Abstract 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 activity 1–3 . 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 lost 4 . 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.

Marine ecosystems are hotspots of biodiversity and biogeochemical activity, yet much of their complexity remains largely inaccessible without genome-resolved data. Here we present a curated dataset of 52 eukaryotic metagenome-assembled genomes (MAGs) reconstructed from samples collected between April 2019 and January 2020 at three NEREA (Naples Ecological REsearch for Augmented observatories) sites in the Gulf of Naples. NEREA is a coastal observatory integrating physical, chemical and biological measurements with state-of-the-art metagenomics. The eukaryotic MAGs have an average completeness of ~55% and genome size of ~20 Mb. Predicted proteins were functionally annotated against UniProtKB, InterPro, and eggNOG databases, and each MAG was taxonomically classified using a curated RNA polymerase A reference dataset. The recovered MAGs encompass diverse eukaryotic lineages, primarily Ochrophyta, Chlorophyta and Haptophyta. Building on the Tara Oceans eukaryotic MAG legacy, this release represents the first reconstruction of eukaryotic MAGs from a coastal time series, enabling temporal and functional analyses of eukaryotic plankton.

Marine microbiology has long considered ultrasmall (<0.2 μm) 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.

Climatic changes in the physical environment modulate biogeochemical cycles, biodiversity, and trophic interactions in the Central Arctic Ocean (CAO). Physical processes and sea-ice conditions are highly seasonal in the CAO and dependent on interactions that occur throughout the evolution of the upper ocean–sea ice–lower atmosphere system. Understanding these seasonal interactions is critical to comprehending and predicting the long-term trends as the CAO moves towards ice-free summers and to informing future policy decisions at the core of ongoing discussions concerning the CAO Fisheries agreement, for example, at the Arctic Council and International Council for Exploration of the Sea working group on the CAO. Here, we review current knowledge of the physical environment, biogeochemical cycles, and biodiversity in the waters of the CAO, identify emerging research questions, and introduce the science plan for the first Tara Polaris drift onboard the Tara Polar Station to advance knowledge and address these questions. Despite increased observational programmes in the CAO over the past years, for example, the Nansen and Amundsen Basin Observational System (NABOS) and Multidisciplinary drifting Observatory for the Study of Arctic Climate (MOSAiC), extensive knowledge gaps remain in relation to ocean stratification, sea ice and lightscape, nitrogen fixation and nutrient fluxes, carbon export and transfer, sympagic-pelagic coupling, aerosol production, contaminant transport and transformation, chronobiology, and fish distribution. Further knowledge on overall CAO biodiversity, ecosystem functionality and interannual variability is also critically needed. We describe a way forward to address these knowledge gaps using ice-tethered and profiling instruments coupled with multi-omics, culturing, and imagery approaches deployed from Tara Polar Station during the first of ten Tara Polaris drifts designed to facilitate detection of interannual variability and change over time.

The Arctic Ocean is currently experiencing, at the forefront of global concerns, the pressures of climate change and global pollution. To boost our ability to understand the state of this ecosystem, its evolution in this context and its resilience, the Tara Ocean Foundation has built the Tara Polar Station (TPS), intended to become a permanent observatory of the central Arctic Ocean. The objective of this initiative is threefold: to deepen our knowledge of the foundations of life in an ice-covered polar ocean, to better understand the dynamics of the coupled ocean-ice-atmosphere system and the role of living organisms, and to identify long-term trends in the main characteristics of the Central Arctic Ocean ecosystem resulting from global change. In this article, we describe the vision that guided the development of the Tara Polaris scientific programme, and more specifically the first of ten transpolar drifts that will be undertaken over the next 20 years aboard the TPS (Tara Polaris I, II, III, etc.). The research activities of the Tara Polaris I expedition will be grouped under four specific but interrelated themes: biosphere-atmosphere interactions, epi- and mesopelagic life in an ice-covered ocean, life in sea ice, and pollution. In addition, a theme that cuts across all environmental compartments and disciplines, and is implemented on all Tara Polaris expeditions, is the establishment of an observatory that will monitor the main sentinels of this ecosystem. This umbrella article introduces these different themes, which are then described in more detail in four other articles in this Special Feature, in addition to an article describing the technical characteristics of the TPS.

