Deep-sea siliceous sponges harbor distinct and functionally diverse microbiomes

ABSTRACT Sponges, phylum Porifera, are long-lived and basal-branching metazoans that play important roles in ocean biogeochemistry and host diverse microbial communities. Siliceous sponges form a major clade of the Porifera; however, their microbiome is not well characterized, particularly in the deep ocean. Here, we used shotgun metagenomics to investigate the composition of the microbial communities of 13 siliceous sponges collected from four sites near Puerto Rico from depths ranging from 400 to 1,900 meters. Nine of the sponges in this study are from five sponge families that have not previously been sequenced using shotgun metagenomics. We assembled a total of 176 metagenome-assembled genomes from 20 bacterial phyla and 1 archaeal phylum. Ammonia-oxidizing archaea (AOA) Nitrosopumilaceae dominated most siliceous sponge microbial communities and was strikingly the sole symbiont associated with one sponge ( Farrea ). Overall, microbiome diversity was relatively low across siliceous sponges, except for a Phloeodictyidae, which is likely a high microbial abundance (HMA) sponge. Our results suggest that host sponge phylogeny may shape microbial community structure, with limited evidence for an environmental role. The sponge-associated microbial communities contained genetic capabilities for diverse metabolic functions, particularly contributing to the carbon, nitrogen, and sulfur cycles. In addition to the AOA, evidence of potential for microbial autotrophy was found through the presence of genes for RuBisCO, methanotrophy, and ATP citrate lyase. These results reveal both conserved relationships and metabolic flexibility across siliceous sponge lineages, suggesting unique evolutionary dynamics and demonstrating the importance of microbial metabolism to sponge host health and nutrient cycling in the oligotrophic deep ocean. IMPORTANCE Marine sponges, emerging ~600 million years ago, have close relationships with microorganisms, but the microbiome of deep-sea siliceous sponges is not well understood. Siliceous sponges play essential roles in deep-sea ecosystems by providing habitats for other metazoans and mediating carbon, nitrogen, and sulfur cycling; however, they remain some of the least-studied sponges. By shotgun sequencing DNA from 13 siliceous sponges collected near Puerto Rico, this study found that host sponge phylogeny is linked to microbial community composition and structure. Ammonia-oxidizing archaea dominated the microbial communities associated with marine sponges, likely playing key roles in utilizing metabolic byproducts and supporting host health. Other microbes also contributed to nutrient cycling and contained the potential to fix carbon, suggesting metabolic flexibility, which may benefit sponge hosts in low-resource environments. These findings emphasize the ecological importance of siliceous sponge-microbe symbioses and contribute to our understanding of the drivers shaping their structure and function.