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Summary paragraph Plankton are essential in marine ecosystems. However, our knowledge of overall community structure is sparse due to inconsistent sampling across their very large organismal size range. Here we use diverse imaging methods to establish complete plankton inventories of organisms spanning five orders of magnitude in size. Plankton community size and trophic structure variation validate a long-held theoretical link between organism size-spectra and ecosystem trophic structures. We found that predator/grazer biomass and biovolume unexpectedly exceed that of primary producers at most (55%) locations, likely due to our better quantification of gelatinous organisms. Bottom- heavy ecosystems (the norm on land) appear to be rare in the ocean. Collectively, gelatinous organisms represent 30% of the total biovolume (8-9% of carbon) of marine plankton communities from tropical to polar ecosystems. Communities can be split into three extreme typologies: diatom/copepod-dominated in eutrophic blooms, rhizarian/chaetognath-dominated in oligotrophic tropical oceans, and gelatinous-dominated elsewhere. While plankton taxonomic composition changes with latitude, functional and trophic structures mostly depend on the amount of prey available for each trophic level. Given future projections of oligotrophication of marine ecosystems, our findings suggest that rhizarian and gelatinous organisms will increasingly dominate the apex position of planktonic ecosystems, leading to significant changes in the ocean’s carbon cycle.

Methane is a potent greenhouse gas contributing to global warming. Microorganisms largely drive the biogeochemical cycling of methane, yet little is known about viral contributions to methane metabolism (MM). We analyzed 982 publicly available metagenomes from host-associated and environmental habitats containing microbial MM genes, expanding the known MM auxiliary metabolic genes (AMGs) from three to 24, including seven genes exclusive to MM pathways. These AMGs are recovered on 911 viral contigs predicted to infect 14 prokaryotic phyla including Halobacteriota, Methanobacteriota, and Thermoproteota. Of those 24, most were encoded by viruses from rumen (16/24), with substantially fewer by viruses from environmental habitats (0–7/24). To search for additional MM AMGs from an environmental habitat, we generate metagenomes from methane-rich sediments in Vrana Lake, Croatia. Therein, we find diverse viral communities, with most viruses predicted to infect methanogens and methanotrophs and some encoding 13 AMGs that can modulate host metabolisms. However, none of these AMGs directly participate in MM pathways. Together these findings suggest that the extent to which viruses use AMGs to modulate host metabolic processes (e.g., MM) varies depending on the ecological properties of the habitat in which they dwell and is not always predictable by habitat biogeochemical properties.

A universal taxonomy of viruses is essential for a comprehensive view of the virus world and for communicating the complicated evolutionary relationships among viruses. However, there are major differences in the conceptualisation and approaches to virus classification and nomenclature among virologists, clinicians, agronomists, and other interested parties. Here, we provide recommendations to guide the construction of a coherent and comprehensive virus taxonomy, based on expert scientific consensus. Firstly, assignments of viruses should be congruent with the best attainable reconstruction of their evolutionary histories, i.e., taxa should be monophyletic. This fundamental principle for classification of viruses is currently included in the International Committee on Taxonomy of Viruses (ICTV) code only for the rank of species. Secondly, phenotypic and ecological properties of viruses may inform, but not override, evolutionary relatedness in the placement of ranks. Thirdly, alternative classifications that consider phenotypic attributes, such as being vector-borne (e.g., "arboviruses"), infecting a certain type of host (e.g., "mycoviruses," "bacteriophages") or displaying specific pathogenicity (e.g., "human immunodeficiency viruses"), may serve important clinical and regulatory purposes but often create polyphyletic categories that do not reflect evolutionary relationships. Nevertheless, such classifications ought to be maintained if they serve the needs of specific communities or play a practical clinical or regulatory role. However, they should not be considered or called taxonomies. Finally, while an evolution-based framework enables viruses discovered by metagenomics to be incorporated into the ICTV taxonomy, there are essential requirements for quality control of the sequence data used for these assignments. Combined, these four principles will enable future development and expansion of virus taxonomy as the true evolutionary diversity of viruses becomes a

In the version of this article initially published, there were mistakes in Fig. 1 (ICTV-ratified species growth): in the 2022 column for the 15-rank structure, the value for “Family” was 260 instead of 264; the value for “Genus” was 2,810 instead of 2,818; and the value for “Species” was 11,265 instead of 11,273. The errors have been corrected in the HTML and PDF versions of the article.

This article summarises the activities of the Bacterial Viruses Subcommittee of the International Committee on Taxonomy of Viruses for the period of March 2021-March 2022. We provide an overview of the new taxa proposed in 2021, approved by the Executive Committee, and ratified by vote in 2022. Significant changes to the taxonomy of bacterial viruses were introduced: the paraphyletic morphological families Podoviridae, Siphoviridae, and Myoviridae as well as the order Caudovirales were abolished, and a binomial system of nomenclature for species was established. In addition, one order, 22 families, 30 subfamilies, 321 genera, and 862 species were newly created, promoted, or moved.

