Comparative metagenomics evidence distinct trends of genome evolution in sponge-dwelling bacteria and their pelagic counterparts

Prokaryotic associations with sponges are among the oldest host-microbiome relationships on Earth. In this study, we investigated how bacteria from several phyla have independently adapted to the sponge interior by comparing metagenome-assembled genomes of sponge-dwelling and pelagic bacteria sourced from broad phylogenetic and geographic samplings. We discovered that sponge-dwelling bacteria have more energetically expensive genomes and share patterns of depletion and enrichment for functional categories of genes that evidence evolution towards lower pathogenicity. We also identified a new defining genomic characteristic of sponge-dwelling bacteria that is virtually absent from pelagic bacteria, the presence of cassettes that contain eukaryotic steroid biosynthesis genes. Collectively, these results illuminate the trends in genome evolution that are associated with a sponge-dwelling life history strategy and have implications for furthering our understanding of how sponge-microbial symbioses have persisted through deep evolutionary time. ImportanceMuch attention has recently been devoted to investigating the evolution of microbes that live in symbiosis with sponge hosts using microbial metagenomic data. However, several biological questions regarding this symbiosis remain unanswered. Two questions that we address here are: 1) what are the long-term consequences of the symbiosis on the evolution of microbial symbiont genome size, protein content, and nucleotide content, and 2) how is the evolution of virulence in sponge-dwelling microbial symbionts, which generally undergo a mixed transmission modes (e.g. horizontal and vertical), related to long-term stability of the symbiosis? By employing the largest comparative metagenomic analysis to date in terms of host sponge species and geographic representation, we address these questions and provide further resolution into the evolutionary processes that are involved in mediating the crosstalk between sponge hosts and their microbial symbionts.