SAR92 clade bacteria are potentially important DMSP degraders and sources of climate-active gases in marine environments

Abstract

ABSTRACT Dimethylsulfoniopropionate (DMSP) is one of Earth’s most abundant organosulfur molecules, which can be catabolized by marine bacteria to release climate-active gases through the cleavage and/or demethylation pathways. The marine SAR92 clade is an abundant oligotrophic group of Gammaproteobacteria in coastal seawater, but their ability to catabolize DMSP is untested. Three SAR92 clade strains isolated from coastal seawater in this study and the SAR92 representative strain HTCC2207 were all shown to catabolize DMSP as a carbon source. All the SAR92 clade strains exhibited DMSP lyase activity producing dimethylsulfide (DMS) and their genomes encoded a ratified DddD DMSP lyase. In contrast, only HTCC2207 and two isolated strains contained the DMSP demethylase dmdA gene and potentially simultaneously demethylated and cleaved DMSP to produce methanethiol (MeSH) and DMS. In SAR92 clade strains with dddD and dmdA , transcription of these genes was inducible by DMSP substrate. Bioinformatic analysis indicated that SAR92 clade bacteria containing and transcribing DddD and DmdA were widely distributed in global oceans, especially in polar regions. This study highlights the SAR92 clade of oligotrophic bacteria as potentially important catabolizers of DMSP and sources of the climate-active gases MeSH and DMS in marine environments, particularly in polar regions. IMPORTANCE Catabolism of dimethylsulfoniopropionate (DMSP) by marine bacteria has important impacts on the global sulfur cycle and climate. However, whether and how members of most oligotrophic bacterial groups participate in DMSP metabolism in marine environments remains largely unknown. In this study, by characterizing culturable strains, we have revealed that bacteria of the SAR92 clade, an abundant oligotrophic group of Gammaproteobacteria in coastal seawater, can catabolize DMSP through the DMSP lyase DddD-mediated cleavage pathway and/or the DMSP demethylase DmdA-mediated demethylation pathway to produce climate-active gases dimethylsulfide and methanethiol. Additionally, we found that SAR92 clade bacteria capable of catabolizing DMSP are widely distributed in global oceans. These results indicate that SAR92 clade bacteria are potentially important DMSP degraders and sources of climate-active gases in marine environments that have been overlooked, contributing to a better understanding of the roles and mechanisms of the oligotrophic bacteria in oceanic DMSP degradation.