Deltaproteobacteria, now proposed to be the phyla Desulfobacterota, Myxococcota, and SAR324, are ubiquitous in marine environments and play essential roles in global carbon, sulfur, and nutrient cycling. Despite their importance, our understanding of these bacteria is biased towards cultured organisms. Here we address this gap by compiling a genomic catalog of 1 792 genomes, including 402 newly reconstructed and characterized metagenome-assembled genomes (MAGs) from coastal and deep-sea sediments. Phylogenomic analyses reveal that many of these novel MAGs are uncultured representatives of Myxococcota and Desulfobacterota that are understudied. To better characterize Deltaproteobacteria diversity, metabolism, and ecology, we clustered ~1 500 genomes based on the presence/absence patterns of their protein families. Protein content analysis coupled with large-scale metabolic reconstructions separates eight genomic clusters of Deltaproteobacteria with unique metabolic profiles. While these eight clusters largely correspond to phylogeny, there are exceptions where more distantly related organisms appear to have similar ecological roles and closely related organisms have distinct protein content. Our analyses have identified previously unrecognized roles in the cycling of methylamines and denitrification among uncultured Deltaproteobacteria. This new view of Deltaproteobacteria diversity expands our understanding of these dominant bacteria and highlights metabolic abilities across diverse taxa.
Asgard archaea are globally distributed prokaryotic microorganisms related to eukaryotes; however, viruses that infect these organisms have not been described. Here, using metagenome sequences recovered from deep-sea hydrothermal sediments, we characterize six relatively large (up to 117 kb) double-stranded DNA (dsDNA) viral genomes that infected two Asgard archaeal phyla, Lokiarchaeota and Helarchaeota. These viruses encode Caudovirales-like structural proteins, as well as proteins distinct from those described in known archaeal viruses. Their genomes contain around 1-5% of genes associated with eukaryotic nucleocytoplasmic large DNA viruses (NCLDVs) and appear to be capable of semi-autonomous genome replication, repair, epigenetic modifications and transcriptional regulation. Moreover, Helarchaeota viruses may hijack host ubiquitin systems similar to eukaryotic viruses. Genomic analysis of these Asgard viruses reveals that they contain features of both prokaryotic and eukaryotic viruses, and provides insights into their potential infection and host interaction mechanisms.Asgard archaea are globally distributed prokaryotic microbes proposed to be closely related to eukaryotes 1,2 . Their genomic composition indicates that they are descendants of the archaeal cell that gave rise to the first eukaryotic common ancestor 3 . Asgard biodiversity has expanded greatly in recent years due to the recovery of metagenome-assembled genomes (MAGs) from a range of marine and terrestrial aquatic sediments 4 . The recovery of these Asgard MAGs has resulted in predictions about their metabolic abilities and evolutionary histories. Recently, an anaerobic slow-growing Asgard, Lokiarchaeota, has been cultured and appears to have syntrophic dependencies with bacteria, a finding that supports previous omics-based predictions 5 . Interactions between bacteria and Asgards are thought to have led to the formation of the first mitochondria-containing eukaryotic cell 5,6 and it is also hypothesized that interactions with viruses contributed to the origin of complex cellular life 7 . This observation is based on the nucleus-like cytoplasmic viral factories of some nucleocytoplasmic large DNA viruses (NCLDVs) 8 and jumbo bacteriophages 9,10 that allow for replication within the host cytoplasm and the decoupling of transcription and translation 7 . Additionally, representatives from the Mimiviridae family possess mRNA capping pathways homologous to those present in eukaryotes 11 . Putative viral proteins have been identified within Lokiarchaeota genomes 12 , suggesting a role of viruses in the exchange of genetic information and the evolution of Asgards. Type I and Type III CRISPR-Cas immune systems have been described in several Asgard phyla (Odinarchaeota, Thorarchaeota, Lokiarchaeota and Helarchaeota) 13 , yet genomes of Asgard-linked viruses have not been extensively detailed.
Microbes in marine sediments play crucial roles in global carbon and nutrient cycling. However, our understanding of microbial diversity and physiology on the ocean floor is limited. Here, we use phylogenomic analyses of thousands of metagenome-assembled genomes (MAGs) from coastal and deep-sea sediments to identify 55 MAGs that are phylogenetically distinct from previously described bacterial phyla. We propose that these MAGs belong to 4 novel bacterial phyla (Blakebacterota, Orphanbacterota, Arandabacterota, and Joyebacterota) and a previously proposed phylum (AABM5-125-24), all of them within the FCB superphylum. Comparison of their rRNA genes with public databases reveals that these phyla are globally distributed in different habitats, including marine, freshwater, and terrestrial environments. Genomic analyses suggest these organisms are capable of mediating key steps in sedimentary biogeochemistry, including anaerobic degradation of polysaccharides and proteins, and respiration of sulfur and nitrogen. Interestingly, these genomes code for an unusually high proportion (~9% on average, up to 20% per genome) of protein families lacking representatives in public databases. Genes encoding hundreds of these protein families colocalize with genes predicted to be involved in sulfur reduction, nitrogen cycling, energy conservation, and degradation of organic compounds. Our findings advance our understanding of bacterial diversity, the ecological roles of these bacteria, and potential links between novel gene families and metabolic processes in the oceans.
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