Abstract 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.

Polar oceanographic regions are exposed to rapid changes in temperature, salinity, and light fields that determine microbial species distributions, but resilience to an increasingly unstable climate is unknown. To unravel microbial genomic potential of the Northern Baffin Bay’s polynya, we constructed eight metagenomes from the same latitude but targeting two sides of Pikialasorsuaq (The North Water) that differ by current systems, stratification, and temperature regimes. Samples from the surface and subsurface chlorophyll maximum (SCM) of both sides were collected 13 months apart. Details of metabolic pathways were determined for 18 bacteria and 10 microbial eukaryote metagenome-assembled genomes (MAGs). The microbial eukaryotic MAGs were associated with the dominant green algae in the Mamiellales and diatoms in the Mediophyceae, which tended to respectively dominate the eastern and western sides of Pikialasorsuaq. We show that microbial community taxonomic and functional signatures were ca. 80% similar at the latitude sampled with only 20% of genes associated with local conditions. From the metagenomes we found genes involved in osmotic regulation, antifreeze proteins, and photosystem protection, with hydrocarbon biodegradation and methane oxidation potential detected. The shared genomic compliment was consistent with adaptation to the Arctic’s extreme fluctuating conditions, with implications for their evolutionary history and the long-term survival of a pan-arctic microbiome. In particular, previously unrecognized genetic capabilities for methane bio-attenuation and hydrocarbon metabolism in eukaryotic phytoplankton suggest adaptation to dark conditions that will remain, despite climate warming, in the high latitude offshore waters of a future Arctic.

Microbiome research has grown substantially over the past decade in terms of the range of biomes sampled, identified taxa, and the volume of data derived from the samples. In particular, experimental approaches such as metagenomics, metabarcoding, metatranscriptomics and metaproteomics have provided profound insights into the vast, hitherto unknown, microbial biodiversity. The ELIXIR Marine Metagenomics Community, initiated amongst researchers focusing on marine microbiomes, has concentrated on promoting standards around microbiome-derived sequence analysis, as well as understanding the gaps in methods and reference databases, and identifying solutions to the computational overheads of performing such analyses. Nevertheless, the methods used and the challenges faced are not confined to marine microbiome studies, but are broadly applicable to other biomes. Thus, expanding this Marine Metagenomics Community to a more inclusive ELIXIR Microbiome Community will enable it to encompass a broader range of biomes and link expertise across ‘omics technologies. Furthermore, engaging with a large number of researchers will improve the efficiency and sustainability of bioinformatics infrastructure and resources for microbiome research (standards, data, tools, workflows, training), which will enable a deeper understanding of the function and taxonomic composition of the different microbial communities.

Microbiome research has grown substantially over the past decade in terms of the range of biomes sampled, identified taxa, and the volume of data derived from the samples. In particular, experimental approaches such as metagenomics, metabarcoding, metatranscriptomics and metaproteomics have provided profound insights into the vast, hitherto unknown, microbial biodiversity. The ELIXIR Marine Metagenomics Community, initiated amongst researchers focusing on marine microbiomes, has concentrated on promoting standards around microbiome-derived sequence analysis, as well as understanding the gaps in methods and reference databases, and identifying solutions to the computational overheads of performing such analyses. Nevertheless, the methods used and the challenges faced are not confined to marine microbiome studies, but are broadly applicable to other biomes. Thus, expanding this Marine Metagenomics Community to a more inclusive ELIXIR Microbiome Community will enable it to encompass a broader range of biomes and link expertise across 'omics technologies. Furthermore, engaging with a large number of researchers will improve the efficiency and sustainability of bioinformatics infrastructure and resources for microbiome research (standards, data, tools, workflows, training), which will enable a deeper understanding of the function and taxonomic composition of the different microbial communities.

