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Mechanistically Diverse Pathways for Sulfoquinovose Degradation in Bacteria

  • Jiayi Liu
    Jiayi Liu
    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
    More by Jiayi Liu
  • Yifeng Wei
    Yifeng Wei
    Singapore Institute of Food and Biotechnology Innovation, Agency for Science, Technology and Research (A*STAR), Singapore 138669, Singapore
    More by Yifeng Wei
  • Kailiang Ma
    Kailiang Ma
    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
    More by Kailiang Ma
  • Junwei An
    Junwei An
    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
    More by Junwei An
  • Xumei Liu
    Xumei Liu
    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
    More by Xumei Liu
  • Yinbo Liu
    Yinbo Liu
    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
    More by Yinbo Liu
  • Ee Lui Ang
    Ee Lui Ang
    Singapore Institute of Food and Biotechnology Innovation, Agency for Science, Technology and Research (A*STAR), Singapore 138669, Singapore
    More by Ee Lui Ang
  • Huimin Zhao*
    Huimin Zhao
    Singapore Institute of Food and Biotechnology Innovation, Agency for Science, Technology and Research (A*STAR), Singapore 138669, Singapore
    Department of Chemical and Biomolecular Engineering, University of Illinois at Urbana-Champaign, 600 South Mathews Avenue, Urbana, Illinois 61801, United States
    *Email: [email protected]. Tel: (217) 333-2631. Fax: (217) 333-5052.
    More by Huimin Zhao
  • , and 
  • Yan Zhang*
    Yan Zhang
    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
    *Email: [email protected]. Tel: (86) 22-87401835. Fax: (86) 22-87401830.
    More by Yan Zhang
Cite this: ACS Catal. 2021, 11, 24, 14740–14750
Publication Date (Web):November 23, 2021
https://doi.org/10.1021/acscatal.1c04321
Copyright © 2021 American Chemical Society

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    Abstract

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    Sulfoquinovose (6-deoxy-6-sulfo-d-glucose, SQ) is the polar headgroup of sulfolipids present in plants and other photosynthetic organisms and is one of the most abundant organosulfur compounds in nature. Bacterial degradation of SQ, termed sulfoglycolysis, is thus an important part of the global sulfur cycle. Three sulfoglycolysis pathways have been reported to date, the first analogous to the Embden–Meyerhof–Parnas (sulfo-EMP) glycolytic pathway (reported in Gram-negative γ-proteobacteria), the second analogous to the Entner–Doudoroff (sulfo-ED) glycolytic pathway, and the third involving a transaldolase (sulfo-TAL) related to that in the pentose phosphate pathway. Here, we report the discovery of three additional sulfoglycolysis pathways, the first involving a transketolase (sulfo-TK) related to that in the pentose phosphate pathway, the second involving oxygenolytic C–S cleavage of SQ by a flavin-dependent alkanesulfonate monooxygenase (sulfo-ASMO), and the third being a variant of the sulfo-EMP pathway in Gram-positive bacteria (sulfo-EMP2). Our findings underscore the diversity of mechanisms through which bacteria degrade and utilize this ubiquitous organosulfur compound as a nutrient source.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acscatal.1c04321.

    • Experimental protocols, primers used for cloning, SDS-PAGE gels, data for characterization, and activity assays of the sulfo-TK, sulfo-ASMO, and sulfo-EMP2 pathways (PDF)

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    Cited By

    This article is cited by 9 publications.

    1. Arashdeep Kaur, Isabelle B. Pickles, Mahima Sharma, Niccolay Madeido Soler, Nichollas E. Scott, Sacha J. Pidot, Ethan D. Goddard-Borger, Gideon J. Davies, Spencer J. Williams. Widespread Family of NAD+-Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism. Journal of the American Chemical Society 2023, 145 (51) , 28216-28223. https://doi.org/10.1021/jacs.3c11126
    2. Qiongxiang Yan, Hua Huang, Xinshuai Zhang. In Vitro Reconstitution of a Bacterial Ergothioneine Sulfonate Catabolic Pathway. ACS Catalysis 2022, 12 (9) , 4825-4832. https://doi.org/10.1021/acscatal.2c00169
    3. Alexander J.D. Snow, Mahima Sharma, Palika Abayakoon, Spencer J. Williams, James N. Blaza, Gideon J. Davies. Structure and mechanism of sulfofructose transaldolase, a key enzyme in sulfoquinovose metabolism. Structure 2023, 31 (3) , 244-252.e4. https://doi.org/10.1016/j.str.2023.01.010
    4. Le Liu, Xiaofeng Chen, Jianing Ye, Xiaoyi Ma, Yu Han, Yajie He, Kai Tang. Sulfoquinovose is a widespread organosulfur substrate for Roseobacter clade bacteria in the ocean. The ISME Journal 2023, 17 (3) , 393-405. https://doi.org/10.1038/s41396-022-01353-1
    5. Janice W.-Y. Mui, David P. De Souza, Eleanor C. Saunders, Malcolm J. McConville, Spencer J. Williams, . Remodeling of Carbon Metabolism during Sulfoglycolysis in Escherichia coli. Applied and Environmental Microbiology 2023, 89 (2) https://doi.org/10.1128/aem.02016-22
    6. Hanchao Lin, Yixin Yu, Le Zhu, Nannan Lai, Luming Zhang, Yu Guo, Xinxin Lin, Dongqin Yang, Ning Ren, Zhiling Zhu, Qiongzhu Dong. Implications of hydrogen sulfide in colorectal cancer: Mechanistic insights and diagnostic and therapeutic strategies. Redox Biology 2023, 59 , 102601. https://doi.org/10.1016/j.redox.2023.102601
    7. Yifeng Wei, Yang Tong, Yan Zhang. New mechanisms for bacterial degradation of sulfoquinovose. Bioscience Reports 2022, 42 (10) https://doi.org/10.1042/BSR20220314
    8. Arashdeep Kaur, Phillip L. van der Peet, Janice W.-Y. Mui, Marion Herisse, Sacha Pidot, Spencer J. Williams. Genome sequences of Arthrobacter spp. that use a modified sulfoglycolytic Embden–Meyerhof–Parnas pathway. Archives of Microbiology 2022, 204 (3) https://doi.org/10.1007/s00203-022-02803-2
    9. Alexander J.D. Snow, Mahima Sharma, James P. Lingford, Yunyang Zhang, Janice W.-Y. Mui, Ruwan Epa, Ethan D. Goddard-Borger, Spencer J. Williams, Gideon J. Davies. The sulfoquinovosyl glycerol binding protein SmoF binds and accommodates plant sulfolipids. Current Research in Structural Biology 2022, 4 , 51-58. https://doi.org/10.1016/j.crstbi.2022.03.001

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