Search bioRxiv⌕ Search

Biology subjects

Pelletier, E.

Publications and source records attributed to Pelletier, E..

At least 19 recordsLinked to original sources

The ultrasmall ocean microbiome: a reservoir of microbial diversity and nitrogen fixation.

Marine microbiology has long considered ultrasmall (<0.2 {micro}m) size fractions as virus-dominated, yet emerging evidence suggests potential prokaryotic activity with implications for global biogeochemical cycles. Here, we present the first comprehensive genome-resolved survey of this fraction, built on 4,058 metagenome-assembled genomes (MAGs) representing 1,152 species across Bacteria (90.7%) and Archaea (9.3%), dominated by Pseudomonadota, Bacteroidota, and Nanoarchaeota. Over 490 non-redundant MAGs occurred exclusively in the ultrasmall fraction, with 66.8% representing novel taxa, particularly abundant in Arctic surface waters. Beyond known ultrasmall organisms (e.g., DPANN archaea and Patescibacteria), which show expected genomic and metabolic reduction, functional annotation revealed diverse metabolic potential across nitrogen, sulfur, and carbon cycling. Focusing on nitrogen fixation, we identified 13 non-cyanobacterial diazotroph species with complete nitrogenase operons spanning four bacterial classes. These resolved into two ecotypes: cosmopolitan low-abundance taxa, and Arctic ultrasmall-restricted strains reaching up to 16.7% relative abundance. Two lineages (50-400-T64 and Novosphingobium) showed ultrasmall exclusive bipolar distributions across Arctic and Southern Oceans. Beyond nitrogen fixation, these diazotrophs encoded pathways for denitrification, DNRA, sulfur oxidation, and carbon fixation. Our findings reveal an overlooked reservoir of microbial diversity including diazotrophs in the ultrasmall ocean microbiome, with significant implications for polar nitrogen budgets and global biogeochemical models.

microbiology↗

A billion-year-old bacterial machinery replicates plastid DNA and supports kleptoplastidy

The endosymbiotic evolution of plastids and mitochondria was central to the origin and success of eukaryotes. One of the most prominent molecular machineries thought to have disappeared early in eukaryote evolution is the multi-subunit bacterial DNA polymerase III (DNApol-III), which is the principal enzyme complex supporting DNA replication in bacteria. Here, we combined worldwide metagenomics and cultivation to characterise the mosaic genomic landscape of abundant phytoplankton lineages of Teleaulax (Cryptophyceae), which contain an endosymbiotically-derived nucleomorph genome. Unexpectedly, the nuclear, plastid and nucleomorph genomes of Teleaulax contain ubiquitously expressed genes for plastid-targeted DNApol-III subunits. These genes shed light on the functioning of Teleaulax genomes when sequestered by the ciliate Mesodinium during its kleptoplastidic photosynthetic activity1-3. In particular, the alpha subunit gene (encoding the polymerase activity), which resides in the nucleomorph genome, is continuously expressed in Mesodinium in controlled laboratory experiments. This provides a mechanistic explanation for the replication of Teleaulax plastid genomes weeks after the nuclear genome is lost4. Beyond Teleaulax and close relatives, we also identified genes encoding plastid-targeted DNApol-III subunits (including alpha) in nuclear genomes of unicellular and multicellular lineages of Archaeplastida that form, along with those of Cryptophyceae, monophyletic clades firmly positioned within Cyanobacteria. Together, our results reveal a previously overlooked retention of bacterial DNA replication machinery from plastid primary endosymbiosis in Archaeplastida, its acquisition by Cryptophyceae during secondary endosymbiosis, and its direct role in contemporary plankton as a facilitator of kleptoplastidic photosynthetic activity by heterotrophic ciliates.

microbiology↗

Metatranscriptome data support the existence of two distinct morphotypes in a single parmalean species in natural environments