Marine algae support the entire ocean ecosystem and greatly impact planetary biology. The availability of 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 manually curated resource of nearly 700 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. We also recovered four genomes, including one near complete, forming a deep-branching plastid lineage of nano-size algae (<5 um) that we informally named leptophytes. This group is globally distributed and generally rare, although it can reach relatively high abundance notably in the Arctic. 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 amplicon data is available. Extensive phylogenetic analyses based on 93 plastid genes and gene content comparison firmly place leptophytes together with haptophytes and cryptophytes, although the exact relationships remain ambiguous. 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. ### Competing Interest Statement The authors have declared no competing interest.

Metagenomics 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. Here, 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 core gene families broadly distributed across the Tree of Life, with essential functions including translational, replication and trafficking processes. For nearly half of them, we identified clusters of remote environmental homologues that showed divergence from the known genetic diversity comparable to the divergence between Archaea and Bacteria, with representatives distributed across all the oceans. In particular, we report the detection of environmental clades with new structural variants of essential SMC (Structural Maintenance of Chromosomes) genes, divergent polymerase subunits forming deep-branching clades in the polymerase tree, and variant DNA recombinases in Bacteria as well as viruses. These 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.

Marine algae underpin entire ocean ecosystems. Yet algae in culture poorly represent their large environmental diversity, and we have a limited understanding of their convoluted evolution by endosymbiosis. Here, we perform 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 marine algae, vastly expanding plastid genome diversity within major algal groups, including many without closely related reference genomes. Notably, we recover four plastid genomes, including one near-complete, forming a deep-branching plastid lineage of nano-size algae that we informally name leptophytes. This group is globally distributed and generally rare, although it can reach relatively high abundance in the Arctic. A near-complete mitochondrial genome showing strong co-occurrence with leptophyte plastids is also recovered and assigned to this group. Leptophytes encompass the enigmatic plastid group DPL2, one of the very few known plastid groups not clearly belonging to major algal groups and previously known only from 16S rDNA sequences. Comparative organellar genomics and phylogenomics indicate 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 hidden organellar diversity, and improve models of plastid evolution.

Mirusviruses infect unicellular eukaryotes and are related to tailed bacteriophages and herpesviruses. Here we expand the known diversity of mirusviruses by screening diverse metagenomic assemblies and characterizing 1,202 non-redundant environmental genomes. Mirusviricota comprises a highly diversified phylum of large and giant eukaryotic viruses that rivals the evolutionary scope and functional complexity of nucleocytoviruses. Critically, major Mirusviricota lineages lack essential genes encoding components of the replication and transcription machineries and, concomitantly, encompass numerous spliceosomal introns that are enriched in virion morphogenesis genes. These features point to multiple transitions from cytoplasmic to nuclear reproduction during mirusvirus evolution. Many mirusvirus introns encode diverse homing endonucleases, suggestive of a previously undescribed mechanism promoting the horizontal mobility of spliceosomal introns. Available metatranscriptomes reveal long-range trans-splicing in a virion morphogenesis gene. Collectively, our data strongly suggest that nuclei of unicellular eukaryotes across marine and freshwater ecosystems worldwide are a major niche for replication of intron-rich mirusviruses.

