Modeling the Hydrolysis of Iron-Sulfur Clusters.
Identifieur interne : 000073 ( Main/Exploration ); précédent : 000072; suivant : 000074Modeling the Hydrolysis of Iron-Sulfur Clusters.
Auteurs : Murilo H. Teixeira [Brésil] ; Felipe Curtolo [Brésil] ; Sofia R G. Camilo [Brésil] ; Martin J. Field [France] ; Peng Zheng [République populaire de Chine] ; Hongbin Li [Canada] ; Guilherme M. Arantes [Brésil]Source :
- Journal of chemical information and modeling [ 1549-960X ] ; 2020.
Abstract
Iron-sulfur (FeS) clusters are essential metal cofactors involved in a wide variety of biological functions. Their catalytic efficiency, biosynthesis, and regulation depend on FeS stability in aqueous solution. Here, molecular modeling is used to investigate the hydrolysis of an oxidized (ferric) mononuclear FeS cluster by bare dissociation and water substitution mechanisms in neutral and acidic solution. First, approximate electronic structure descriptions of FeS reactions by density functional theory are validated against high-level wave function CCSD(T) calculations. Solvation contributions are included by an all-atom model with hybrid quantum chemical/molecular mechanical (QM/MM) potentials and enhanced sampling molecular dynamics simulations. The free energy profile obtained for FeS cluster hydrolysis indicates that the hybrid functional M06 together with an implicit solvent correction capture the most important aspects of FeS cluster reactivity in aqueous solution. Then, 20 reaction channels leading to two consecutive Fe-S bond ruptures were explored with this calibrated model. For all protonation states, nucleophilic substitution with concerted bond breaking and forming to iron is the preferred mechanism, both kinetic and thermodynamically. In neutral solution, proton transfer from water to the sulfur leaving group is also concerted. Dissociative reactions show higher barriers and will not be relevant for FeS reactivity when exposed to solvent. These hydrolysis mechanisms may help to explain the stability and catalytic mechanisms of FeS clusters of multiple sizes and proteins.
DOI: 10.1021/acs.jcim.9b00881
PubMed: 31790241
Affiliations:
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Teixeira</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP </wicri:regionArea><wicri:noRegion>SP </wicri:noRegion></affiliation></author><author><name sortKey="Curtolo, Felipe" sort="Curtolo, Felipe" uniqKey="Curtolo F" first="Felipe" last="Curtolo">Felipe Curtolo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP </wicri:regionArea><wicri:noRegion>SP </wicri:noRegion></affiliation></author><author><name sortKey="Camilo, Sofia R G" sort="Camilo, Sofia R G" uniqKey="Camilo S" first="Sofia R G" last="Camilo">Sofia R G. Camilo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP </wicri:regionArea><wicri:noRegion>SP </wicri:noRegion></affiliation></author><author><name sortKey="Field, Martin J" sort="Field, Martin J" uniqKey="Field M" first="Martin J" last="Field">Martin J. Field</name><affiliation wicri:level="3"><nlm:affiliation>CNRS, CEA, IRIG, Laboratoire de Chimie et Biologie des Métaux , Université Grenoble Alpes , 17 rue des Martyrs , 38000 Grenoble , France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>CNRS, CEA, IRIG, Laboratoire de Chimie et Biologie des Métaux , Université Grenoble Alpes , 17 rue des Martyrs , 38000 Grenoble </wicri:regionArea><placeName><region type="region" nuts="2">Auvergne-Rhône-Alpes</region><region type="old region" nuts="2">Rhône-Alpes</region><settlement type="city">Grenoble </settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Institut Laue-Langevin , BP 156, 41 Avenue des Martyrs , 38042 Grenoble , Cedex 9, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Institut Laue-Langevin , BP 156, 41 Avenue des Martyrs , 38042 Grenoble , Cedex 9</wicri:regionArea><wicri:noRegion>Cedex 9</wicri:noRegion><wicri:noRegion>Cedex 9</wicri:noRegion></affiliation></author><author><name sortKey="Zheng, Peng" sort="Zheng, Peng" uniqKey="Zheng P" first="Peng" last="Zheng">Peng Zheng</name><affiliation wicri:level="1"><nlm:affiliation>State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering , Nanjing University , Nanjing , Jiangsu 210023 , China.