of a cosmopolitan eukaryotic planktonic specie and reveal "minimal mutational strategies" which finely tune the properties of specific proteins at different temperatures.

genomics↗

Insights into biotic and abiotic modulation of ocean mesopelagic communities

For decades, marine plankton have been investigated for their capacity to modulate biogeochemical cycles and provide fishery resources. Between the sunlit (epipelagic) layer and the deep dark waters, lies a vast and heterogeneous part of the ocean: the mesopelagic zone. How plankton composition is shaped by environment has been well-explored in the epipelagic but much less in the mesopelagic ocean. Here, we conducted comparative analyses of trans-kingdom community assemblages thriving in the mesopelagic oxygen minimum zone (OMZ), mesopelagic oxic, and their epipelagic counterparts. We identified nine distinct types of intermediate water masses that correlate with variation in mesopelagic community composition. Furthermore, oxygen, NO - and particle flux together appeared as the main drivers governing these communities. Novel taxonomic signatures emerged from OMZ while a global co-occurrence network analysis showed that about 70% of the abundance of mesopelagic plankton groups is organized into three community modules. One module gathers prokaryotes, pico-eukaryotes and Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from oxic regions, and the two other modules are enriched in OMZ prokaryotes and OMZ pico-eukaryotes, respectively. We hypothesize that OMZ conditions led to a diversification of ecological niches, and thus communities, due to selective pressure from limited resources. Our study further clarifies the interplay between environmental factors in the mesopelagic oxic and OMZ, and the compositional features of communities.

ecology↗

Environmental vulnerability of the global ocean plankton community interactome

Marine plankton form complex communities of interacting organisms at the base of the food web, which sustain oceanic biogeochemical cycles, and help regulate climate. Though global surveys are starting to reveal ecological drivers underlying planktonic community structure, and predicted climate change responses, it is unclear how community-scale species interactions will be affected by climate change. Here we leveraged Tara Oceans sampling to infer a global ocean cross-domain plankton co-occurrence network - the community interactome - and used niche modeling to assess its vulnerabilities to environmental change. Globally, this revealed a plankton interactome self-organized latitudinally into marine biomes (Trades, Westerlies, Polar), and more connected poleward. Integrated niche modeling revealed biome-specific community interactome responses to environmental change, and forecasted most affected lineages for each community. These results provide baseline approaches to assess community structure and organismal interactions under climate scenarios, while identifying plausible plankton bioindicators for ocean monitoring of climate change.

ecology↗

Restructuring of genomic provinces of surface ocean plankton under climate change

The impact of climate change on diversity, functioning and biogeography of marine plankton remains a major unresolved issue. Here, niche theory is applied to plankton metagenomes of 6 size fractions, from viruses to meso-zooplankton, sampled during the Tara Oceans expedition. Niches are used to derive plankton size-dependent structuring of the oceans south of 60{degrees}N in climato-genomic provinces characterized by signature genomes. By 2090, assuming the RCP8.5 high warming scenario, provinces would be reorganized over half of the considered ocean area and quasi-systematically displaced poleward. Particularly, tropical provinces would expand at the expense of temperate ones. Sea surface temperature is identified as the main driver of changes (50%) followed by phosphate (11%) and salinity (10%). Compositional shifts among key planktonic groups suggest impacts on the nitrogen and carbon cycles. Provinces are linked to estimates of carbon export fluxes which are projected to decrease on average by 4% in response to biogeographical restructuring.

ecology↗

Functional repertoire convergence of distantly related eukaryotic plankton lineages revealed by genome-resolved metagenomics

Marine planktonic eukaryotes play a critical role in global biogeochemical cycles and climate. However, their poor representation in culture collections limits our understanding of the evolutionary history and genomic underpinnings of planktonic ecosystems. Here, we used 280 billion Tara Oceans metagenomic reads from polar, temperate, and tropical sunlit oceans to reconstruct and manually curate more than 700 abundant and widespread eukaryotic environmental genomes ranging from 10 Mbp to 1.3 Gbp. This genomic resource covers a wide range of poorly characterized eukaryotic lineages that complement long-standing contributions from culture collections while better representing plankton in the upper layer of the oceans. We performed the first comprehensive genome-wide functional classification of abundant unicellular eukaryotic plankton, revealing four major groups connecting distantly related lineages. Neither trophic modes of plankton nor its vertical evolutionary history could explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years. CoverNavigating on the map of plankton genomics with Tara Oceans and anvio: a comprehensive genome-resolved metagenomic survey dedicated to eukaryotic plankton. O_FIG O_LINKSMALLFIG WIDTH=153 HEIGHT=200 SRC="FIGDIR/small/341214v2_ufig1.gif" ALT="Figure 1"> View larger version (82K): org.highwire.dtl.DTLVardef@536fe5org.highwire.dtl.DTLVardef@1d72cc9org.highwire.dtl.DTLVardef@1bd5281org.highwire.dtl.DTLVardef@739512_HPS_FORMAT_FIGEXP M_FIG C_FIG

