XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase
Methyl-Coenzyme M Reductase (MCR) catalyzes the biosynthesis of methane in methanogenic archaea, using a catalytic Ni-centered Cofactor F430 in its active site. It also catalyzes the reverse reaction, that is, the anaerobic activation and oxidation, including the cleavage of the CH bond in methane....
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier BV
2022
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| Online Access: | https://hdl.handle.net/1721.1/146795 |
| _version_ | 1826197000263041024 |
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| author | Ohmer, Christopher J Dasgupta, Medhanjali Patwardhan, Anjali Bogacz, Isabel Kaminsky, Corey Doyle, Margaret D Chen, Percival Yang-Ting Keable, Stephen M Makita, Hiroki Simon, Philipp S Massad, Ramzi Fransson, Thomas Chatterjee, Ruchira Bhowmick, Asmit Paley, Daniel W Moriarty, Nigel W Brewster, Aaron S Gee, Leland B Alonso-Mori, Roberto Moss, Frank Fuller, Franklin D Batyuk, Alexander Sauter, Nicholas K Bergmann, Uwe Drennan, Catherine L Yachandra, Vittal K Yano, Junko Kern, Jan F Ragsdale, Stephen W |
| author2 | Massachusetts Institute of Technology. Department of Biology |
| author_facet | Massachusetts Institute of Technology. Department of Biology Ohmer, Christopher J Dasgupta, Medhanjali Patwardhan, Anjali Bogacz, Isabel Kaminsky, Corey Doyle, Margaret D Chen, Percival Yang-Ting Keable, Stephen M Makita, Hiroki Simon, Philipp S Massad, Ramzi Fransson, Thomas Chatterjee, Ruchira Bhowmick, Asmit Paley, Daniel W Moriarty, Nigel W Brewster, Aaron S Gee, Leland B Alonso-Mori, Roberto Moss, Frank Fuller, Franklin D Batyuk, Alexander Sauter, Nicholas K Bergmann, Uwe Drennan, Catherine L Yachandra, Vittal K Yano, Junko Kern, Jan F Ragsdale, Stephen W |
| author_sort | Ohmer, Christopher J |
| collection | MIT |
| description | Methyl-Coenzyme M Reductase (MCR) catalyzes the biosynthesis of methane in methanogenic archaea, using a catalytic Ni-centered Cofactor F430 in its active site. It also catalyzes the reverse reaction, that is, the anaerobic activation and oxidation, including the cleavage of the CH bond in methane. Because methanogenesis is the major source of methane on earth, understanding the reaction mechanism of this enzyme can have massive implications in global energy balances. While recent publications have proposed a radical-based catalytic mechanism as well as novel sulfonate-based binding modes of MCR for its native substrates, the structure of the active state of MCR, as well as a complete characterization of the reaction, remain elusive. Previous attempts to structurally characterize the active MCR-Ni(I) state have been unsuccessful due to oxidation of the redox- sensitive catalytic Ni center. Further, while many cryo structures of the inactive Ni(II)-enzyme in various substrates-bound forms have been published, no room temperature structures have been reported, and the structure and mechanism of MCR under physiologically relevant conditions is not known. In this study, we report the first room temperature structure of the MCRred1-silent Ni(II) form using an X-ray Free-Electron Laser (XFEL), with simultaneous X-ray Emission Spectroscopy (XES) and X-ray Diffraction (XRD) data collection. In celebration of the seminal contributions of inorganic chemist Dick Holm to our understanding of nickel-based catalysis, we are honored to announce our findings in this special issue dedicated to this remarkable pioneer of bioinorganic chemistry. |
| first_indexed | 2024-09-23T10:41:11Z |
| format | Article |
| id | mit-1721.1/146795 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2025-02-19T04:19:10Z |
| publishDate | 2022 |
| publisher | Elsevier BV |
| record_format | dspace |
