Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii.
Identifieur interne : 000151 ( Main/Exploration ); précédent : 000150; suivant : 000152Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from Roseiflexus castenholzii.
Auteurs : Yang Shi [République populaire de Chine] ; Yueyong Xin [République populaire de Chine] ; Chao Wang [République populaire de Chine] ; Robert E. Blankenship [États-Unis] ; Fei Sun [République populaire de Chine] ; Xiaoling Xu [République populaire de Chine]Source :
- Science advances [ 2375-2548 ] ; 2020.
Abstract
Alternative complex III (ACIII) is a multisubunit quinol:electron acceptor oxidoreductase that couples quinol oxidation with transmembrane proton translocation in both the respiratory and photosynthetic electron transport chains of bacteria. The coupling mechanism, however, is poorly understood. Here, we report the cryo-EM structures of air-oxidized and dithionite-reduced ACIII from the photosynthetic bacterium Roseiflexus castenholzii at 3.3- and 3.5-Å resolution, respectively. We identified a menaquinol binding pocket and an electron transfer wire comprising six hemes and four iron-sulfur clusters that is capable of transferring electrons to periplasmic acceptors. We detected a proton translocation passage in which three strictly conserved, mid-passage residues are likely essential for coupling the redox-driven proton translocation across the membrane. These results allow us to propose a previously unrecognized coupling mechanism that links the respiratory and photosynthetic functions of ACIII. This study provides a structural basis for further investigation of the energy transformation mechanisms in bacterial photosynthesis and respiration.
DOI: 10.1126/sciadv.aba2739
PubMed: 32832681
PubMed Central: PMC7439408
Affiliations:
- République populaire de Chine, États-Unis
- Missouri (État)
- Pékin, Saint-Louis (Missouri)
- Université Washington de Saint-Louis
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China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Laboratory of Biomacromolecules, National Center of Protein Science-Beijing, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>University of Chinese Academy of Sciences, Beijing 100049, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>University of Chinese Academy of Sciences, Beijing 100049</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xin, Yueyong" sort="Xin, Yueyong" uniqKey="Xin Y" first="Yueyong" last="Xin">Yueyong Xin</name><affiliation wicri:level="1"><nlm:affiliation>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province</wicri:regionArea><wicri:noRegion>Zhejiang Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, Zhejiang, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Chao" sort="Wang, Chao" uniqKey="Wang C" first="Chao" last="Wang">Chao Wang</name><affiliation wicri:level="1"><nlm:affiliation>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province</wicri:regionArea><wicri:noRegion>Zhejiang Province</wicri:noRegion></affiliation></author><author><name sortKey="Blankenship, Robert E" sort="Blankenship, Robert E" uniqKey="Blankenship R" first="Robert E" last="Blankenship">Robert E. Blankenship</name><affiliation wicri:level="4"><nlm:affiliation>Departments of Biology and Chemistry, Washington University in St. Louis, St. Louis, MO 63130, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Biology and Chemistry, Washington University in St. Louis, St. Louis, MO 63130</wicri:regionArea><placeName><region type="state">Missouri (État)</region><settlement type="city">Saint-Louis (Missouri)</settlement></placeName><orgName type="university">Université Washington de Saint-Louis</orgName></affiliation></author><author><name sortKey="Sun, Fei" sort="Sun, Fei" uniqKey="Sun F" first="Fei" last="Sun">Fei Sun</name><affiliation wicri:level="1"><nlm:affiliation>National Laboratory of Biomacromolecules, National Center of Protein Science-Beijing, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>National Laboratory of Biomacromolecules, National Center of Protein Science-Beijing, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>University of Chinese Academy of Sciences, Beijing 100049, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>University of Chinese Academy of Sciences, Beijing 100049</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Center for Biological Imaging, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Center for Biological Imaging, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Xu, Xiaoling" sort="Xu, Xiaoling" uniqKey="Xu X" first="Xiaoling" last="Xu">Xiaoling Xu</name><affiliation wicri:level="1"><nlm:affiliation>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province</wicri:regionArea><wicri:noRegion>Zhejiang Province</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, Zhejiang, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>Key Laboratory of Aging and Cancer Biology of Zhejiang Province, School of Medicine and The Affiliated Hospital, Hangzhou Normal University, Hangzhou 311121, Zhejiang, China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Key Laboratory of Aging and Cancer Biology of Zhejiang Province, School of Medicine and The Affiliated Hospital, Hangzhou Normal University, Hangzhou 311121, Zhejiang</wicri:regionArea><wicri:noRegion>Zhejiang</wicri:noRegion></affiliation></author></analytic><series><title level="j">Science advances</title><idno type="eISSN">2375-2548</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Alternative complex III (ACIII) is a multisubunit quinol:electron acceptor oxidoreductase that couples quinol