ABSTRACT
The microbial communities of marine seep sediments contain unexplored physiological and phylogenetic diversity. Here, we examined 30 bacterial metagenome-assembled genomes (MAGs) from cold seeps in the South China Sea, the Indian Ocean, the Scotian Basin, and the Gulf of Mexico, as well as from deep-sea hydrothermal sediments in the Guaymas Basin, Gulf of California. Phylogenetic analyses of these MAGs indicate that they form a distinct phylum-level bacterial lineage, which we propose as a new phylum,
Candidatus
Effluviviacota, in reference to its preferential occurrence at diverse seep areas. Based on tightly clustered high-quality MAGs, we propose two new genus-level candidatus taxa,
Candidatus
Effluvivivax and
Candidatus
Effluvibates. Genomic content analyses indicate that
Candidatus
Effluviviacota are chemoheterotrophs that harbor the Embden–Meyerhof–Parnas glycolysis pathway. They gain energy by fermenting organic substrates. Additionally, they display potential capabilities for the degradation of cellulose, hemicellulose, starch, xylan, and various peptides. Extracellular anaerobic respiration appears to rely on metals as electron acceptors, with electron transfer primarily mediated by multiheme cytochromes and by a flavin-based extracellular electron transfer (EET) mechanism that involves NADH-quinone oxidoreductase-demethylmenaquinone-synthesizing enzymes, uncharacterized membrane proteins, and flavin-binding proteins, also known as the NUO-DMK-EET-FMN complex. The heterogeneity within the
Ca
. Effluviviacota phylum suggests varying roles in energy metabolism among different genera. While NUO-DMK-EET-FMN electron transfer has been reported predominantly in Gram-positive bacteria, it is now identified in
Ca
. Effluviviacota as well. We detected the presence of genes associated with bacterial microcompartments in
Ca
. Effluviviacota, which can promote specific metabolic processes and protect the cytosol from toxic intermediates.
IMPORTANCE
The newly discovered bacterial phylum
Candidatus
Effluviviacota is widespread across diverse seepage ecosystems, marine environments, and freshwater environments, with a notable preference for cold seeps. While maintaining an average abundance of approximately 1% in the global gene catalog of cold seep habitats, it has not hitherto been characterized. The metabolic versatility of
Ca
. Effluviviacota in anaerobic carbon, hydrogen, and metal cycling aligns with its prevalence in anoxic niches, with a preference for cold seep environments. Variations in metabolic potential between
Ca
. Effluvivivax and
Ca
. Effluvibates may contribute to shaping their respective habitat distributions.