| spelling | mit-1721.1/1467952024-12-21T06:08:11Z XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase Ohmer, Christopher J Dasgupta, Medhanjali Patwardhan, Anjali Bogacz, Isabel Kaminsky, Corey Doyle, Margaret D Chen, Percival Yang-Ting Keable, Stephen M Makita, Hiroki Simon, Philipp S Massad, Ramzi Fransson, Thomas Chatterjee, Ruchira Bhowmick, Asmit Paley, Daniel W Moriarty, Nigel W Brewster, Aaron S Gee, Leland B Alonso-Mori, Roberto Moss, Frank Fuller, Franklin D Batyuk, Alexander Sauter, Nicholas K Bergmann, Uwe Drennan, Catherine L Yachandra, Vittal K Yano, Junko Kern, Jan F Ragsdale, Stephen W Massachusetts Institute of Technology. Department of Biology Methyl-Coenzyme M Reductase (MCR) catalyzes the biosynthesis of methane in methanogenic archaea, using a catalytic Ni-centered Cofactor F430 in its active site. It also catalyzes the reverse reaction, that is, the anaerobic activation and oxidation, including the cleavage of the CH bond in methane. Because methanogenesis is the major source of methane on earth, understanding the reaction mechanism of this enzyme can have massive implications in global energy balances. While recent publications have proposed a radical-based catalytic mechanism as well as novel sulfonate-based binding modes of MCR for its native substrates, the structure of the active state of MCR, as well as a complete characterization of the reaction, remain elusive. Previous attempts to structurally characterize the active MCR-Ni(I) state have been unsuccessful due to oxidation of the redox- sensitive catalytic Ni center. Further, while many cryo structures of the inactive Ni(II)-enzyme in various substrates-bound forms have been published, no room temperature structures have been reported, and the structure and mechanism of MCR under physiologically relevant conditions is not known. In this study, we report the first room temperature structure of the MCRred1-silent Ni(II) form using an X-ray Free-Electron Laser (XFEL), with simultaneous X-ray Emission Spectroscopy (XES) and X-ray Diffraction (XRD) data collection. In celebration of the seminal contributions of inorganic chemist Dick Holm to our understanding of nickel-based catalysis, we are honored to announce our findings in this special issue dedicated to this remarkable pioneer of bioinorganic chemistry. 2022-12-07T19:00:16Z 2022-12-07T19:00:16Z 2022 2022-12-07T18:56:00Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/146795 Ohmer, Christopher J, Dasgupta, Medhanjali, Patwardhan, Anjali, Bogacz, Isabel, Kaminsky, Corey et al. 2022. "XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase." Journal of Inorganic Biochemistry, 230. en 10.1016/J.JINORGBIO.2022.111768 Journal of Inorganic Biochemistry Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier BV PMC |
| spellingShingle | Ohmer, Christopher J Dasgupta, Medhanjali Patwardhan, Anjali Bogacz, Isabel Kaminsky, Corey Doyle, Margaret D Chen, Percival Yang-Ting Keable, Stephen M Makita, Hiroki Simon, Philipp S Massad, Ramzi Fransson, Thomas Chatterjee, Ruchira Bhowmick, Asmit Paley, Daniel W Moriarty, Nigel W Brewster, Aaron S Gee, Leland B Alonso-Mori, Roberto Moss, Frank Fuller, Franklin D Batyuk, Alexander Sauter, Nicholas K Bergmann, Uwe Drennan, Catherine L Yachandra, Vittal K Yano, Junko Kern, Jan F Ragsdale, Stephen W XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase |
| title | XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase |
| title_full | XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase |
| title_fullStr | XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase |
| title_full_unstemmed | XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase |
| title_short | XFEL serial crystallography reveals the room temperature structure of methyl-coenzyme M reductase |
| title_sort | xfel serial crystallography reveals the room temperature structure of methyl coenzyme m reductase |
| url | https://hdl.handle.net/1721.1/146795 |
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