oxidation with transmembrane proton translocation in both the respiratory and photosynthetic electron transport chains of bacteria. The coupling mechanism, however, is poorly understood. Here, we report the cryo-EM structures of air-oxidized and dithionite-reduced ACIII from the photosynthetic bacterium <i>Roseiflexus castenholzii</i> at 3.3- and 3.5-Å resolution, respectively. We identified a menaquinol binding pocket and an electron transfer wire comprising six hemes and four iron-sulfur clusters that is capable of transferring electrons to periplasmic acceptors. We detected a proton translocation passage in which three strictly conserved, mid-passage residues are likely essential for coupling the redox-driven proton translocation across the membrane. These results allow us to propose a previously unrecognized coupling mechanism that links the respiratory and photosynthetic functions of ACIII. This study provides a structural basis for further investigation of the energy transformation mechanisms in bacterial photosynthesis and respiration.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32832681</PMID><DateRevised><Year>2020</Year><Month>08</Month><Day>25</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">2375-2548</ISSN><JournalIssue CitedMedium="Internet"><Volume>6</Volume><Issue>31</Issue><PubDate><Year>2020</Year><Month>Jul</Month></PubDate></JournalIssue><Title>Science advances</Title><ISOAbbreviation>Sci Adv</ISOAbbreviation></Journal><ArticleTitle>Cryo-EM structures of the air-oxidized and dithionite-reduced photosynthetic alternative complex III from <i>Roseiflexus castenholzii</i>.</ArticleTitle><Pagination><MedlinePgn>eaba2739</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1126/sciadv.aba2739</ELocationID><Abstract><AbstractText>Alternative complex III (ACIII) is a multisubunit quinol:electron acceptor oxidoreductase that couples quinol oxidation with transmembrane proton translocation in both the respiratory and photosynthetic electron transport chains of bacteria. The coupling mechanism, however, is poorly understood. Here, we report the cryo-EM structures of air-oxidized and dithionite-reduced ACIII from the photosynthetic bacterium <i>Roseiflexus castenholzii</i> at 3.3- and 3.5-Å resolution, respectively. We identified a menaquinol binding pocket and an electron transfer wire comprising six hemes and four iron-sulfur clusters that is capable of transferring electrons to periplasmic acceptors. We detected a proton translocation passage in which three strictly conserved, mid-passage residues are likely essential for coupling the redox-driven proton translocation across the membrane. These results allow us to propose a previously unrecognized coupling mechanism that links the respiratory and photosynthetic functions of ACIII. This study provides a structural basis for further investigation of the energy transformation mechanisms in bacterial photosynthesis and respiration.</AbstractText><CopyrightInformation>Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Shi</LastName><ForeName>Yang</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0003-1579-7561</Identifier><AffiliationInfo><Affiliation>National Laboratory of Biomacromolecules, National Center of Protein Science-Beijing, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>University of Chinese Academy of Sciences, Beijing 100049, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xin</LastName><ForeName>Yueyong</ForeName><Initials>Y</Initials><Identifier Source="ORCID">0000-0002-0252-7346</Identifier><AffiliationInfo><Affiliation>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, Zhejiang, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Wang</LastName><ForeName>Chao</ForeName><Initials>C</Initials><Identifier Source="ORCID">0000-0002-0534-8984</Identifier><AffiliationInfo><Affiliation>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Blankenship</LastName><ForeName>Robert E</ForeName><Initials>RE</Initials><Identifier Source="ORCID">0000-0003-0879-9489</Identifier><AffiliationInfo><Affiliation>Departments of Biology and Chemistry, Washington University in St. Louis, St. Louis, MO 63130, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sun</LastName><ForeName>Fei</ForeName><Initials>F</Initials><Identifier Source="ORCID">0000-0002-0351-5144</Identifier><AffiliationInfo><Affiliation>National Laboratory of Biomacromolecules, National Center of Protein Science-Beijing, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>University of Chinese Academy of Sciences, Beijing 100049, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Center for Biological Imaging, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Xu</LastName><ForeName>Xiaoling</ForeName><Initials>X</Initials><Identifier Source="ORCID">0000-0001-8995-1213</Identifier><AffiliationInfo><Affiliation>Hangzhou Normal University, 2318 Yuhangtang Road, Cangqian, Yuhang District, Hangzhou 311121, Zhejiang Province, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Photosynthesis Research Center, College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 311121, Zhejiang, China.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Key Laboratory of Aging and Cancer Biology of Zhejiang Province, School of Medicine and The Affiliated Hospital, Hangzhou Normal University, Hangzhou 311121, Zhejiang, China.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Sci 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E" sort="Blankenship, Robert E" uniqKey="Blankenship R" first="Robert E" last="Blankenship">Robert E. 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