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Delmont, T. O.

Publications and source records attributed to Delmont, T. O..

At least 19 recordsLinked to original sources

Genomic detection of domoic acid biosynthesis uncovers expanded toxigenic diversity across Pseudo-nitzschia diatoms

Domoic acid (DA) production by diatom genus Pseudo-nitzschia causes recurrent harmful algal blooms with major consequences for marine ecosystems, fisheries, and human health. Predicting DA risk remains challenging because toxin production varies across morphologically similar and cryptic lineages. Consequently, morphology or single marker genes often fail to resolve toxigenic potential. Here, we expand genomic resources for Pseudo-nitzschia by generating and compiling high-quality genomes spanning diverse species and biogeographic origins, establishing a genus-wide phylogenomic framework to investigate the distribution and evolution of the DA biosynthesis (dab) gene cluster. Among chemically characterized strains, the dab pathway was detected in species only with confirmed DA production. While the cluster exhibits a conserved core structure, several lineages display signatures of ongoing evolution, including intronization, locus rearrangement, and pseudogenization. One striking example of dab variation occurs in toxigenic P. australis strains, in which its biochemically validated isodomoic acid A synthase-encoding gene dabC is located outside the dab locus. Metatranscriptomic surveys reveal widespread environmental dab expression across size classes and species, implicating taxa not typically associated with environmental DA events, such as P. cf. obtusa and P. cf. plurisecta. To connect dab expression with chemical output, nutrient limitation experiments in the historically inconsistent DA producer P. pseudodelicatissima combined transcriptional profiling and nontargeted metabolomics demonstrating coordinated dab expression across distinct co-expression modules and DA accumulation in response to silicon limitation. Together, these results refine the phylogenetic scope of DA production and provide a genome-resolved basis for improved molecular monitoring of toxigenic diversity.

genetics↗

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↗

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↗

Ribosomal protein phylogeography offers quantitative insights into the efficacy of genome-resolved surveys of microbial communities

The increasing availability of microbial genomes is essential to gain insights into microbial ecology and evolution that can propel biotechnological and biomedical advances. Recent advances in genome recovery have significantly expanded the catalogue of microbial genomes from diverse habitats. However, the ability to explain how well a set of genomes account for the diversity in a given environment remains challenging for individual studies or biome-specific databases. Here we present EcoPhylo, a computational workflow to characterize the phylogeography of any gene family through integrated analyses of genomes and metagenomes, and apply this approach to ribosomal proteins to quantify phylogeny-aware genome recovery rates in two genome-resolved investigations of the human gut and oral cavity. Our results demonstrate that EcoPhylo reveals highly resolved, reference-free, multi-domain phylogenies in conjunction with distribution patterns of individual clades across environments, providing a means to assess genome recovery in individual studies and benchmark genome collections.

microbiology↗

Unexpected diversity and ecological significance of uncultivable large virus-like particles in aquatic environments

The discovery of Jumbo phages and giant viruses of microeukaryotes has transformed our perception of the virosphere. Metagenomic and metatranscriptomic data further highlight their diversity and ecological impact. Nevertheless, sequence-based approaches fail to take into account the morphological diversity of non-cultivated viruses, resulting in our fragmented understanding of their nature and role in the environment. Here, we combined flow cytometry and electron microscopy to uncover both previously unsuspected morphological diversity as well as significant abundances of large viruses in aquatic environments. We discovered four new viral morphotypes, all of which were associated with microeukaryotes. We also obtained insights into the multi-year dynamics of the abundances of both giant microeukaryotic viruses and Jumbo phages. This work deepens our understanding of large viruses and reveals their key role as regulators of microbial communities.

ecology↗

Egoviruses: distant relatives of poxviruses abundant in the gut microbiome of humans and animals worldwide