Satellite remote sensing is a powerful tool 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 community types from a global plankton network that includes phytoplankton and heterotrophic protists and to predict their biogeography using global satellite observations. Six plankton community types were identified from a co-occurrence network inferred using a novel rDNA 18 S V4 planetary-scale eukaryotic metabarcoding dataset. Machine learning techniques were then applied to construct a model that predicted these community types from satellite data. The model showed an overall 67% accuracy in the prediction of the community types. The prediction using 17 satellite-derived parameters showed better performance than that using only temperature and/or the concentration of chlorophyll a. The constructed model predicted the global spatiotemporal distribution of community types over 19 years. The predicted distributions exhibited strong seasonal changes in community types in the subarctic–subtropical boundary regions, which were consistent with previous field observations. The model also identified the long-term trends in the distribution of community types, which suggested responses to ocean warming.

Microbial genome annotation is the process of identifying structural and functional elements in DNA sequences and subsequently attaching biological information to those elements. DRAM is a tool developed to annotate bacterial, archaeal, and viral genomes derived from pure cultures or metagenomes. DRAM goes beyond traditional annotation tools by distilling multiple gene annotations to genome level summaries of functional potential. Despite these benefits, a downside of DRAM is the requirement of large computational resources, which limits its accessibility. Further, it did not integrate with downstream metabolic modeling tools that require genome annotation. To alleviate these constraints, DRAM and the viral counterpart, DRAM-v, are now available and integrated with the freely accessible KBase cyberinfrastructure. With kb_DRAM users can generate DRAM annotations and functional summaries from microbial or viral genomes in a point-and-click interface, as well as generate genome-scale metabolic models from DRAM annotations.Availability and implementationFor kb_DRAM users, the kb_DRAM apps on KBase can be found in the catalog at https://narrative.kbase.us/#catalog/modules/kb_DRAM. For kb_DRAM users, a tutorial workflow with all documentation is available at https://narrative.kbase.us/narrative/129480. For kb_DRAM developers, software is available at https://github.com/shafferm/kb_DRAM.

This article summarises the activities of the Bacterial Viruses Subcommittee of the International Committee on Taxonomy of Viruses for the period of March 2021−March 2022. We provide an overview of the new taxa proposed in 2021, approved by the Executive Committee, and ratified by vote in 2022. Significant changes to the taxonomy of bacterial viruses were introduced: the paraphyletic morphological families Podoviridae, Siphoviridae, and Myoviridae as well as the order Caudovirales were abolished, and a binomial system of nomenclature for species was established. In addition, one order, 22 families, 30 subfamilies, 321 genera, and 862 species were newly created, promoted, or moved.

A universal taxonomy of viruses is essential for a comprehensive view of the virus world and for communicating the complicated evolutionary relationships among viruses. However, there are major differences in the conceptualisation and approaches to virus classification and nomenclature among virologists, clinicians, agronomists, and other interested parties. Here, we provide recommendations to guide the construction of a coherent and comprehensive virus taxonomy, based on expert scientific consensus. Firstly, assignments of viruses should be congruent with the best attainable reconstruction of their evolutionary histories, i.e., taxa should be monophyletic. This fundamental principle for classification of viruses is currently included in the International Committee on Taxonomy of Viruses (ICTV) code only for the rank of species. Secondly, phenotypic and ecological properties of viruses may inform, but not override, evolutionary relatedness in the placement of ranks. Thirdly, alternative classifications that consider phenotypic attributes, such as being vector-borne (e.g., "arboviruses"), infecting a certain type of host (e.g., "mycoviruses," "bacteriophages") or displaying specific pathogenicity (e.g., "human immunodeficiency viruses"), may serve important clinical and regulatory purposes but often create polyphyletic categories that do not reflect evolutionary relationships. Nevertheless, such classifications ought to be maintained if they serve the needs of specific communities or play a practical clinical or regulatory role. However, they should not be considered or called taxonomies. Finally, while an evolution-based framework enables viruses discovered by metagenomics to be incorporated into the ICTV taxonomy, there are essential requirements for quality control of the sequence data used for these assignments. Combined, these four principles will enable future development and expansion of virus taxonomy as the true evolutionary diversity of viruses becomes appa

The fate of oceanic carbon and nutrients depends on interactions between viruses, prokaryotes, and unicellular eukaryotes (protists) in a highly interconnected planktonic food web. To date, few controlled mechanistic studies of these interactions exist, and where they do, they are largely pairwise, focusing either on viral infection (i.e., virocells) or protist predation. Here we studied population-level responses of Synechococcus cyanobacterial virocells (i.e., cyanovirocells) to the protist Oxyrrhis marina using transcriptomics, endo- and exo-metabolomics, photosynthetic efficiency measurements, and microscopy. Protist presence had no measurable impact on Synechococcus transcripts or endometabolites. The cyanovirocells alone had a smaller intracellular transcriptional and metabolic response than cyanovirocells co-cultured with protists, displaying known patterns of virus-mediated metabolic reprogramming while releasing diverse exometabolites during infection. When protists were added, several exometabolites disappeared, suggesting microbial consumption. In addition, the intracellular cyanovirocell impact was largest, with 4.5- and 10-fold more host transcripts and endometabolites, respectively, responding to protists, especially those involved in resource and energy production. Physiologically, photosynthetic efficiency also increased, and together with the transcriptomics and metabolomics findings suggest that cyanovirocell metabolic demand is highest when protists are present. These data illustrate cyanovirocell responses to protist presence that are not yet considered when linking microbial physiology to global-scale biogeochemical processes.