Parmales (Bolidophyceae), the closest relatives of diatoms, includes isolates exhibiting one of two distinct morphotypes: a silicified non-flagellated form (S-type) and a naked flagellated form (F-type). Although alternation of these two forms for a single isolate has not been formally established, previous studies hypothesized that these morphotypes represent alternating stages of a single parmalean. In this study, we investigated the global expression patterns of S- and F-type marker genes by integrating parmalean Metagenome-Assembled Genomes (MAGs) and the metatranscriptomic dataset from Tara Oceans. We detected the expression of both S- and F-type marker genes from individual environmental MAGs. This finding provides the first metatranscriptomic evidence that natural parmalean genomes possess the potential to manifest both morphotypes. Furthermore, our analysis revealed different geographical expression patterns between the two forms. The expression of F-type markers showed a broad distribution, whereas that of S-type markers was more restricted, suggesting distinct niches for the two morpho-phases. Moreover, S-type gene expression appears to require specific environmental triggers that lead to a higher population density, whereas F-type expression is rather constitutively maintained. Overall, our results support the hypothesis of a life cycle involving morphological switching and reconcile the long-standing discrepancy between the ubiquity of parmaleans in molecular surveys and the limited geographical range for the observation of silicified cells. Based on these patterns, we propose a threshold-based model in which F-type-dominated populations persist under conditions unfavorable for growth and a morphological switch to the S-type is triggered once environmental conditions exceed a critical threshold for growth.

microbiology↗

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↗

New deep-branching environmental plastid genomes on the algal tree of life

Marine algae support the entire ocean ecosystem and beyond. Algae in culture poorly represents their large environmental diversity, and we still have a limited understanding of their convoluted evolution by endosymbiosis. Here, we performed a phylogeny-guided plastid genome-resolved metagenomic survey of Tara Oceans expeditions. We present a curated resource of 660 new non-redundant plastid genomes of environmental pelagic algae. This catalogue vastly expands the plastid genome diversity within major algal groups, often corresponding to algae without closely related reference genomes. Notably, we recovered four plastid genomes, including one near complete, forming a deep-branching plastid lineage of nano-size algae that we informally named leptophytes. This group is globally distributed and generally rare, although it can reach relatively high abundance at least in the Arctic. A mitochondrial contig including 62 genes showing strong read coverage correlation with leptophytes was also recovered from these Arctic samples and assigned to this group. Leptophytes encompass the enigmatic marine plastid group DPL2, one of the very few known plastid groups not clearly belonging to any major algal groups and for which only 16S rDNA amplicon data is available. Extensive gene content comparison and organellar phylogenomics support the view that leptophytes are sister to haptophytes, and raise the intriguing possibility that cryptophytes acquired their plastids from haptophytes. Collectively, our study demonstrates that metagenomics can reveal currently hidden diversity of organellar genomes, and shows the importance of including this diversity to improve models for plastid evolution.

evolutionary biology↗

An ocean of opsins

In this study, we explored the diversity and evolution of opsins using meta-omic data from the TARA Oceans and TARA Polar Circle expeditions, one of the largest marine datasets available. By using molecular clustering and phylogenetic analyses, we identified and characterized opsins across various taxonomic groups and gene subfamilies. Our results indicate that the majority of opsin sequences belong to arthropods and vertebrates. However, we also detected sequences from all major opsin subfamilies, including r-opsin, c-opsin, xenopsin, and Group-4 opsins. Despite the broad taxonomic scope, no novel opsin gene families were discovered, suggesting a comprehensive understanding of opsin diversity in marine ecosystems. Additionally, we present novel opsin sequences from less-studied taxa, which may serve as a valuable resource for future research into opsin function and diversity.