microbiology↗

Evolutionary diversification of tiny ocean predators

Unicellular eukaryotic predators have a crucial role in the functioning of the ocean ecosystem by recycling nutrients and energy that are channeled to upper trophic levels. Traditionally, these evolutionary-diverse organisms have been combined into a single functional group (Heterotrophic flagellates), overlooking their organismal differences. Here we investigate four evolutionary related species belonging to one cosmopolitan family of uncultured marine picoeukaryotic predators: MAST-4 (species A, B, C, and E). Co-occurrence and distribution analyses in the global surface ocean indicated contrasting patterns in MAST-4A & C, suggesting adaptation to different temperatures. We then investigated whether these spatial distribution patterns were mirrored by MAST-4 genomic content using Single-Cell Genomics. Analyses of 69 single-cells recovered 66-83% of the MAST-4A/B/C/E genomes, which displayed substantial inter-species divergence. MAST-4 genomes were similar in terms of broad gene functional categories, but they differed in enzymes of ecological relevance, such as glycoside hydrolases (GHs), which are part of the food degradation machinery in MAST-4. Interestingly, MAST-4 species featuring a similar GH composition co-excluded each other (A & C) in the surface global ocean, while species with a different set of GHs appeared to be able to co-exist (species B & C) suggesting further niche diversification associated to prey digestion. We propose that differential niche adaptation to temperature and prey type has promoted adaptive evolutionary diversification in MAST-4. Altogether, we show that minute ocean predators from the same family may have different biogeography and genomic content, which need to be accounted to better comprehend marine food webs.

ecology↗

Giant viruses encode novel types of actins possibly related to the origin of eukaryotic actin: the viractins

Actin is a major component of the eukaryotic cytoskeleton. Many related actin homologues can be found in eukaryotes1, some of them being present in most or all eukaryotic lineages. The gene repertoire of the Last Eukaryotic Common Ancestor (LECA) therefore would have harbored both actin and various actin-related proteins (ARPs). A current hypothesis is that the different ARPs originated by gene duplication in the proto-eukaryotic lineage from an actin gene that was inherited from Asgard archaea. Here, we report the first detection of actin-related genes in viruses (viractins), encoded by 19 genomes belonging to the Imitervirales, a viral order encompassing the giant Mimiviridae. Most viractins were closely related to the actin, contrasting with actin-related genes of Asgard archaea and Bathyarchaea (a newly discovered clade). Our phylogenetic analysis suggests viractins could have been acquired from proto-eukaryotes and possibly gave rise to the conventional eukaryotic actin after being reintroduced into the pre-LECA eukaryotic lineage.

evolutionary biology↗

Elucidation of Codon Usage Signatures across the Domains of Life

Due to the degeneracy of the genetic code, multiple codons are translated into the same amino acid. Despite being synonymous, these codons are not equally used. Selective pressures are thought to drive the choice among synonymous codons within a genome, while GC content, which is generally attributed to mutational drift, is the major determinant of interspecies codon usage bias. Here we find that in addition to the bias caused by GC content, inter-species codon usage signatures can also be detected. More specifically, we show that a single amino acid, arginine, is the major contributor to codon usage bias differences across domains of life. We then exploit this finding, and show that the identified domain-specific codon bias signatures can be used to classify a given sequence into its corresponding domain with high accuracy. Considering that species belonging to the same domain share similar tRNA decoding strategies, we then wondered whether the inclusion of codon autocorrelation patterns might improve the classification performance of our algorithm. However, we find that autocorrelation patterns are not domain-specific, and surprisingly, are unrelated to tRNA reusage, in contrast to the common belief. Instead, our results reveal that codon autocorrelation patterns are a consequence of codon optimality throughout a sequence, where highly expressed genes display autocorrelated optimal codons, whereas lowly expressed genes display autocorrelated non-optimal codons.

evolutionary biology↗