The Tara Pacific expedition (2016–2018) sampled coral ecosystems around 32 islands in the Pacific Ocean and the ocean surface waters at 249 locations, resulting in the collection of nearly 58 000 samples. The expedition was designed to systematically study warm-water coral reefs and included the collection of corals, fish, plankton, and seawater samples for advanced biogeochemical, molecular, and imaging analysis. Here we provide a complete description of the sampling methodology, and we explain how to explore and access the different datasets generated by the expedition. Environmental context data were obtained from taxonomic registries, gazetteers, almanacs, climatologies, operational biogeochemical models, and satellite observations. The quality of the different environmental measures has been validated not only by various quality control steps, but also through a global analysis allowing the comparison with known environmental large-scale structures. Such publicly released datasets open the perspective to address a wide range of scientific questions.

Tropical coral reefs are among the most affected ecosystems by climate change and face increasing loss in the coming decades. Effective conservation strategies that maximize ecosystem resilience must be informed by the accurate characterization of extant genetic diversity and population structure together with an understanding of the adaptive potential of keystone species. Here we analyzed samples from the Tara Pacific Expedition (2016–2018) that completed an 18,000 km longitudinal transect of the Pacific Ocean sampling three widespread corals—Pocillopora meandrina, Porites lobata, and Millepora cf. platyphylla—across 33 sites from 11 islands. Using deep metagenomic sequencing of 269 colonies in conjunction with morphological analyses and climate variability data, we can show that despite a targeted sampling the transect encompasses multiple cryptic species. These species exhibit disparate biogeographic patterns and, most importantly, distinct evolutionary patterns in identical environmental regimes. Our findings demonstrate on a basin scale that evolutionary trajectories are species-specific and can only in part be predicted from the environment. This highlights that conservation strategies must integrate multi-species investigations to discern the distinct genomic footprints shaped by selection as well as the genetic potential for adaptive change.

Our knowledge of viral sequence space has exploded with advancing sequencing technologies and large-scale sampling and analytical efforts. Though archaea are important and abundant prokaryotes in many systems, our knowledge of archaeal viruses outside of extreme environments is limited. This largely stems from the lack of a robust, high-throughput, and systematic way to distinguish between bacterial and archaeal viruses in datasets of curated viruses. Here we upgrade our prior text-based tool (MArVD) via training and testing a random forest machine learning algorithm against a newly curated dataset of archaeal viruses. After optimization, MArVD2 presented a significant improvement over its predecessor in terms of scalability, usability, and flexibility, and will allow user-defined custom training datasets as archaeal virus discovery progresses. Benchmarking showed that a model trained with viral sequences from the hypersaline, marine, and hot spring environments correctly classified 85% of the archaeal viruses with a false detection rate below 2% using a random forest prediction threshold of 80% in a separate benchmarking dataset from the same habitats.

Predicting elemental cycles and maintaining water quality under increasing anthropogenic influence requires understanding the spatial drivers of river microbiomes. However, the unifying microbial processes governing river biogeochemistry are hindered by a lack of genome-resolved functional insights and sampling across multiple rivers. Here we employed a community science effort to accelerate the sampling, sequencing, and genome-resolved analyses of river microbiomes to create the Genome Resolved Open Watersheds database (GROWdb). This resource profiled the identity, distribution, function, and expression of thousands of microbial genomes across rivers covering 90% of United States watersheds. Specifically, GROWdb encompasses 1,469 microbial species from 27 phyla, including novel lineages from 10 families and 128 genera, and defines the core river microbiome for the first time at genome level. GROWdb analyses coupled to extensive geospatial information revealed local and regional drivers of microbial community structuring, while also presenting a myriad of foundational hypotheses about ecosystem function. Building upon the previously conceived River Continuum Concept 1 , we layer on microbial functional trait expression, which suggests the structure and function of river microbiomes is predictable. We make GROWdb available through various collaborative cyberinfrastructures 2, 3 so that it can be widely accessed across disciplines for watershed predictive modeling and microbiome-based management practices.

