The missing part of the DMSP cycle in coral holobionts: Endozoicomonas exports acetate derived from DMSP degradation

Abstract

Endozoicomonas, a dominant symbiotic bacterium in coral holobionts, is noted for its ability to degrade dimethylsulfoniopropionate (DMSP) so as to generate acetate. While acetate is a well-known short-chain fatty acid in metabolic cross-feeding relationships, it remains unclear whether acetate derived from bacterial DMSP degradation is available to corals and their other symbionts. In this study, we employed Endozoicomonas ruthgatesiae strain 8E (herein referred as 8E) as a model to examine availability of DMSP-derived acetate for other symbionts. Using gas chromatography-mass spectrometry (GC-MS), we observed a significant increase in acetate excretion in 8E upon exposure to DMSP. Stable isotope labeling further confirmed that this elevated acetate efflux originated directly from DMSP, suggesting a complete cycle of DMSP-derived carbon among coral symbionts. Transcriptomic analysis revealed that DMSP exposure upregulated dddD expression and triggered a systemic reconfiguration of metabolism, characterized by down-regulation of the TCA cycle and the Pta-AckA pathway, with carbon flux redirected to the glyoxylate shunt. These findings suggest that upon exposure to DMSP, metabolism of 8E shifts from biomass production to DMSP catabolism, resulting in acetate efflux. Notably, we found that elevated temperature diminishes DMSP cleavage activity of 8E, indicating thermal sensitivity of this bacterial metabolic activity. ImportanceEndozoicomonas is known for its dominance in coral holobionts and its ability to degrade DMSP, an important compound in the marine sulfur cycle. Acetate is one resulting product in microbial DMSP metabolism and a common cross-feeding molecule. Whether DMSP-derived acetate in coral-associated DMSP-degrading bacteria is employed for cross-feeding stands a critical step in making a complete carbon cycle of DMSP metabolism within coral holobionts. In this study, we employed GC-MS and RNA-sequencing techniques to offer the first evidence of acetate excretion in Endozoicomonas while metabolizing DMSP, as well as its underlying genetic mechanism. Furthermore, we demonstrate reduced genetic response and DMSP-degrading capability under an elevated temperature in Endozoicomonas ruthgatesiae strain 8E, the model bacterium employed in this study. These findings provide the missing puzzle of DMSP metabolism in coral holobionts and suggest a potential role of DMSP in modulating symbiotic interactions within coral holobionts.