evolutionary biology↗

Transportome remodeling of a symbiotic microalga inside a planktonic host

Metabolic exchange is one of the foundations of symbiotic associations between organisms and is a driving force in evolution. In the ocean, photosymbiosis between heterotrophic host and microalgae is powered by photosynthesis and relies on the transfer of organic carbon to the host (e.g. sugars). Yet, the identity of transferred carbohydrates as well as the molecular mechanisms that drive this exchange remain largely unknown, especially in unicellular photosymbioses that are widespread in the open ocean. Combining genomics, single-holobiont transcriptomics and environmental metatranscriptomics, we revealed the transportome of the marine microalga Phaeocystis in symbiosis within acantharia, with a focus on sugar transporters. At the genomic level, the sugar transportome of Phaeocystis is comparable to non-symbiotic haptophytes. By contrast, we found significant remodeling of the expression of the transportome in symbiotic microalgae compared to the free-living stage. More particularly, 32% of sugar transporter genes were differentially expressed. Several of them, such as GLUTs, TPTs and aquaporins, with glucose, triose-phosphate sugars and glycerol as potential substrates, were upregulated at the holobiont and community level. We also showed that algal sugar transporter genes exhibit distinct temporal expression patterns during the day. This reprogrammed transportome indicates that symbiosis has a major impact on sugar fluxes within and outside the algal cell, and highlights the complexity and the dynamics of metabolic exchanges between partners. This study improves our understanding of the molecular players of the metabolic connectivity underlying the ecological success of planktonic photosymbiosis and paves the way for more studies on transporters across photosymbiotic models.

cell biology↗

Network studies unveil new groups of highly divergent proteins in families as old as cellular life with important biological functions in the ocean

BackgroundMetagenomics has considerably broadened our knowledge of microbial diversity, unravelling fascinating adaptations and characterising multiple novel major taxonomic groups, e.g. CPR bacteria, DPANN and Asgard archaea, and novel viruses. Such findings profoundly reshaped the structure of the known tree of life and emphasised the central role of investigating uncultured organisms. However, despite significant progresses, a large portion of proteins predicted from metagenomes remain today unannotated, both taxonomically and functionally, across many biomes and in particular in oceanic waters, including at relatively lenient clustering thresholds. ResultsHere, we used an iterative, network-based approach for remote homology detection, to probe a dataset of 40 million ORFs predicted in marine environments. We assessed the environmental diversity of 53 gene families as old as cellular life, broadly distributed across the Tree of Life. About half of them harboured clusters of environmental homologues that diverged significantly from the known diversity of published complete genomes, with representatives distributed across all the oceans. In particular, we report the detection of environmental clades with new structural variants of essential genes (SMC), divergent polymerase subunits forming deep-branching clades in the polymerase tree, and variant DNA recombinases of unknown origin in the ultra-small size fraction. ConclusionsThese results indicate that significant environmental diversity may yet be unravelled even in strongly conserved gene families. Protein sequence similarity network approaches, in particular, appear well-suited to highlight potential sources of biological novelty and make better sense of microbial dark matter across taxonomical scales.

evolutionary biology↗

Picoeukaryotic photosynthetic potential is functionally redundant but taxonomically structured at global scale

Primary production, performed by RUBISCO, and often associated with carbon concentration mechanisms, is of major importance in the oceans. Thanks to growing metagenomic resources (e.g., eukaryotic Metagenome-Assembled-Genomes; MAGs), we provide the first reproducible machine-learning-based framework to derive the potential biogeography of a given function, through the multi-output regression of the standardized number of reads of the associated genes on environmental climatologies. We use it to study the genomic potential of C4-photosynthesis of picoeukaryotes, a diverse and abundant group of marine unicellular photosynthetic organisms. We show that the genomic potential supporting C4-enzymes and RUBISCO exhibit strong functional redundancy and an important affinity towards tropical oligotrophic waters. This redundancy is then structured taxonomically by the dominance of Mamiellophyceae and Prymnesiophyceae in mid and high latitudes. Finally, unlike the genomic potential related to most C4-enzymes, the one of RUBISCO showed a clear pattern affinity for temperate waters.