Tropical coral reefs are among the most affected ecosystems by climate change and face increasing loss in the coming decades. Effective conservation strategies that maximize ecosystem resilience must be informed by the accurate characterization of extant genetic diversity and population structure together with an understanding of the adaptive potential of keystone species. Here we analyzed samples from the Tara Pacific Expedition (2016–2018) that completed an 18,000 km longitudinal transect of the Pacific Ocean sampling three widespread corals—Pocillopora meandrina, Porites lobata, and Millepora cf. platyphylla—across 33 sites from 11 islands. Using deep metagenomic sequencing of 269 colonies in conjunction with morphological analyses and climate variability data, we can show that despite a targeted sampling the transect encompasses multiple cryptic species. These species exhibit disparate biogeographic patterns and, most importantly, distinct evolutionary patterns in identical environmental regimes. Our findings demonstrate on a basin scale that evolutionary trajectories are species-specific and can only in part be predicted from the environment. This highlights that conservation strategies must integrate multi-species investigations to discern the distinct genomic footprints shaped by selection as well as the genetic potential for adaptive change.

The Tara Pacific expedition (2016–2018) sampled coral ecosystems around 32 islands in the Pacific Ocean and the ocean surface waters at 249 locations, resulting in the collection of nearly 58 000 samples. The expedition was designed to systematically study warm-water coral reefs and included the collection of corals, fish, plankton, and seawater samples for advanced biogeochemical, molecular, and imaging analysis. Here we provide a complete description of the sampling methodology, and we explain how to explore and access the different datasets generated by the expedition. Environmental context data were obtained from taxonomic registries, gazetteers, almanacs, climatologies, operational biogeochemical models, and satellite observations. The quality of the different environmental measures has been validated not only by various quality control steps, but also through a global analysis allowing the comparison with known environmental large-scale structures. Such publicly released datasets open the perspective to address a wide range of scientific questions.

Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2 & PRIME;-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ(1)), 2 & PRIME;-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ(1)), 2 & PRIME;-deoxy-7-deazaguanine (dDG) and 2 & PRIME;-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ(1) formyltransferase (DpdN) and dPreQ(1) methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.

Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2′-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2′-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2′-deoxy-7-deazaguanine (dDG) and 2′-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases., Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2'-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2'-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2'-deoxy-7-deazaguanine (dDG) and 2'-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.

The Arctic Ocean (AO) is being rapidly transformed by global warming, but its biodiversity remains understudied for many planktonic organisms, in particular for unicellular eukaryotes that play pivotal roles in marine food webs and biogeochemical cycles. The aim of this study was to characterize the biogeographic ranges of species that comprise the contemporary pool of unicellular eukaryotes in the AO as a first step toward understanding mechanisms that structure these communities and identifying potential target species for monitoring. Leveraging the Tara Oceans DNA metabarcoding data, we mapped the global distributions of operational taxonomic units (OTUs) found on Arctic shelves into five biogeographic categories, identified biogeographic indicators, and inferred the degree to which AO communities of unicellular eukaryotes share members with assemblages from lower latitudes. Arctic/Polar indicator OTUs, as well as some globally ubiquitous OTUs, dominated the detection and abundance of DNA reads in the Arctic samples. OTUs detected only in Arctic samples (Arctic-exclusives) showed restricted distribution with relatively low abundances, accounting for 10–16% of the total Arctic OTU pool. OTUs with high abundances in tropical and/or temperate latitudes (non-Polar indicators) were also found in the AO but mainly at its periphery. We observed a large change in community taxonomic composition across the Atlantic-Arctic continuum, supporting the idea that advection and environmental filtering are important processes that shape plankton assemblages in the AO. Altogether, this study highlights the connectivity between the AO and other oceans, and provides a framework for monitoring and assessing future changes in this vulnerable ecosystem.

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, NO3− 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

It is well known that only a small fraction of the marine microbial diversity, which mainly belong to the so-called rare biosphere, can be retrieved by isolation. However, this paradigm has not been fully tested at a broad scale, especially in the deep ocean and in the ocean particle microbiome. Here, we compared 16S rRNA gene sequences from a large collection (>2000) of cultured heterotrophic marine bacteria with global 16S rRNA metabarcoding (16S Tags) datasets covering surface, mesopelagic and bathypelagic ocean samples that included 16 of the 22 samples used for isolation. These global datasets represent 60.322 unique 16S amplicon sequence variants (ASVs). Our results reveal a significantly higher proportion of isolates identical to ASVs in deeper ocean layers, which included the isolation of 3 of the top 10 most abundant 16S ASVs in the global bathypelagic ocean, related to the genera Sulfitobacter, Halomonas and Erythrobacter. These isolates contributed differently to the prokaryotic communities across different plankton size fractions, recruiting between 38% in the free-living fraction (0.2 -0.8 ¿m) and up to 45% in the largest particles (20-200 ¿m) in the bathypelagic ocean. Our findings support the hypothesis that sinking particles in the bathypelagic act as resource-rich habitats, suitable for the growth of heterotrophic bacteria with a copiotroph lifestyle that can be cultured, and that these cultivable bacteria can also thrive as free-living bacteria