</nlm:affiliation><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering , Nanjing University , Nanjing , Jiangsu 210023 </wicri:regionArea><wicri:noRegion>Jiangsu 210023 </wicri:noRegion></affiliation></author><author><name sortKey="Li, Hongbin" sort="Li, Hongbin" uniqKey="Li H" first="Hongbin" last="Li">Hongbin Li</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry , University of British Columbia , Vancouver , British Columbia V6T 1Z1 , Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Chemistry , University of British Columbia , Vancouver , British Columbia V6T 1Z1 </wicri:regionArea><wicri:noRegion>British Columbia V6T 1Z1 </wicri:noRegion></affiliation></author><author><name sortKey="Arantes, Guilherme M" sort="Arantes, Guilherme M" uniqKey="Arantes G" first="Guilherme M" last="Arantes">Guilherme M. Arantes</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP </wicri:regionArea><wicri:noRegion>SP </wicri:noRegion></affiliation></author></analytic><series><title level="j">Journal of chemical information and modeling</title><idno type="eISSN">1549-960X</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">Iron-sulfur (FeS) clusters are essential metal cofactors involved in a wide variety of biological functions. Their catalytic efficiency, biosynthesis, and regulation depend on FeS stability in aqueous solution. Here, molecular modeling is used to investigate the hydrolysis of an oxidized (ferric) mononuclear FeS cluster by bare dissociation and water substitution mechanisms in neutral and acidic solution. First, approximate electronic structure descriptions of FeS reactions by density functional theory are validated against high-level wave function CCSD(T) calculations. Solvation contributions are included by an all-atom model with hybrid quantum chemical/molecular mechanical (QM/MM) potentials and enhanced sampling molecular dynamics simulations. The free energy profile obtained for FeS cluster hydrolysis indicates that the hybrid functional M06 together with an implicit solvent correction capture the most important aspects of FeS cluster reactivity in aqueous solution. Then, 20 reaction channels leading to two consecutive Fe-S bond ruptures were explored with this calibrated model. For all protonation states, nucleophilic substitution with concerted bond breaking and forming to iron is the preferred mechanism, both kinetic and thermodynamically. In neutral solution, proton transfer from water to the sulfur leaving group is also concerted. Dissociative reactions show higher barriers and will not be relevant for FeS reactivity when exposed to solvent. These hydrolysis mechanisms may help to explain the stability and catalytic mechanisms of FeS clusters of multiple sizes and proteins.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31790241</PMID><DateRevised><Year>2020</Year><Month>08</Month><Day>21</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1549-960X</ISSN><JournalIssue CitedMedium="Internet"><Volume>60</Volume><Issue>2</Issue><PubDate><Year>2020</Year><Month>02</Month><Day>24</Day></PubDate></JournalIssue><Title>Journal of chemical information and modeling</Title><ISOAbbreviation>J Chem Inf Model</ISOAbbreviation></Journal><ArticleTitle>Modeling the Hydrolysis of Iron-Sulfur Clusters.</ArticleTitle><Pagination><MedlinePgn>653-660</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1021/acs.jcim.9b00881</ELocationID><Abstract><AbstractText>Iron-sulfur (FeS) clusters are essential metal cofactors involved in a wide variety of biological functions. Their catalytic efficiency, biosynthesis, and regulation depend on FeS stability in aqueous solution. Here, molecular modeling is used to investigate the hydrolysis of an oxidized (ferric) mononuclear FeS cluster by bare dissociation and water substitution mechanisms in neutral and acidic solution. First, approximate electronic structure descriptions of FeS reactions by density functional theory are validated against high-level wave function CCSD(T) calculations. Solvation contributions are included by an all-atom model with hybrid quantum chemical/molecular mechanical (QM/MM) potentials and enhanced sampling molecular dynamics simulations. The free energy profile obtained for FeS cluster hydrolysis indicates that the hybrid functional M06 together