Large and giant double-stranded DNA viruses are diverse and highly prevalent in the environment where they substantially affect the ecology and evolution of eukaryotes1-4. Until now, they were only sporadically found in the digestive system of vertebrates5-7. Here, we present the discovery of a diversified group of DNA viruses with large linear genomes dubbed egoviruses that comprise a putative viral order most closely related to animal-infecting poxviruses. Egoviruses are found worldwide, almost exclusively in the digestive system of humans, livestock and wild animals. One egovirus is human-specific, evolutionarily constrained, and spread across continents, demonstrating a long-term association between egoviruses and the human population. Analysis of eukaryotic homologs of egovirus core genes suggests that these viruses primarily infect Trichostomatia (Ciliates), which play a central role in ruminant digestive processes8, and Parabasalia (Metamonada), which directly influence animal immunity and gut microbiome ecology9. Egoviruses also contributed to the genetic makeup of polintons, endogenous viruses that proliferated in genomes of Trichomonas vaginalis10 and its close relatives among the Parabasalia. Unlike poxviruses that form brick-shaped virions, egoviruses are predicted to form multilayered icosahedral capsids resembling those of asfuviruses and likely representing the ancestral virion structure. Egoviruses currently are the only known clade of eukaryotic DNA viruses abundant in the animal digestive system. Phylogenomic analysis suggests an evolutionary scenario whereby egovirus-like ancestors of poxviruses infected anaerobic unicellular eukaryotes inside the gut of ancestral animals, before transitioning to animal cell infection which was accompanied by the virion metamorphosis.

microbiology↗

Complex genomes of early nucleocytoviruses revealed by ancient origins of viral aminoacyl-tRNA synthetases

Aminoacyl-tRNA synthetases (aaRSs), also known as tRNA ligases, are essential enzymes in translation. Owing to their functional essentiality, these enzymes are conserved in all domains of life and used as informative markers to trace the evolutionary history of cellular organisms. Unlike cellular organisms, viruses generally lack aaRSs because of their obligate parasitic nature, but several large and giant DNA viruses in the phylum Nucleocytoviricota encode aaRSs in their genomes. The discovery of viral aaRSs led to the idea that the phylogenetic analysis of aaRSs can shed light on ancient viral evolution. However, conflicting results have been reported from previous phylogenetic studies: one posited that nucleocytoviruses recently acquired their aaRSs from their host eukaryotes, while another hypothesized that the viral aaRSs have ancient origins. Here, we investigated 4,168 nucleocytovirus genomes, including metagenome-assembled genomes derived from large-scale metagenomic studies. In total, we identified 780 viral aaRS sequences in 273 viral genomes. We generated and examined phylogenetic trees of these aaRSs with a large set of cellular sequences to trace evolutionary relationships between viral and cellular aaRSs. The analyses firmly establish that the origins of some viral aaRSs predate the last common eukaryotic ancestor. Inside viral aaRS clades, we identify intricate evolutionary trajectories of viral aaRSs with horizontal transfers, losses, and displacements. Overall, these results suggest that ancestral nucleocytoviruses already developed complex genomes with an expanded set of aaRSs in the proto-eukaryotic era.

evolutionary biology↗

The defensome of complex bacterial communities

Bacteria have developed various defense mechanisms to avoid infection and killing in response to the fast evolution and turnover of viruses and other genetic parasites. Such pan-immune system (or defensome) encompasses a growing number of defense lines that include well-studied innate and adaptive systems such as restriction-modification, CRISPR-Cas and abortive infection, but also newly found ones whose mechanisms are still poorly understood. While the abundance and distribution of defense systems is well-known in complete and culturable genomes, there is a void in our understanding of their diversity and richness in complex microbial communities. Here we performed a large-scale in-depth analysis of the defensomes of 7,759 high-quality bacterial population genomes reconstructed from soil, marine, and human gut environments. We observed a wide variation in the frequency and nature of the defensome among large phyla, which correlated with lifestyle, genome size, habitat, and geographic background. The defensomes genetic mobility, its clustering in defense islands, and genetic variability was found to be system-specific and shaped by the bacterial environment. Hence, our results provide a detailed picture of the multiple immune barriers present in environmentally distinct bacterial communities and set the stage for subsequent identification of novel and ingenious strategies of diversification among uncultivated microbes.

