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In Vitro Reconstitution of a Five-Step Pathway for Bacterial Ergothioneine Catabolism

Cite this: ACS Chem. Biol. 2021, 16, 2, 397–403
Publication Date (Web):February 5, 2021
https://doi.org/10.1021/acschembio.0c00968
Copyright © 2021 American Chemical Society

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    Abstract

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    Ergothioneine is a histidine-derived sulfur metabolite that is biosynthesized by bacteria and fungi. Plants and animals absorb ergothioneine as a micronutrient from their environment or nutrition. Several different mechanisms of microbial ergothioneine production have been described in the past ten years. Much less is known about the genetic and structural basis for ergothioneine catabolism. In this report, we describe the in vitro reconstitution of a five-step pathway that degrades ergothioneine to l-glutamate, trimethylamine, hydrogen sulfide, carbon dioxide, and ammonia. The first two steps are catalyzed by the two enzymes ergothionase and thiourocanate hydratase. These enzymes are closely related to the first two enzymes in histidine catabolism. However, the crystal structure of thiourocanate hydratase from the firmicute Paenibacillus sp. reveals specific structural features that strictly differentiate the activity of this enzyme from that of urocanate hydratases. The final two steps are catalyzed by metal-dependent hydrolases that share most homology with the last two enzymes in uracil catabolism. The early and late part of this pathway are connected by an entirely new enzyme type that catalyzes desulfurization of a thiohydantoin intermediate. Homologous enzymes are encoded in many soil-dwelling firmicutes and proteobacteria, suggesting that bacterial activity may have a significant impact on the environmental availability of ergothioneine.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acschembio.0c00968.

    • Detailed descriptions of all experiments, Figures S1–S24, and Tables S1–S5 (PDF)

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    Cited By

    This article is cited by 14 publications.

    1. Camille M. Vasseur, Dishani Karunasegaram, Florian P. Seebeck. Structure and Substrate Specificity of S-Methyl Thiourocanate Hydratase. ACS Chemical Biology 2024, 19 (3) , 718-724. https://doi.org/10.1021/acschembio.3c00745
    2. Mariia A. Beliaeva, Reyhan Atac, Florian P. Seebeck. Bacterial Degradation of Nτ-Methylhistidine. ACS Chemical Biology 2022, 17 (7) , 1989-1995. https://doi.org/10.1021/acschembio.2c00437
    3. 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
    4. Barry Halliwell, Irwin Cheah. Are age-related neurodegenerative diseases caused by a lack of the diet-derived compound ergothioneine?. Free Radical Biology and Medicine 2024, 217 , 60-67. https://doi.org/10.1016/j.freeradbiomed.2024.03.009
    5. Egor Y. Nalivaiko, Florian P. Seebeck. A Rhodanese‐Like Enzyme that Catalyzes Desulfination of Ergothioneine Sulfinic Acid. ChemBioChem 2024, 596 https://doi.org/10.1002/cbic.202400131
    6. Yannik Brack, Chenghai Sun, Dong Yi, Uwe T. Bornscheuer. Systematic Analysis of the MIO‐forming Residues of Aromatic Ammonia Lyases. ChemBioChem 2024, 25 (6) https://doi.org/10.1002/cbic.202400016
    7. Egor Y. Nalivaiko, Camille M. Vasseur, Florian P. Seebeck. Enzyme‐Catalyzed Oxidative Degradation of Ergothioneine. Angewandte Chemie 2024, 136 (8) https://doi.org/10.1002/ange.202318445
    8. Egor Y. Nalivaiko, Camille M. Vasseur, Florian P. Seebeck. Enzyme‐Catalyzed Oxidative Degradation of Ergothioneine. Angewandte Chemie International Edition 2024, 63 (8) https://doi.org/10.1002/anie.202318445
    9. Hisashi Muramatsu, Daisuke Inouchi, Masaaki Yamada, Akihito Koujitani, Hiroki Maguchi, Shin-ichiro Kato. Purification and characterization of 3-(5-oxo-2-thioxoimidazolidin-4-yl) propionic acid desulfhydrase involved in ergothioneine utilization in Burkholderia sp. HME13. Bioscience, Biotechnology, and Biochemistry 2023, 88 (1) , 74-78. https://doi.org/10.1093/bbb/zbad139
    10. Daniel G. Dumitrescu, Stavroula K. Hatzios. Emerging roles of low-molecular-weight thiols at the host–microbe interface. Current Opinion in Chemical Biology 2023, 75 , 102322. https://doi.org/10.1016/j.cbpa.2023.102322
    11. Hisashi Muramatsu, Akihito Koujitani, Masaaki Yamada, Hiroki Maguchi, Takehiro Kashiwagi, Shin-ichiro Kato. Characterization of hydantoin-5-propionic acid amidohydrolase involved in ergothioneine utilization in Burkholderia sp. HME13. Bioscience, Biotechnology, and Biochemistry 2023, 87 (4) , 411-419. https://doi.org/10.1093/bbb/zbad002
    12. Yifan Zhang, Giovanni Gonzalez-Gutierrez, Katherine A. Legg, Brenna J. C. Walsh, Cristian M. Pis Diez, Katherine A. Edmonds, David P. Giedroc. Discovery and structure of a widespread bacterial ABC transporter specific for ergothioneine. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-35277-3
    13. Daniel G. Dumitrescu, Elizabeth M. Gordon, Yekaterina Kovalyova, Anna B. Seminara, Brianna Duncan-Lowey, Emily R. Forster, Wen Zhou, Carmen J. Booth, Aimee Shen, Philip J. Kranzusch, Stavroula K. Hatzios. A microbial transporter of the dietary antioxidant ergothioneine. Cell 2022, 185 (24) , 4526-4540.e18. https://doi.org/10.1016/j.cell.2022.10.008
    14. Jean‐Claude Yadan. Matching chemical properties to molecular biological activities opens a new perspective on l ‐ergothioneine. FEBS Letters 2022, 596 (10) , 1299-1312. https://doi.org/10.1002/1873-3468.14264

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