Study of sulfoglycolysis in Enterococcus gilvus reveals a widespread bifurcated pathway for dihydroxypropanesulfonate degradation
Yiwei Chen,
Ruoxing Chu,
Kailiang Ma,
Li Jiang,
Qiaoyu Yang,
Zhi Li,
Min Hu,
Qiuyi Guo,
Fengxia Lu,
Yifeng Wei,
Yan Zhang,
Yang Tong
Affiliations
Yiwei Chen
College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Ruoxing Chu
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Kailiang Ma
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Li Jiang
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Qiaoyu Yang
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Zhi Li
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Min Hu
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Qiuyi Guo
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China
Fengxia Lu
College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China; Corresponding author
Yifeng Wei
Singapore Institute of Food and Biotechnology Innovation, Agency for Science, Technology and Research (A∗STAR), Singapore 138669, Singapore; Corresponding author
Yan Zhang
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Frontiers Science Center for Synthetic Biology (Ministry of Education), Tianjin University, Tianjin 300072, China; Key Laboratory of Systems Bioengineering (Ministry of Education), School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China; School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China; Carbon-Negative Synthetic Biology for Biomaterial Production from CO2 (CNSB), Campus for Research Excellence and Technological Enterprise (CREATE), 1 CREATE Way, Singapore 138602, Singapore; Corresponding author
Yang Tong
New Cornerstone Science Laboratory, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Tianjin Key Laboratory for Modern Drug Delivery & High-Efficiency, Collaborative Innovation Center of Chemical Science and Engineering, School of Pharmaceutical Science and Technology, Tianjin University, Tianjin 300072, China; Corresponding author
Summary: 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 Enterococcus gilvus, 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. E. gilvus 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 Bilophila wadsworthia, 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.