Traditional culture techniques usually retrieve a small fraction of the marine microbial diversity, which mainly belong to the so-called rare biosphere. However, this paradigm has not been fully tested at a broad scale, especially in the deep ocean. Here, we examined the fraction of heterotrophic bacterial communities in photic and deep ocean layers that could be recovered by culture-dependent techniques at a large scale. We compared 16S rRNA gene sequences from a collection of 2003 cultured heterotrophic marine bacteria with global 16S rRNA metabarcoding datasets (16S TAGs) covering surface, mesopelagic and bathypelagic ocean samples that included 16 of the 23 samples used for isolation. These global datasets represent 60 322 unique 16S amplicon sequence variants (ASVs). Our results reveal a significantly higher proportion of isolates identical to ASVs in deeper ocean layers reaching up to 28% of the 16S TAGs of the bathypelagic microbial communities, which included the isolation of 3 of the top 10 most abundant 16S ASVs in the global bathypelagic ocean, related to the genera Sulfitobacter, Halomonas and Erythrobacter. These isolates contributed differently to the prokaryotic communities across different plankton size fractions, recruiting between 38% in the free-living fraction (0.2–0.8 µm) and up to 45% in the largest particles (20–200 µm) in the bathypelagic ocean. Our findings support the hypothesis that sinking particles in the bathypelagic act as resource-rich habitats, suitable for the growth of heterotrophic bacteria with a copiotroph lifestyle that can be cultured, and that these cultivable bacteria can also thrive as free-living bacteria

Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2′-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2′-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2′-deoxy-7-deazaguanine (dDG) and 2′-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases., Bacteriophages and bacteria are engaged in a constant arms race, continually evolving new molecular tools to survive one another. To protect their genomic DNA from restriction enzymes, the most common bacterial defence systems, double-stranded DNA phages have evolved complex modifications that affect all four bases. This study focuses on modifications at position 7 of guanines. Eight derivatives of 7-deazaguanines were identified, including four previously unknown ones: 2'-deoxy-7-(methylamino)methyl-7-deazaguanine (mdPreQ1), 2'-deoxy-7-(formylamino)methyl-7-deazaguanine (fdPreQ1), 2'-deoxy-7-deazaguanine (dDG) and 2'-deoxy-7-carboxy-7-deazaguanine (dCDG). These modifications are inserted in DNA by a guanine transglycosylase named DpdA. Three subfamilies of DpdA had been previously characterized: bDpdA, DpdA1, and DpdA2. Two additional subfamilies were identified in this work: DpdA3, which allows for complete replacement of the guanines, and DpdA4, which is specific to archaeal viruses. Transglycosylases have now been identified in all phages and viruses carrying 7-deazaguanine modifications, indicating that the insertion of these modifications is a post-replication event. Three enzymes were predicted to be involved in the biosynthesis of these newly identified DNA modifications: 7-carboxy-7-deazaguanine decarboxylase (DpdL), dPreQ1 formyltransferase (DpdN) and dPreQ1 methyltransferase (DpdM), which was experimentally validated and harbors a unique fold not previously observed for nucleic acid methylases.

One-quarter of photosynthesis-derived carbon on Earth rapidly cycles through a set of short-lived seawater metabolites that are generated from the activities of marine phytoplankton, bacteria, grazers and viruses. Here we discuss the sources of microbial metabolites in the surface ocean, their roles in ecology and biogeochemistry, and approaches that can be used to analyse them from chemistry, biology, modelling and data science. Although microbial-derived metabolites account for only a minor fraction of the total reservoir of marine dissolved organic carbon, their flux and fate underpins the central role of the ocean in sustaining life on Earth.

Marine planktonic eukaryotes play critical roles 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, to our knowledge, 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 completely explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years.

Peatlands are climate critical carbon (C) reservoirs that could become a C source under continued warming. A strong relationship between plant tissue chemistry and the soil organic matter (SOM) that fuels C gas emissions is inferred, but rarely examined at the molecular level. Here we compared Fourier transform infrared (FT-IR) spectroscopy measurements of solid phase functionalities in plants and SOM to ultra-high-resolution mass spectrometric analyses of plant and SOM water extracts across a palsa-bog-fen thaw and moisture gradient in an Arctic peatland. From these analyses we calculated the C oxidation state (NOSC), a measure which can be used to assess organic matter quality. Palsa plant extracts had the highest NOSC, indicating high quality, whereas extracts of Sphagnum, which dominated the bog, had the lowest NOSC. The percentage of plant compounds that are less bioavailable and accumulate in the peat, increases from palsa (25%) to fen (41%) to bog (47%), reflecting the pattern of percent Sphagnum cover. The pattern of NOSC in the plant extracts was consistent with the high number of consumed compounds in the palsa and low number of consumed compounds in the bog. However, in the FT-IR analysis of the solid phase bog peat, carbohydrate content was high implying high quality SOM. We explain this discrepancy as the result of low solubilization of bog SOM facilitated by the low pH in the bog which makes the solid phase carbohydrates less available to microbial decomposition. Plant-associated condensed aromatics, tannins, and lignin-like compounds declined in the unsaturated palsa peat indicating decomposition, but lignin-like compounds accumulated in the bog and fen peat where decomposition was presumably inhibited by the anaerobic conditions. A molecular-level comparison of the aboveground C sources and peat SOM demonstrates that climate-associated vegetation shifts in peatlands are important controls on the mechanisms underlying changing C g

