Sponges are benthic filter feeders that play pivotal roles in coupling benthic-pelagic processes in the oceans that involve transformation of dissolved and particulate organic carbon and nitrogen into biomass. While the contribution of sponge holobionts to the nitrogen cycle has been recognized in past years, their importance in the sulfur cycle, both oceanic and physiological, has only recently gained attention. Sponges in general, and Theonella swinhoei in particular, harbour a multitude of associated microorganisms that could affect sulfur cycling within the holobiont. We reconstructed the genome of a Chromatiales (class Gammaproteobacteria) bacterium from a metagenomic sequence dataset of a T. swinhoei-associated microbial community. This relatively abundant bacterium has the metabolic capability to oxidize sulfide yet displays reduced metabolic potential suggestive of its lifestyle as an obligatory symbiont. This bacterium was detected in multiple sponge orders, according to similarities in key genes such as 16S rRNA and polyketide synthase genes. Due to its sulfide oxidation metabolism and occurrence in many members of the Porifera phylum, we suggest naming the newly described taxon Candidatus Porisulfidus.