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 world’s ocean. By bridging genomic data with biogeochemical metrics, this study provides novel resources for integrating plankton at genomic resolution into next-generation biogeochemical models. ### Competing Interest Statement The authors have declared no competing interest. European Union, https://ror.org/019w4f821, 862923, 101082304 Royal Society, https://ror.org/03wnrjx87, RSRP\R\241002 UK NERC, NE/V011103/1

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 sequence similarity methods and phylogenetic analyses, we identified opsins across the different metazoan groups. Our results indicate that most of the opsin sequences belong to arthropods and vertebrates. We also detected sequences from all known opsin subfamilies, including r-opsin, c-opsin, xenopsin, and Group-4 opsins. Despite the broad taxonomic scope, no new opsin families were discovered; however, we provide valuable taxonomic insights into known opsin subfamilies and reinforce existing phylogenetic hypotheses. Additionally, we present novel opsin sequences from less-studied taxa, such as chaetognaths, rotifers, acoelomates, and tunicates, and which may serve as a valuable resource for future research into opsin function and diversity.

This document reports on the agenda, key points, and outcomes of the ELIXIR Microbiome Community's face-to-face and hybrid meeting, which took place on April 9-10, 2025, in Barcelona, Spain.

Carbon fixation is a key metabolic function shaping marine life, but the underlying taxonomic and functional diversity involved is only partially understood. Using metagenomic resources targeted at marine piconanoplankton, we provide a reproducible machine learning framework to derive the potential biogeography of genomic functions through the multi-output regression of gene read counts on environmental climatologies. Leveraging the Marine Atlas of Tara Oceans Unigenes, we investigate the genomic potential of primary production in the global ocean. The latter is performed by ribulose-1,5-bisphosphate carboxylase/oxygenase (RUBISCO) and is often associated with carbon concentration mechanisms in piconanoplankton, major marine unicellular photosynthetic organisms. We show that the genomic potential supporting C 4 enzymes and RUBISCO exhibits strong functional redundancy and important affinity toward tropical oligotrophic waters. This redundancy is taxonomically structured by the dominance of Mamiellophyceae and Prymnesiophyceae in mid and high latitudes. These findings enhance our understanding of the relationship between functional and taxonomic diversity of microorganisms and environmental drivers of key biogeochemical cycles.

Brown seaweeds are keystone species of coastal ecosystems, often forming extensive underwater forests, and are under considerable threat from climate change. In this study, analysis of multiple genomes has provided insights across the entire evolutionary history of this lineage, from initial emergence, through later diversification of the brown algal orders, down to microevolutionary events at the genus level. Emergence of the brown algal lineage was associated with a marked gain of new orthologous gene families, enhanced protein domain rearrangement, increased horizontal gene transfer events, and the acquisition of novel signaling molecules and key metabolic pathways, the latter notably related to biosynthesis of the alginate-based extracellular matrix, and halogen and phlorotannin biosynthesis. We show that brown algal genome diversification is tightly linked to phenotypic divergence, including changes in life cycle strategy and zoid flagellar structure. The study also showed that integration of large viral genomes has had a significant impact on brown algal genome content throughout the emergence of the lineage.

Native amine dehydrogenases offer sustainable access to chiral amines, so the search for scaffolds capable of converting more diverse carbonyl compounds is required to reach the full potential of this alternative to conventional synthetic reductive aminations. Here we report a multidisciplinary strategy combining bioinformatics, chemoinformatics and biocatalysis to extensively screen billions of sequences in silico and to efficiently find native amine dehydrogenases features using computational approaches. In this way, we achieve a comprehensive overview of the initial native amine dehydrogenase family, extending it from 2,011 to 17,959 sequences, and identify native amine dehydrogenases with non-reported substrate spectra, including hindered carbonyls and ethyl ketones, and accepting methylamine and cyclopropylamine as amine donor. We also present preliminary model-based structural information to inform the design of potential (R)-selective amine dehydrogenases, as native amine dehydrogenases are mostly (S)-selective. This integrated strategy paves the way for expanding the resource of other enzyme families and in highlighting enzymes with original features. Sustainable chemistry can benefit from biocatalysis, but a high diversity of enzymes is needed. Here, the authors screen billions of protein sequences to provide an overview of the native amine dehydrogenase family for amine synthesis.

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 hosts 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, 36% 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 reprogramed 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.