Peatlands are climate critical carbon (C) reservoirs that could become a C source under continued warming. A strong relationship between plant tissue chemistry and the soil organic matter (SOM) that fuels C gas emissions is inferred, but rarely examined at the molecular level. Here we compared Fourier transform infrared (FT-IR) spectroscopy measurements of solid phase functionalities in plants and SOM to ultra-high-resolution mass spectrometric analyses of plant and SOM water extracts across a palsa-bog-fen thaw and moisture gradient in an Arctic peatland. From these analyses we calculated the C oxidation state (NOSC), a measure which can be used to assess organic matter quality. Palsa plant extracts had the highest NOSC, indicating high quality, whereas extracts of Sphagnum, which dominated the bog, had the lowest NOSC. The percentage of plant compounds that are less bioavailable and accumulate in the peat, increases from palsa (25%) to fen (41%) to bog (47%), reflecting the pattern of percent Sphagnum cover. The pattern of NOSC in the plant extracts was consistent with the high number of consumed compounds in the palsa and low number of consumed compounds in the bog. However, in the FT-IR analysis of the solid phase bog peat, carbohydrate content was high implying high quality SOM. We explain this discrepancy as the result of low solubilization of bog SOM facilitated by the low pH in the bog which makes the solid phase carbohydrates less available to microbial decomposition. Plant-associated condensed aromatics, tannins, and lignin-like compounds declined in the unsaturated palsa peat indicating decomposition, but lignin-like compounds accumulated in the bog and fen peat where decomposition was presumably inhibited by the anaerobic conditions. A molecular-level comparison of the aboveground C sources and peat SOM demonstrates that climate-associated vegetation shifts in peatlands are important controls on the mechanisms underlying changing C gas emissions.

Microbial communities in oxygen minimum zones (OMZs) are known to have significant impacts on global biogeochemical cycles, but viral influence on microbial processes in these regions are much less studied. Here we provide baseline ecological patterns using microscopy and viral metagenomics from the Eastern Tropical North Pacific (ETNP) OMZ region that enhance our understanding of viruses in these climate-critical systems. While extracellular viral abundance decreased below the oxycline, viral diversity and lytic infection frequency remained high within the OMZ, demonstrating that viral influences on microbial communities were still substantial without the detectable presence of oxygen. Viral community composition was strongly related to oxygen concentration, with viral populations in low-oxygen portions of the water column being distinct from their surface layer counterparts. However, this divergence was not accompanied by the expected differences in viral-encoded auxiliary metabolic genes (AMGs) relating to nitrogen and sulfur metabolisms that are known to be performed by microbial communities in these low-oxygen and anoxic regions. Instead, several abundant AMGs were identified in the oxycline and OMZ that may modulate host responses to low-oxygen stress. We hypothesize that this is due to selection for viral-encoded genes that influence host survivability rather than modulating host metabolic reactions within the ETNP OMZ. Together, this study shows that viruses are not only diverse throughout the water column in the ETNP, including the OMZ, but their infection of microorganisms has the potential to alter host physiological state within these biogeochemically important regions of the ocean.

Microbes drive myriad ecosystem processes, but under strong influence from viruses. Because studying viruses in complex systems requires different tools than those for microbes, they remain underexplored. To combat this, we previously aggregated double-stranded DNA (dsDNA) virus analysis capabilities and resources into ‘iVirus’ on the CyVerse collaborative cyberinfrastructure. Here we substantially expand iVirus’s functionality and accessibility, to iVirus 2.0, as follows. First, core iVirus apps were integrated into the Department of Energy’s Systems Biology KnowledgeBase (KBase) to provide an additional analytical platform. Second, at CyVerse, 20 software tools (apps) were upgraded or added as new tools and capabilities. Third, nearly 20-fold more sequence reads were aggregated to capture new data and environments. Finally, documentation, as “live” protocols, was updated to maximize user interaction with and contribution to infrastructure development. Together, iVirus 2.0 serves as a uniquely central and accessible analytical platform for studying how viruses, particularly dsDNA viruses, impact diverse microbial ecosystems.

The growth and physiology of soil microorganisms, which play vital roles in biogeochemical cycling, are shaped by both current and historical soil environmental conditions. Here, we developed and applied a genome-resolved metagenomic implementation of quantitative stable isotope probing (qSIP) with an H218O labeling experiment to identify actively growing soil microorganisms and their genomic capacities. qSIP enabled measurement of taxon-specific growth because isotopic incorporation into microbial DNA requires production of new genome copies. We studied three Mediterranean grassland soils across a rainfall gradient to evaluate the hypothesis that historic precipitation levels are an important factor controlling trait selection. We used qSIP-informed genome-resolved metagenomics to resolve the active subset of soil community members and identify their characteristic ecophysiological traits. Higher year-round precipitation levels correlated with higher activity and growth rates of flagellar motile microorganisms. In addition to heavily isotopically labeled bacteria, we identified abundant isotope-labeled phages, suggesting phage-induced cell lysis likely contributed to necromass production at all three sites. Further, there was a positive correlation between phage activity and the activity of putative phage hosts. Contrary to our expectations, the capacity to decompose the diverse complex carbohydrates common in soil organic matter or oxidize methanol and carbon monoxide were broadly distributed across active and inactive bacteria in all three soils, implying that these traits are not highly selected for by historical precipitation. IMPORTANCE Soil moisture is a critical factor that strongly shapes the lifestyle of soil organisms by changing access to nutrients, controlling oxygen diffusion, and regulating the potential for mobility. We identified active microorganisms in three grassland soils with similar mineral contexts, yet different historic rainfall inputs, by