genomics↗

A 2-million-year-old microbial and viral communities from the Kap Kobenhavn Formation in North Greenland

Environmental DNA (eDNA) from the 2-million-year-old Kap Kobenhavn Formation of northern Greenland has revealed an ecosystem of plants and animals with no contemporary analogue1. Here, we reconstruct the microbial (bacterial, archaeal, and viral) communities that thrived at the site during this time. By leveraging a novel analytical framework that integrates taxonomic profiling, DNA damage estimates, and functional reconstructions, we identify and distinguish pioneer microbial communities from later permafrost microbial assemblages. We show that at the time of sediment deposition, the terrestrial input at the Kap Kobenhavn site originated from a palustrine wetland, suggesting warmer, non-permafrost conditions. During this period, the detection of methanogenic archaea and signals of their carbon metabolism is consistent with Kap Kobenhavn and similar northern ecosystems contributing moderate methane emissions. Intriguingly, we discover a remarkable nucleotide sequence similarity--exceeding 98%--between pioneer methanogens and present-day analogues in thawing permafrost. This aligns with the concept of "time-traveling" microbes2 surviving across geological time and waiting for conditions to turn favourable rather than evolving to adapt to changing conditions. Importantly, in contrast to the plant and animal communities of the Kap Kobenhavn, a striking similarity in microbial composition to that of a contemporary thawing Arctic suggests that microbial communities may serve as the first indication of broader climate-driven ecosystem disruptions.

microbiology↗

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↗

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↗

AGNOSTOS-DB: a resource to unlock the uncharted regions of the coding sequence space

Genomes and metagenomes contain a considerable percentage of genes of unknown function, which are often excluded from downstream analyses limiting our understanding of the studied biological systems. To address this challenge, we developed AGNOSTOS, a combined database-computational workflow resource that unifies the known and unknown coding sequence space of genomes and metagenomes. Here, we present AGNOSTOS-DB, an extensive database of high-quality gene clusters enriched with functional, ecological and phylogenetic information. Moreover, AGNOSTOS allows integrating new data into existing AGNOSTOS-DBs, maximizing the information retrievable for the genes of unknown function. As a proof of concept, we provide a seed database that integrates the predicted genes from marine and human metagenomes, as well as from Bacteria, Archaea, Eukarya and giant viruses environmental and cultivar genomes. The seed database comprises 6,572,081 gene clusters connecting 342 million genes and represents a comprehensive and scalable resource for the inclusion and exploration of the unknown fraction of genomes and metagenomes.

microbiology↗

Uncharted biosynthetic potential of the ocean microbiome

Microbes are phylogenetically and metabolically diverse. Yet capturing this diversity, assigning functions to host organisms and exploring the biosynthetic potential in natural environments remains challenging. We reconstructed >25,000 draft genomes, including from >2,500 uncharacterized species, from globally-distributed ocean microbial communities, and combined them with [~]10,000 genomes from cultivated and single cells. Mining this resource revealed [~]40,000 putative biosynthetic gene clusters (BGCs), many from unknown phylogenetic groups. Among these, we discovered Candidatus Eudoremicrobiaceae as one of the most biosynthetically diverse microbes detected to date. Discrete transcriptional states structuring natural populations were associated with a potentially niche-partitioning role for BGC products. Together with the characterization of the first Eudoremicrobiaceae natural product, this study demonstrates how microbiomics enables prospecting for candidate bioactive compounds in underexplored microbes and environments.

microbiology↗

Heterotrophic bacterial diazotrophs are more abundant than their cyanobacterial counterparts in metagenomes covering most of the sunlit ocean