ecology↗

Bursts of novel composite gene families at major nodes in animal evolution

A molecular level perspective on how novel phenotypes evolve is contingent on our understanding of how genomes evolve through time, and of particular interest is how novel elements emerge or are lost. Mechanisms of protein evolution such as gene duplication have been well established. Studies of gene fusion events show they often generate novel functions and adaptive benefits. Identifying gene fusion and fission events on a genome scale allows us to establish the mode and tempo of emergence of composite genes across the animal tree of life, and allows us to test the repeatability of evolution in terms of determining how often composite genes can arise independently. Here we show that [~]5% of all animal gene families are composite, and their phylogenetic distribution suggests an abrupt, rather than gradual, emergence during animal evolution. We find that gene fusion occurs at a higher rate than fission (73.3% vs 25.4%) in animal composite genes, but many gene fusions (79% of the 73.3%) have more complex patterns including subsequent fission or loss. We demonstrate that nodes such as Bilateria, Euteleostomi, and Eutheria, have significantly higher rates of accumulation of composite genes. We observe that in general deuterostomes have a greater amount of composite genes as compared to protostomes. Intriguingly, up to 41% of composite gene families have evolved independently in different clades showing that the same solutions to protein innovation have evolved time and again in animals. Significance statementNew genes emerge and are lost from genomes over time. Mechanisms that can produce new genes include, but are not limited to, gene duplication, retrotransposition, de novo gene genesis, and gene fusion/fission. In this work, we show that new genes formed by fusing distinct homologous gene families together comprise a significant portion of the animal proteome. Their pattern of emergence through time is not gradual throughout the animal phylogeny - it is intensified on nodes of major transition in animal phylogeny. Interestingly, we see that evolution replays the tape frequently in these genes with 41% of gene fusion/fission events occurring independently throughout animal evolution.

evolutionary biology↗

kmindex and ORA: indexing and real-time user-friendly queries in terabytes-sized complex genomic datasets

Public sequencing databases contain vast amounts of biological information, yet they are largely underutilized as one cannot efficiently search them for any sequence(s) of interest. We present kmindex, an innovative approach that can index thousands of highly complex metagenomes and perform sequence searches in a fraction of a second. The index construction is an order of magnitude faster than previous methods, while search times are two orders of magnitude faster. With negligible false positive rates below 0.01%, kmindex outperforms the precision of existing approaches by four orders of magnitude. We demonstrate the scalability of kmindex by successfully indexing 1,393 complex marine seawater metagenome samples from the Tara Oceans project. Additionally, we introduce the publicly accessible web server "Ocean Read Atlas" (ORA) at https://ocean-read-atlas.mio.osupytheas.fr/, which enables real-time queries on the Tara Oceans dataset. The open-source kmindex software is available at https://github.com/tlemane/kmindex.

bioinformatics↗

PhotoEukStein: Towards an omics-based definition of unicellular eukaryote phototrophs functional traits via metabolic modelling

Defining biological functional traits for unicellular organisms relies on comprehending the set and combination of the biochemical reactions their genomes encode for. This network of biochemical reactions defines the metabolic strategy organisms and communities use. Understanding the functional traits of unicellular organisms involves studying the combination of biochemical reactions encoded in their genomes. These reactions determine the metabolic strategy that organisms and communities use to grow in a specific environment. While prokaryotes have been extensively studied for their metabolic networks, eukaryotes have lagged behind due to the complexity of their genomes and the need for a better understanding of their metabolism. We have created PhotoEukstein, a meta-metabolic model for unicellular phototrophic eukaryotes. This meta-model enables quick and automated derivation of Genome-Scale Metabolic models directly from genomes. We have used it to analyse 533 environmental genomes and marine eukaryotic unicellular plankton transcriptomes. These models can help predict functional traits that cannot be purely deducted from taxonomic information or the listing of metabolic reactions encoded by the genome. They provide the opportunity to build connections with Earth System Models to pinpoint environmental parameters to capture specific functional traits.

systems biology↗

Genomic adaptation of giant viruses in polar oceans

Despite being perennially frigid, polar oceans form an ecosystem hosting high and unique biodiversity. Various organisms show different adaptative strategies in this habitat, but how viruses adapt to this environment is largely unknown. Viruses of phyla Nucleocytoviricota and Mirusviricota are groups of eukaryote-infecting large and giant DNA viruses with genomes encoding a variety of functions. Here, by leveraging the Global Ocean Eukaryotic Viral database, we investigate the biogeography and functional repertoire of these viruses at a global scale. We first confirm the existence of an ecological barrier that clearly separates polar and nonpolar viral communities, and demonstrate that temperature drives dramatic changes in the virus-host network at the polar/nonpolar boundary. Ancestral niche reconstruction suggests that adaptation of these viruses to polar conditions has occurred repeatedly over the course of evolution, with polar-adapted viruses in the modern ocean being scattered across their phylogeny. Numerous viral genes are specifically associated with polar adaptation, although most of their homologues are not identified as polar-adaptive genes in eukaryotes. These results suggest that giant viruses adapt to cold environments by changing their functional repertoire, and this viral evolutionary strategy is independent of the polar adaptation of their hosts.

