Novel enzyme for dimethyl sulfide-releasing in bacteria reveals a missing route in the marine sulfur cycle

Abstract

Dimethylsulfoniopropionate (DMSP) is an abundant and ubiquitous organosulfur molecule and plays important roles in the global sulfur cycle. Cleavage of DMSP produces volatile dimethyl sulfide (DMS), which has impacts on the global climate. Multiple pathways for DMSP catabolism have been identified. Here we identified yet another novel pathway, the ATP DMSP lysis pathway. The key enzyme, AcoD, is an ATP-dependent DMSP lyase. AcoD belongs to the acyl-CoA synthetase superfamily, which is totally different from other DMSP lyases, showing a new evolution route. AcoD catalyses the conversion of DMSP to DMS by a two-step reaction: the ligation of DMSP with CoA to form the intermediate DMSP-CoA, which is then cleaved to DMS and acryloyl-CoA. The novel catalytic mechanism was elucidated by structural and biochemical analyses. AcoD is widely distributed in many bacterial lineages including Alphaproteobacteria, Betaproteobacteria, Gammaproteobacteria and Firmicutes, revealing this new pathway plays important roles in global DMSP/DMS cycles.

DMS emissions from the Arctic marginal ice zone

“…In the OW, the highest dddP:dmdA ratios occurred in the 9-41 m layer with a median of 3-4 (data from leg 1a), in good accordance with enhanced DMS below the surface (Figure 4d). The dddP:dmdA ratios reported here provide a lower bound for the ratio between bacterial cleavage and demethylation genes, because as many as eight genes encoding for bacterial DMSP lyases have been described to date (Curson et al, 2011;Li et al, 2020), of which three (dddK, dddP, and dddD) appear to be abundant in the global surface ocean (Landa et al, 2019).…”

The Stereochemical Course of DmdC, an Enzyme Involved in the Degradation of Dimethylsulfoniopropionate

“…In contrast, the DMSP lyase DddD catalyses the hydrolysis of DMSP to DMS and 3-hydroxypropionate (2), [30] while the recently described lyase DddX is a bifunctional enzyme that first converts DMSP into the corresponding coenzyme A thioester before cleavage into DMS and acyloyl-CoA (3). [31] Another fraction of DMSP is oxidised to dimethylsulfoxonium propionate (DMSOP), [32] but no enzyme is known for this important transformation. The cleavage of DMSOP leads to the non-volatile and water soluble metabolite dimethylsulfoxide (DMSO), a reaction that can be catalysed by DMSP lyases in vitro and in vivo.…”

On the Substrate Scope of Dimethylsulfonium Propionate Lyases toward Dimethylsulfoxonium Propionate Derivatives

“…In contrast, the recently characterized bifunctional enzyme DddX cleaves DMSP after its conversion into the coenzyme A thioester, leading to the formation of DMS and acryloyl-CoA (3). [35] Two pathways can redirect the metabolism of DMSP and limit the sulfur flux from the ocean to the atmosphere through the formation of water soluble products. Along the DMSP demetylation pathway (Scheme 1B) DMSP is first demethylated by DmdA to 3-(methylsulfanyl)propionate (4) which is subsequently converted into the coenzyme A thioester 5 by DmdB.…”