Biological nitrogen fixation is a major factor contributing to microbial primary productivity in the open ocean. The current view depicts a few cyanobacterial diazotrophs as the most relevant marine nitrogen fixers, whereas heterotrophic diazotrophs are more diverse and considered to have lower impacts on the nitrogen balance. Here, we used 891 Tara Oceans metagenomes to create a manually curated, non-redundant genomic database corresponding to free-living, as well as filamentous, colony-forming, particle-attached and symbiotic bacterial and archaeal populations occurring in the surface of five oceans and two seas. Notably, the database provided the genomic content of eight cyanobacterial diazotrophs including Trichodesmium populations and a newly discovered population similar to Richelia, as well as 40 heterotrophic bacterial diazotrophs organized into three main functional groups that considerably expand the known diversity of abundant marine nitrogen fixers compared to previous genomic surveys. Critically, these 48 populations may account for more than 90% of cells containing known nifH genes and occurring in the sunlit ocean, suggesting that the genomic characterization of the most abundant marine diazotrophs may be nearing completion. The newly identified heterotrophic bacterial diazotrophs are widespread, express their nifH genes in situ, and co-occur under nitrate-depleted conditions in large size fractions where they might form aggregates providing the low-oxygen microenvironments required for nitrogen fixation. Most significantly, we found heterotrophic bacterial diazotrophs to be more abundant than cyanobacterial diazotrophs in most metagenomes from the open oceans and seas. This large-scale environmental genomic survey emphasizes the considerable potential of heterotrophs in the marine nitrogen balance.

microbiology↗

Environmental genomics points to non-diazotrophic Trichodesmium species abundant and widespread in the open ocean

Filamentous and colony-forming cells within the cyanobacterial genus Trichodesmium might account for nearly half of nitrogen fixation in the sunlit ocean, a critical mechanism that sustains planktons primary productivity at large-scale. Here, we report the genome-resolved metagenomic characterization of two newly identified marine species we tentatively named Ca. Trichodesmium miru and Ca. Trichodesmium nobis. Near-complete environmental genomes for those closely related candidate species revealed unexpected functional features including a lack of the entire nitrogen fixation gene apparatus and hydrogen recycling genes concomitant with the enrichment of nitrogen assimilation genes and apparent acquisition of the nirb gene from a non-cyanobacterial lineage. These comparative genomic insights were cross-validated by complementary metagenomic investigations. Our results contrast with the current paradigm that Trichodesmium species are necessarily capable of nitrogen fixation. The black queen hypothesis could explain gene loss linked to nitrogen fixation among Trichodesmium species, possibly triggered by gene acquisitions from the colony epibionts. Critically, the candidate species are not only widespread in the 3-2000 m planktonic size fraction of the surface of the oceans and seas, but might also substantially expand the ecological niche of Trichodesmium, stressing the need to disconnect taxonomic signal for this genus from a microbial communitys ability to fix nitrogen. Especially, differentiating diazotrophic from non-diazotrophic populations when counting Trichodesmium filaments and colonies might help refine our understanding of the marine nitrogen balance. While culture representatives are needed to move beyond metagenomic insights, we are reminded that established links between taxonomic lineages and functional traits might not always hold true.

microbiology↗

Discovery of viral myosin genes with complex evolutionary history within plankton

Nucleocytoplasmic large DNA viruses (NCLDVs) infect diverse eukaryotes and form a group of viruses with capsids encapsulating large genomes. Recent studies are increasingly revealing a spectacular array of functions encoded in their genomes, including genes for energy metabolisms, nutrient uptake, as well as cytoskeleton. Here, we report the discovery of genes homologous to myosins, the major eukaryotic motor proteins previously unrecognized in the virosphere, in environmental genomes of NCLDVs from the surface of the oceans. Interestingly, these genes were often accompanied by kinesin genes in the environmental genomes, suggesting a role of these viral proteins in the intracellular viral particle transport. Phylogenetic analyses indicate that most viral myosins (named "virmyosins") belong to the Imitervirales order, except for one belonging to the Phycodnaviridae family. On the one hand, the phylogenetic positions of virmyosin-encoding Imitervirales are scattered within the Imitervirales. On the other hand, Imitervirales virmyosin genes form a monophyletic group in the phylogeny of diverse myosin sequences. Furthermore, phylogenetic trends for the virmyosin genes and viruses containing them were incongruent. Based on these results, we argue that multiple transfers of myosin homologs have occurred not only from eukaryotes to viruses but also between viruses, supposedly during co-infections of the same host.

microbiology↗