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

iScience (Oct 2024)

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

Journal volume & issue: Vol. 27, no. 10
p. 111010

Abstract

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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.

Published in iScience

ISSN: 2589-0042 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Science
Website: http://www.cell.com/iscience/home

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