Metagenomic binning reveals community and functional characteristics of sulfur- and methane-oxidizing bacteria in cold seep sponge ground

BACKGROUND: Cold seep sponges typically reside in the carbonate rock areas surrounding the vents, often comprising only a few individuals of a limited number of species. Previous limited studies have indicated that sponges living in seeps or vents host chemolithotrophic microorganisms, including sulfur-oxidizing bacteria (SOB) and methane-oxidizing bacteria (MOB), regardless of their feeding habits. This suggests that they may utilize compounds from their environment. However, when multiple sponge species are found co-occurring in a single sponge ground sharing identical environmental and material conditions, it remains unclear how their symbiotic community structure will behave. Specifically, it is uncertain whether the community will exhibit greater similarity or, as seen in most studies, demonstrate host specificity. RESULTS: We utilize metagenomics and binning analysis to characterize six new sponge species belonging to two classes and two distinct dietary habits, all discovered in the same cold seep. Our findings reveal that their associated microbial communities, primarily composed of SOB and MOB from the phylum Proteobacteria, exhibit a high abundance of groups with the same chemosynthetic functions. Binning recovered diverse, novel MAGs (metagenome-assembled genomes) primarily dominated by order PS1 (SOB) and order Methylococcales (MOB). This similarity extends beyond the dietary habits and higher taxonomic levels of the sponge hosts. Phylogenetic and abundance difference analyses of MAGs indicate significant host specificity in the selection of symbiotic microbial species among different sponge species. Notably, these MOB and SOB exhibit potential novelty within their clade compared to known taxa. Furthermore, the genomes of these SOB and MOB contain abundant functions related to their adaptation to the chemoautotrophic environment and symbiotic lifestyle within the cold seep. CONCLUSIONS: The chemosynthetic environment shapes the high relative abundance of key functional groups that dominate the symbiotic community, while the species differences among host sponges determine the strain selection within these groups. The metabolic functions expressed by this "convergence with divergence" community structure collectively endow the holobionts with the ability to adapt to the cold seep environment.