with an implicit solvent correction capture the most important aspects of FeS cluster reactivity in aqueous solution. Then, 20 reaction channels leading to two consecutive Fe-S bond ruptures were explored with this calibrated model. For all protonation states, nucleophilic substitution with concerted bond breaking and forming to iron is the preferred mechanism, both kinetic and thermodynamically. In neutral solution, proton transfer from water to the sulfur leaving group is also concerted. Dissociative reactions show higher barriers and will not be relevant for FeS reactivity when exposed to solvent. These hydrolysis mechanisms may help to explain the stability and catalytic mechanisms of FeS clusters of multiple sizes and proteins.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Teixeira</LastName><ForeName>Murilo H</ForeName><Initials>MH</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Curtolo</LastName><ForeName>Felipe</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Camilo</LastName><ForeName>Sofia R G</ForeName><Initials>SRG</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Field</LastName><ForeName>Martin J</ForeName><Initials>MJ</Initials><Identifier Source="ORCID">0000-0001-8674-7997</Identifier><AffiliationInfo><Affiliation>CNRS, CEA, IRIG, Laboratoire de Chimie et Biologie des Métaux , Université Grenoble Alpes , 17 rue des Martyrs , 38000 Grenoble , France.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Institut Laue-Langevin , BP 156, 41 Avenue des Martyrs , 38042 Grenoble , Cedex 9, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zheng</LastName><ForeName>Peng</ForeName><Initials>P</Initials><Identifier Source="ORCID">0000-0003-4792-6364</Identifier><AffiliationInfo><Affiliation>State Key Laboratory of Coordination Chemistry, School of Chemistry and Chemical Engineering , Nanjing University , Nanjing , Jiangsu 210023 , China.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Hongbin</ForeName><Initials>H</Initials><Identifier Source="ORCID">0000-0001-7813-1332</Identifier><AffiliationInfo><Affiliation>Department of Chemistry , University of British Columbia , Vancouver , British Columbia V6T 1Z1 , Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Arantes</LastName><ForeName>Guilherme M</ForeName><Initials>GM</Initials><Identifier Source="ORCID">0000-0001-5356-7703</Identifier><AffiliationInfo><Affiliation>Department of Biochemistry, Instituto de Química , Universidade de São Paulo , Av. Prof. Lineu Prestes 748 , 05508-900 São Paulo , SP , Brazil.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>12</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>J Chem Inf Model</MedlineTA><NlmUniqueID>101230060</NlmUniqueID><ISSNLinking>1549-9596</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>12</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>12</Month><Day>4</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>12</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31790241</ArticleId><ArticleId IdType="doi">10.1021/acs.jcim.9b00881</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Brésil</li><li>Canada</li><li>France</li><li>République populaire de Chine</li></country><region><li>Auvergne-Rhône-Alpes</li><li>Rhône-Alpes</li></region><settlement><li>Grenoble </li></settlement></list><tree><country name="Brésil"><noRegion><name sortKey="Teixeira, Murilo H" sort="Teixeira, Murilo H" uniqKey="Teixeira M" first="Murilo H" last="Teixeira">Murilo H. Teixeira</name></noRegion><name sortKey="Arantes, Guilherme M" sort="Arantes, Guilherme M" uniqKey="Arantes G" first="Guilherme M" last="Arantes">Guilherme M. Arantes</name><name sortKey="Camilo, Sofia R G" sort="Camilo, Sofia R G" uniqKey="Camilo S" first="Sofia R G" last="Camilo">Sofia R G. Camilo</name><name sortKey="Curtolo, Felipe" sort="Curtolo, Felipe" uniqKey="Curtolo F" first="Felipe" last="Curtolo">Felipe Curtolo</name></country><country name="France"><region name="Auvergne-Rhône-Alpes"><name sortKey="Field, Martin J" sort="Field, Martin J" uniqKey="Field M" first="Martin J" last="Field">Martin J. Field</name></region><name sortKey="Field, Martin J" sort="Field, Martin J" uniqKey="Field M" first="Martin J" last="Field">Martin J. 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