Integrated transcriptomic and metabolite analyses link DMSP cleavage to acetate overflow in the coral symbiont Endozoicomonas ruthgatesiae

Abstract

Endozoicomonas, a dominant bacterial symbiont of corals, degrades dimethylsulfoniopropionate (DMSP) and produces dimethylsulfide (DMS), a key compound in the global sulfur cycle. By contrast, the carbon backbone of DMSP has received far less attention. Using Endozoicomonas ruthgatesiae strain 8E as a model, we exposed cultures to DMSP at 25 and 31, simulating an ambient condition and thermal stress, respectively. Using gas chromatography-mass spectrometry (GC-MS) to monitor DMS and acetate production, we observed a significant increase in acetate efflux from 8E during DMSP metabolism in a growth phase-dependent manner. This increase in acetate was not observed when the native compound was replaced with 13C-labeled DMSP, suggesting that the additional acetate originated from DMSP. Transcriptomic analysis revealed that DMSP exposure upregulated dddD expression and triggered a reconfiguration of 8E's central carbon metabolism, with upregulation of genes associated with the glyoxylate shunt-associated genes, and down-regulation of the TCA cycle and the Pta-AckA pathway. These findings suggest that DMSP-derived acetate overflows when its assimilation into biomass is restricted. Notably, elevated temperature diminished DMSP cleavage activity of 8E, indicating thermal sensitivity of this bacterial metabolic activity. Together, our results indicate that exposure to DMSP redirects carbon flow in Endozoicomonas, resulting in overflow of DMSP-derived acetate.