Novel Insights Into Bacterial Dimethylsulfoniopropionate Catabolism in the East China Sea

Abstract

The compatible solute dimethylsulfoniopropionate (DMSP), made by many marine organisms, is one of Earth's most abundant organosulfur molecules. Many marine bacteria import DMSP and can degrade it as a source of carbon and/or sulfur via DMSP cleavage or DMSP demethylation pathways, which can generate the climate active gases dimethyl sulfide (DMS) or methanthiol (MeSH), respectively. Here we used culture-dependent and -independent methods to study bacteria catabolizing DMSP in the East China Sea (ECS). Of bacterial isolates, 42.11% showed DMSP-dependent DMS (Ddd⁺) activity, and 12.28% produced detectable levels of MeSH. Interestingly, although most Ddd⁺ isolates were <i>Alphaproteobacteria</i> (mainly Roseobacters), many gram-positive <i>Actinobacteria</i> were also shown to cleave DMSP producing DMS. The mechanism by which these <i>Actinobacteria</i> cleave DMSP is unknown, since no known functional <i>ddd</i> genes have been identified in genome sequences of Ddd⁺ <i>Microbacterium</i> and <i>Agrococcus</i> isolates or in any other sequenced <i>Actinobacteria</i> genomes. Gene probes to the DMSP demethylation gene <i>dmdA</i> and the DMSP lyase gene <i>dddP</i> demonstrated that these DMSP-degrading genes are abundant and widely distributed in ECS seawaters. <i>dmdA</i> was present in relatively high proportions in both surface (19.53% ± 6.70%) and bottom seawater bacteria (16.00% ± 8.73%). In contrast, <i>dddP</i> abundance positively correlated with chlorophyll <i>a</i>, and gradually decreased with the distance from land, which implies that the bacterial DMSP lyase gene <i>dddP</i> might be from bacterial groups that closely associate with phytoplankton. Bacterial community analysis showed positive correlations between <i>Rhodobacteraceae</i> abundance and concentrations of DMS and DMSP, further confirming the link between this abundant bacterial class and the environmental DMSP cycling.