Dimethylsulfoniopropionate catabolism of marine sponge Diacarnus erythraeanus microorganisms

Sponge microbes have been hypothesized to play a crucial role in the sponge sulfur cycle. However, to date no study confirms the role of sponge microorganisms in dimethylsulfoniopropionate (DMSP) catabolism. In this study, metagenomics, metatranscriptomics and RT-qPCR analyses indicate the microbial DMSP catabolism potentials along with assimilatory sulfate reduction, dissimilarity sulfate reduction and sulfur oxidation in Red Sea shallow-water and mesophotic sponge Diacarnus erythraenus. The overall sulfur metabolic functional genes show no significant difference in their relative abundance between shallow-water and mesophotic sponge D. erythraenus. Meanwhile, DMSP catabolism mediated microbial sulfur cycle of sponge Diacarnus erythraenus is suggested. In particular, a novel bacterial species Microbulbifer spongiae MI-GT isolated from sponge D. erythraeanus is found to be able to use DMSP as the sole carbon source. This study provides the genomic, functional and biochemical evidence for the ability of sponge D. erythraenus-associated M. spongiae MI-GT to degrades DMSP into dimethylsulfide (DMS) through cleavage pathway by heterologous expression of dddD gene and recombinant DddD protein activity analysis. In summary, it is the first time to reveal the DMSP catabolism of sponge microorganisms at the microbiome, metatranscriptome and strain levels, providing novel insights into the sponge microorganisms’ role in marine sulfur cycling.