Marine planktonic eukaryotes play critical roles 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, to our knowledge, 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 completely explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years.

Marine planktonic eukaryotes play critical roles 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, to our knowledge, 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 completely explain the functional repertoire convergence of major eukaryotic lineages that coexisted within oceanic currents for millions of years.

The International Virus Bioinformatics Meeting 2022 took place online, on 23-25 March 2022, and has attracted about 380 participants from all over the world. The goal of the meeting was to provide a meaningful and interactive scientific environment to promote discussion and collaboration and to inspire and suggest new research directions and questions. The participants created a highly interactive scientific environment even without physical face-to-face interactions. This meeting is a focal point to gain an insight into the state-of-the-art of the virus bioinformatics research landscape and to interact with researchers in the forefront as well as aspiring young scientists. The meeting featured eight invited and 18 contributed talks in eight sessions on three days, as well as 52 posters, which were presented during three virtual poster sessions. The main topics were: SARS-CoV-2, viral emergence and surveillance, virus-host interactions, viral sequence analysis, virus identification and annotation, phages, and viral diversity. This report summarizes the main research findings and highlights presented at the meeting.

Biogeographical studies have traditionally focused on readily visible organisms, but recent technological advances are enabling analyses of the large-scale distribution of microscopic organisms, whose biogeographical patterns have long been debated. Here we assessed the global structure of plankton geography and its relation to the biological, chemical, and physical context of the ocean (the ‘seascape’) by analyzing metagenomes of plankton communities sampled across oceans during the Tara Oceans expedition, in light of environmental data and ocean current transport. Using a consistent approach across organismal sizes that provides unprecedented resolution to measure changes in genomic composition between communities, we report a pan-ocean, size-dependent plankton biogeography overlying regional heterogeneity. We found robust evidence for a basin-scale impact of transport by ocean currents on plankton biogeography, and on a characteristic timescale of community dynamics going beyond simple seasonality or life history transitions of plankton.

Natural microbial communities are phylogenetically and metabolically diverse. In addition to underexplored organismal groups1, this diversity encompasses a rich discovery potential for ecologically and biotechnologically relevant enzymes and biochemical compounds2,3. However, studying this diversity to identify genomic pathways for the synthesis of such compounds4 and assigning them to their respective hosts remains challenging. The biosynthetic potential of microorganisms in the open ocean remains largely uncharted owing to limitations in the analysis of genome-resolved data at the global scale. Here we investigated the diversity and novelty of biosynthetic gene clusters in the ocean by integrating around 10,000 microbial genomes from cultivated and single cells with more than 25,000 newly reconstructed draft genomes from more than 1,000 seawater samples. These efforts revealed approximately 40,000 putative mostly new biosynthetic gene clusters, several of which were found in previously unsuspected phylogenetic groups. Among these groups, we identified a lineage rich in biosynthetic gene clusters (‘Candidatus Eudoremicrobiaceae’) that belongs to an uncultivated bacterial phylum and includes some of the most biosynthetically diverse microorganisms in this environment. From these, we characterized the phospeptin and pythonamide pathways, revealing cases of unusual bioactive compound structure and enzymology, respectively. Together, this research demonstrates how microbiomics-driven strategies can enable the investigation of previously undescribed enzymes and natural products in underexplored microbial groups and environments

Biogeographical studies have traditionally focused on readily visible organisms, but recent technological advances are enabling analyses of the large-scale distribution of microscopic organisms, whose biogeographical patterns have long been debated. Here we assessed the global structure of plankton geography and its relation to the biological, chemical and physical context of the ocean (the `seascape') by analyzing metagenomes of plankton communities sampled across oceans during the Tara Oceans expedition, in light of environmental data and ocean current transport. Using a consistent approach across organismal sizes that provides unprecedented resolution to measure changes in genomic composition between communities, we report a pan-ocean, size-dependent plankton biogeography overlying regional heterogeneity. We found robust evidence for a basin-scale impact of transport by ocean currents on plankton biogeography, and on a characteristic timescale of community dynamics going beyond simple seasonality or life history transitions of plankton.