microbiology↗

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↗

Whole-genome scanning reveals selection mechanisms in epipelagic Chaetoceros diatom populations

Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms adapt to different oceanic ecoregions is essential given their short generation times, which may allow rapid adaptations to different environments; and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros, the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single nucleotide variants identified within the different MAG populations allowed us to draw a first landscape of Chaetoceros genetic diversity and to reveal an elevated genetic structure in some Arctic Ocean populations with FST levels ranging up to [&ge;] 0.2. Genetic differentiation patterns of closely related Chaetoceros populations appear to be correlated with abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate and phosphate (e.g., polyamine synthase), that were further confirmed in Chaetoceros transcriptomes. Altogether, these results provide new insights and perspectives into diatom metapopulation genomics through the integration of metagenomic and environmental data.

ecology↗

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↗

Linking extreme seasonality and gene expression in arctic marine protists

At high latitudes, strong seasonal differences in light availability affect marine organisms and restrict the timing of ecosystem processes. Marine protists are key players in Arctic aquatic ecosystems, yet little is known about their ecological roles over yearly cycles. This is especially true for the dark polar night period, which up until recently was assumed to be devoid of biological activity. A 12 million transcripts catalogue was built from 0.45-10 m protist assemblages sampled over 13 months in a time series station in an arctic fjord in Svalbard. Community gene expression was correlated with seasonality, with light as the main driving factor. Transcript diversity and evenness were higher during polar night compared to polar day. Light-dependent functions had higher relative expression during polar day, except phototransduction. 64% of the most expressed genes could not be functionally annotated, yet up to 78% were identified in arctic samples from Tara Oceans, suggesting that arctic marine assemblages are distinct from those from other oceans. Our study increases understanding of the links between extreme seasonality and biological processes in pico- and nanoplanktonic protists. Our results set the ground for future monitoring studies investigating the seasonal impact of climate change on the communities of microbial eukaryotes in the High Arctic.

microbiology↗

Genomic adaptation of the picoeukaryote Pelagomonas calceolata to temperate iron-poor oceans revealed by a chromosome-scale genome sequence.

The smallest phytoplankton species are key actors in oceans biogeochemical cycling and their abundance and distribution are affected with global environmental changes. Picoalgae (cells <2{micro}m) of the Pelagophyceae class encompass coastal species causative of harmful algal blooms while others are cosmopolitan and abundant in open ocean ecosystems. Despite the ecological importance of Pelagophytes, only a few genomic references exist limiting our capacity to identify them and study their adaptation mechanisms in a changing environment. Here, we report the complete chromosome-scale assembled genome sequence of Pelagomonas calceolata. We identified unusual large low-GC and gene-rich regions potentially representing centromeres. These particular genomic structures could be explained by the absence of genes from a recombination pathway involving double Holiday Junctions. We identified a large repertoire of genes involved in inorganic nitrogen sensing and uptake and several genes replacing iron-requiring proteins potentially explaining P. calceolata ecological success in oligotrophic waters. Finally, based on this high-quality assembly, we evaluated P. calceolata relative abundance in all oceans using environmental Tara Oceans datasets. Our results suggest that P. calceolata is one of the most abundant eukaryotic species in the oceans with a relative abundance favoured by high temperature and iron-poor conditions. Climate change projections based on its relative abundance suggest an extension of the P. calceolata habitat toward the poles at the end of this century. Collectively, these findings reveal the ecological importance of P. calceolata and lay the foundation for a global scale analysis of the adaptation and acclimation strategies of picoalgae in a changing environment.

genomics↗