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Structural insights into the electron/proton transfer pathways in the quinol:fumarate reductase from Desulfovibrio gigas

Guan, Hong-Hsiang and Hsieh, Yin-Cheng and Lin, Pei-Ju and Huang, Yen-Chieh and Yoshimura, Masato and Chen, Li-Ying and Chen, Shao-Kang and Chuankhayan, Phimonphan and Lin, Chien-Chih and Chen, Nai-Chi and Nakagawa, Atsushi and Chan, Sunney I. and Chen, Chun-Jung (2018) Structural insights into the electron/proton transfer pathways in the quinol:fumarate reductase from Desulfovibrio gigas. Scientific Reports, 8 . Art. No. 14935. ISSN 2045-2322. PMCID PMC6175931. https://resolver.caltech.edu/CaltechAUTHORS:20181016-085612513

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Abstract

The membrane-embedded quinol:fumarate reductase (QFR) in anaerobic bacteria catalyzes the reduction of fumarate to succinate by quinol in the anaerobic respiratory chain. The electron/proton-transfer pathways in QFRs remain controversial. Here we report the crystal structure of QFR from the anaerobic sulphate-reducing bacterium Desulfovibrio gigas (D. gigas) at 3.6 Å resolution. The structure of the D. gigas QFR is a homo-dimer, each protomer comprising two hydrophilic subunits, A and B, and one transmembrane subunit C, together with six redox cofactors including two b-hemes. One menaquinone molecule is bound near heme b_L in the hydrophobic subunit C. This location of the menaquinone-binding site differs from the menaquinol-binding cavity proposed previously for QFR from Wolinella succinogenes. The observed bound menaquinone might serve as an additional redox cofactor to mediate the proton-coupled electron transport across the membrane. Armed with these structural insights, we propose electron/proton-transfer pathways in the quinol reduction of fumarate to succinate in the D. gigas QFR.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41598-018-33193-5DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6175931PubMed CentralArticle
ORCID:
AuthorORCID
Yoshimura, Masato0000-0002-7466-2192
Nakagawa, Atsushi0000-0002-1700-7861
Chan, Sunney I.0000-0002-5348-2723
Chen, Chun-Jung0000-0002-5157-4288
Additional Information:© 2018 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 29 March 2018; Accepted 18 September 2018; Published 08 October 2018. Accession Codes: The structural factors and coordinates have been deposited in the RCSB Protein Data Bank. The PDB code is 5XMJ. We are indebted to the Yuch-Cheng Jean and staff at TLS beamlines BL13B1, BL13C1 and BL15A1 and TPS 05 A at the National Synchrotron Radiation Research Center (NSRRC) in Taiwan and Hirofumi Ishii at the Taiwan contracted beamline BL12B2 and Eiki Yamashita and Akifumi Higashiura at the BL44XU at SPring-8 in Japan for technical assistance under the proposal numbers 2014B6600, 2014B6965, 2015A6600, 2015A4000, 2015B6600, 2015B4004, 2015B4010, 2016A6600, 2016A6659, 2016A4012, 2016B6600, 2016B4000, 2017A4000, 2017A6600, 2017B4000, 2017B6769 and 2017B6600. This work was in part performed under the International Collaborative Research Program of Institute for Protein Research, Osaka University, ICR-17-05. Portions of this research were carried out at the NSRRC-NCKU Protein Crystallography Laboratory at National Cheng Kung University (NCKU). This work was supported in part by National Science Council (NSC) grants 101–2628-B-213-001-MY4, 102-2627-M-213-001-MY3, Ministry of Science and Technology (MOST) 105-2311-B-231-001-MY3 and NSRRC grants 1034RSB02, 1044RSB02, 1054RSB02 and 1064RSB02 to C.-J. Chen. Author Contributions: Yin-Cheng Hsieh, Yen-Chieh Huang and Pei-Ju Lin performed the cell culturing of D. gigas and QFR protein purification and characterization; Yin-Cheng Hsieh carried out the crystallization and the crystal optimization; Yin-Cheng Hsieh and Masato Yoshimura did the data collection and diffraction data analyses; Hong-Hsiang Guan determined and refined the structure; Hong-Hsiang Guan, Li-Ying Chen, Phimonphan Chuankhayan, Chien-Chih Lin, Nai-Chi Chen, Shao-Kang Chen and Sunney I. Chan analyzed the structure and interpret the functional mechanism. Atsushi Nakagawa provided the collaborative BL44XU beamtime and discussion. Chun-Jung Chen initiated the project and designed the research; Hong-Hsiang Guan, Sunney I. Chan and Chun-Jung Chen wrote and edited the paper. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
National Science Council (Taipei)101-2628-B-213-001-MY4
National Science Council (Taipei)102-2627-M-213-001-MY3
Ministry of Science and Technology (Taipei)105-2311-B-231-001-MY3
National Synchrotron Radiation Research Center1034RSB02
National Synchrotron Radiation Research Center1044RSB02
National Synchrotron Radiation Research Center1054RSB02
National Synchrotron Radiation Research Center1064RSB02
PubMed Central ID:PMC6175931
Record Number:CaltechAUTHORS:20181016-085612513
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181016-085612513
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90274
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:16 Oct 2018 17:23
Last Modified:03 Oct 2019 20:23

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