Biogeographical studies have traditionally focused on readily visible organisms, but recent technological advances are enabling analyses of the large-scale distribution of microscopic organisms, whose biogeographical patterns have long been debated. Here we assessed the global structure of plankton geography and its relation to the biological, chemical and physical context of the ocean (the `seascape') by analyzing metagenomes of plankton communities sampled across oceans during the Tara Oceans expedition, in light of environmental data and ocean current transport. Using a consistent approach across organismal sizes that provides unprecedented resolution to measure changes in genomic composition between communities, we report a pan-ocean, size-dependent plankton biogeography overlying regional heterogeneity. We found robust evidence for a basin-scale impact of transport by ocean currents on plankton biogeography, and on a characteristic timescale of community dynamics going beyond simple seasonality or life history transitions of plankton.

Natural microbial communities are phylogenetically and metabolically diverse. In addition to underexplored organismal groups1, this diversity encompasses a rich discovery potential for ecologically and biotechnologically relevant enzymes and biochemical compounds2,3. However, studying this diversity to identify genomic pathways for the synthesis of such compounds4 and assigning them to their respective hosts remains challenging. The biosynthetic potential of microorganisms in the open ocean remains largely uncharted owing to limitations in the analysis of genome-resolved data at the global scale. Here we investigated the diversity and novelty of biosynthetic gene clusters in the ocean by integrating around 10,000 microbial genomes from cultivated and single cells with more than 25,000 newly reconstructed draft genomes from more than 1,000 seawater samples. These efforts revealed approximately 40,000 putative mostly new biosynthetic gene clusters, several of which were found in previously unsuspected phylogenetic groups. Among these groups, we identified a lineage rich in biosynthetic gene clusters (‘Candidatus Eudoremicrobiaceae’) that belongs to an uncultivated bacterial phylum and includes some of the most biosynthetically diverse microorganisms in this environment. From these, we characterized the phospeptin and pythonamide pathways, revealing cases of unusual bioactive compound structure and enzymology, respectively. Together, this research demonstrates how microbiomics-driven strategies can enable the investigation of previously undescribed enzymes and natural products in underexplored microbial groups and environments.

The biological carbon pump, in which carbon fixed by photosynthesis is exported to the deep ocean through sinking, is a major process in Earth's carbon cycle. The proportion of primary production that is exported is termed the carbon export efficiency (CEE). Based on in-lab or regional scale observations, viruses were previously suggested to affect the CEE (i.e., viral “shunt” and “shuttle”). In this study, we tested associations between viral community composition and CEE measured at a global scale. A regression model based on relative abundance of viral marker genes explained 67% of the variation in CEE. Viruses with high importance in the model were predicted to infect ecologically important hosts. These results are consistent with the view that the viral shunt and shuttle functions at a large scale and further imply that viruses likely act in this process in a way dependent on their hosts and ecosystem dynamics.

In this article, we – the Bacterial Viruses Subcommittee and the Archaeal Viruses Subcommittee of the International Committee on Taxonomy of Viruses (ICTV) – summarise the results of our activities for the period March 2020 – March 2021. We report the division of the former Bacterial and Archaeal Viruses Subcommittee in two separate Subcommittees, welcome new members, a new Subcommittee Chair and Vice Chair, and give an overview of the new taxa that were proposed in 2020, approved by the Executive Committee and ratified by vote in 2021. In particular, a new realm, three orders, 15 families, 31 subfamilies, 734 genera and 1845 species were newly created or redefined (moved/promoted).

Historically, virus taxonomy has been limited to describing viruses that were readily cultivated in the laboratory or emerging in natural biomes. Metagenomic analyses, single-particle sequencing, and database mining efforts have yielded new sequence data on an astounding number of previously unknown viruses. As metagenomes are relatively free of biases, these data provide an unprecedented insight into the vastness of the virosphere, but to properly value the extent of this diversity it is critical that the viruses are taxonomically classified. Inclusion of uncultivated viruses has already improved the process as well as the understanding of the taxa, viruses, and their evolutionary relationships. The continuous development and testing of computational tools will be required to maintain a dynamic virus taxonomy that can accommodate the new discoveries.

Ocean plankton comprise organisms from viruses to fish larvae that are fundamental to ecosystem functioning and the provision of marine services such as fisheries and CO2 sequestration. The latter services are partly governed by variations in plankton community composition and the expression of traits such as body size at community-level. While community assembly has been thoroughly studied for the smaller end of the plankton size spectrum, the larger end comprises ectotherms that are often studied at the species, or group-level, rather than as communities. The body size of marine ectotherms decreases with temperature, but controls on community-level traits remain elusive, hindering the predictability of marine services provision. Here, we leverage Tara Oceans datasets to determine how zooplankton community composition and size structure varies with latitude, temperature and productivity-related covariates in the global surface ocean. Zooplankton abundance and median size decreased towards warmer and less productive environments, as a result of changes in copepod composition. However, some clades displayed the opposite relationships, which may be ascribed to alternative feeding strategies. Given that climate models predict increasingly warmed and stratified oceans, our findings suggest that zooplankton communities will shift towards smaller organisms which might weaken their contribution to the biological carbon pump.