Study of sulfoglycolysis in Enterococcus gilvus reveals a widespread bifurcated pathway for dihydroxypropanesulfonate degradation

Sulfoquinovose (SQ), the polar head group of sulfolipids essential for photosynthesis, is naturally abundant. Anaerobic Firmicutes degrade SQ through a transaldolase-dependent (sulfo-TAL) pathway, producing dihydroxypropanesulfonate (DHPS). Some bacteria extend this pathway by the sequential action of HpfG and HpfD converting DHPS to 3-hydroxypropanesulfonate (3-HPS) via 3-sulfopropionaldehyde (3-SPA). Here, we report a variant sulfo-TAL pathway in <i>Enterococcus gilvus</i>, involving additional enzymes, a NAD⁺-dependent 3-SPA dehydrogenase HpfX, and a 3-sulfopropionyl-CoA synthetase HpfYZ, which oxidize 3-SPA to 3-sulfopropionate (3-SP) coupled with ATP formation. <i>E. gilvus</i> grown on SQ or DHPS produced a mixture of 3-HPS and 3-SP, indicating the bifurcated pathway. Similar genes are found in various Firmicutes, including gut bacteria. Importantly, 3-SP, but not 3-HPS, can serve as a respiratory terminal electron acceptor for <i>Bilophila wadsworthia</i>, a common intestinal pathobiont, resulting in the production of toxic H₂S. This research expands our understanding of sulfonate metabolism and reveals cross-feeding in the anaerobic microbiome.