The reconstruction of bacterial and archaeal genomes from shotgun metagenomes has enabled insights into the ecology and evolution of environmental and host-associated microbiomes. Here we applied this approach to >10,000 metagenomes collected from diverse habitats covering all of Earth’s continents and oceans, including metagenomes from human and animal hosts, engineered environments, and natural and agricultural soils, to capture extant microbial, metabolic and functional potential. This comprehensive catalog includes 52,515 metagenome-assembled genomes representing 12,556 novel candidate species-level operational taxonomic units spanning 135 phyla. The catalog expands the known phylogenetic diversity of bacteria and archaea by 44% and is broadly available for streamlined comparative analyses, interactive exploration, metabolic modeling and bulk download. We demonstrate the utility of this collection for understanding secondary-metabolite biosynthetic potential and for resolving thousands of new host linkages to uncultivated viruses. This resource underscores the value of genome-centric approaches for revealing genomic properties of uncultivated microorganisms that affect ecosystem processes.

SummaryRecognition is an important stage in the establishment of highly specific mutualistic associations. Yet, for the majority of symbioses, very few of the mechanisms involved in recognition and specificity are known. In this study, we provide evidence for a recognition mechanism at the onset of symbiosis between larvae of the coral Fungia scutaria and their endosymbiotic dinoflagellate algae. This recognition step occurs during initial cellular contact between the symbiotic partners through a lectin/glycan interaction. We determined that an intact algal cell surface was required for successful infection of F. scutaria larvae. Modification of the algal cell surface by enzymatic digestion with trypsin or N-glycosidase significantly reduced infection success, and implicated algal cell surface glycans in recognition. Using flow cytometry, a-mannose/aglucose and a-galactose residues were identified as potential recognition ligands on the algal cell surface. Finally, inhibition of these cell surface glycans significantly reduced infection of F. scutaria larvae by the algae. These data provide evidence that the algal cell surface contains glycan ligands, such as a-mannose/ a-glucose and a-galactose, which play a role in recognition during initial contact at the onset of symbiosis with F. scutaria larvae.

SignificanceMarine microbial communities exert a large influence on ocean ecosystem processes, and viruses in these communities play key roles in controlling microbial abundances, nutrient cycling, and productivity. We show here that dominant viruses in the open ocean persist for long time periods and that many appear tightly locked in coordinated diel oscillations with their bacterial hosts. The persistent structure of viral assemblages, as well as synchronized daily oscillations of viruses and hosts, are in part the result of the regular diurnal coupling of viral and host replication cycles. Collectively, our results suggest that viruses, as key components of marine ecosystems, are intrinsically synchronized with the daily rhythms of microbial community processes in the ocean’s photic zone.

Viruses are abundant in the ocean and a major driving force in plankton ecology and evolution. It has been assumed that most of the viruses in seawater contain DNA and infect bacteria, but RNA-containing viruses in the ocean, which almost exclusively infect eukaryotes, have never been quantified. We compared the total mass of RNA and DNA in the viral fraction harvested from seawater and using data on the mass of nucleic acid per RNA- or DNA-containing virion, estimated the abundances of each. Our data suggest that the abundance of RNA viruses rivaled or exceeded that of DNA viruses in samples of coastal seawater. The dominant RNA viruses in the samples were marine picorna-like viruses, which have small genomes and are at or below the detection limit of common fluorescence-based counting methods. If our results are typical, this means that counts of viruses and the rate measurements that depend on them, such as viral production, are significantly underestimated by current practices. As these RNA viruses infect eukaryotes, our data imply that protists contribute more to marine viral dynamics than one might expect based on their relatively low abundance. This conclusion is a departure from the prevailing view of viruses in the ocean, but is consistent with earlier theoretical predictions.