Phylogenomics aims to describe evolutionary relatedness between organisms by analyzing genomic data. The common practice is to produce phylogenomic trees from molecular information in the sequence, order, and content of genes in genomes. These phylogenies describe the evolution of life and become valuable tools for taxonomy. The recent availability of structural and functional data for hundreds of genomes now offers the opportunity to study evolution using more deep, conserved, and reliable sets of molecular features. Here, we reconstruct trees of life from the functions of proteins. We start by inferring rooted phylogenomic trees and networks of organisms directly from Gene Ontology annotations. Phylogenies and networks yield novel insights into the emergence and evolution of cellular life. The ancestor of Archaea originated earlier than the ancestors of Bacteria and Eukarya and was thermophilic. In contrast, basal bacterial lineages were non-thermophilic. A close relationship between Plants and Metazoa was also identified that disagrees with the traditional Fungi-Metazoa grouping. While measures of evolutionary reticulation were minimum in Eukarya and maximum in Bacteria, the massive role of horizontal gene transfer in microbes did not materialize in phylogenomic networks. Phylogenies and networks also showed that the best reconstructions were recovered when problematic taxa (i.e., parasitic/symbiotic organisms) and horizontally transferred characters were excluded from analysis. Our results indicate that functionomic data represent a useful addition to the set of molecular characters used for tree reconstruction and that trees of cellular life carry in deep branches considerable predictive power to explain the evolution of living organisms.

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Candidate phylum Atribacteria JS1 lineage is one of the predominant bacterial groups in anoxic subseafloor sediments, especially in organic-rich or gas hydrate-containing sediments. However, due to the lack of axenic culture representatives, metabolic potential and biogeochemical roles of this phylum have remained elusive. Here, we examined the microbial communities of marine sediments of the Ross Sea, Antarctica, and found candidate phylum Atribacteria JS1 lineage was the most abundant candidate phylum accounting for 9.8–40.8% of the bacterial communities with a single dominant operational taxonomic unit (OTU). To elucidate the metabolic potential and ecological function of this species, we applied a single-cell genomic approach and obtained 18 single-cell amplified genomes presumably from a single species that was consistent with the dominant OTU throughout the sediments. The composite genome constructed by co-assembly showed the highest genome completeness among available Atribacteria JS1 genomes. Metabolic reconstruction suggested fermentative potential using various substrates and syntrophic acetate oxidation coupled with hydrogen or formate scavenging methanogens. This metabolic potential supports the predominance of Atribacteria JS1 in anoxic environments expanding our knowledge of the ecological function of this uncultivated group.