The [4Fe-4S] cluster of sulfurtransferase TtuA desulfurizes TtuB during tRNA modification in Thermus thermophilus.
Identifieur interne : 000020 ( Main/Exploration ); précédent : 000019; suivant : 000021The [4Fe-4S] cluster of sulfurtransferase TtuA desulfurizes TtuB during tRNA modification in Thermus thermophilus.
Auteurs : Minghao Chen [Japon] ; Masato Ishizaka [Japon] ; Shun Narai [Japon] ; Masaki Horitani [Japon] ; Naoki Shigi [Japon] ; Min Yao [Japon] ; Yoshikazu Tanaka [Japon]Source :
- Communications biology [ 2399-3642 ] ; 2020.
Abstract
TtuA and TtuB are the sulfurtransferase and sulfur donor proteins, respectively, for biosynthesis of 2-thioribothymidine (s2T) at position 54 of transfer RNA (tRNA), which is responsible for adaptation to high temperature environments in Thermus thermophilus. The enzymatic activity of TtuA requires an iron-sulfur (Fe-S) cluster, by which a sulfur atom supplied by TtuB is transferred to the tRNA substrate. Here, we demonstrate that the Fe-S cluster directly receives sulfur from TtuB through its inherent coordination ability. TtuB forms a [4Fe-4S]-TtuB intermediate, but that sulfur is not immediately released from TtuB. Further desulfurization assays and mutation studies demonstrated that the release of sulfur from the thiocarboxylated C-terminus of TtuB is dependent on adenylation of the substrate tRNA, and the essential residue for TtuB desulfurization was identified. Based on these findings, the molecular mechanism of sulfur transfer from TtuB to Fe-S cluster is proposed.
DOI: 10.1038/s42003-020-0895-3
PubMed: 32265486
PubMed Central: PMC7138817
Affiliations:
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TtuB during tRNA modification in Thermus thermophilus.</title><author><name sortKey="Chen, Minghao" sort="Chen, Minghao" uniqKey="Chen M" first="Minghao" last="Chen">Minghao Chen</name><affiliation wicri:level="1"><nlm:affiliation>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810</wicri:regionArea><wicri:noRegion>060-0810</wicri:noRegion></affiliation></author><author><name sortKey="Ishizaka, Masato" sort="Ishizaka, Masato" uniqKey="Ishizaka M" first="Masato" last="Ishizaka">Masato Ishizaka</name><affiliation wicri:level="1"><nlm:affiliation>Graduate School of Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Graduate School of Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810</wicri:regionArea><wicri:noRegion>060-0810</wicri:noRegion></affiliation></author><author><name sortKey="Narai, Shun" sort="Narai, Shun" uniqKey="Narai S" first="Shun" last="Narai">Shun Narai</name><affiliation wicri:level="1"><nlm:affiliation>Graduate School of Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Graduate School of Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810</wicri:regionArea><wicri:noRegion>060-0810</wicri:noRegion></affiliation></author><author><name sortKey="Horitani, Masaki" sort="Horitani, Masaki" uniqKey="Horitani M" first="Masaki" last="Horitani">Masaki Horitani</name><affiliation wicri:level="1"><nlm:affiliation>Faculty of Agriculture, Department of Applied Biochemistry and Food Science, Saga University, 1 Honjo-machi, Saga, 840-8502, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Faculty of Agriculture, Department of Applied Biochemistry and Food Science, Saga University, 1 Honjo-machi, Saga, 840-8502</wicri:regionArea><wicri:noRegion>840-8502</wicri:noRegion></affiliation></author><author><name sortKey="Shigi, Naoki" sort="Shigi, Naoki" uniqKey="Shigi N" first="Naoki" last="Shigi">Naoki Shigi</name><affiliation wicri:level="1"><nlm:affiliation>Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology, 2-4-7 Aomi, Koto-ku, Tokyo, 135-0064, Japan.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology, 2-4-7 Aomi, Koto-ku, Tokyo, 135-0064</wicri:regionArea><wicri:noRegion>135-0064</wicri:noRegion></affiliation></author><author><name sortKey="Yao, Min" sort="Yao, Min" uniqKey="Yao M" first="Min" last="Yao">Min Yao</name><affiliation wicri:level="1"><nlm:affiliation>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan. yao@castor.sci.hokudai.ac.jp.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810</wicri:regionArea><wicri:noRegion>060-0810</wicri:noRegion></affiliation></author><author><name sortKey="Tanaka, Yoshikazu" sort="Tanaka, Yoshikazu" uniqKey="Tanaka Y" first="Yoshikazu" last="Tanaka">Yoshikazu Tanaka</name><affiliation wicri:level="1"><nlm:affiliation>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan. yoshikazu.tanaka@tohoku.ac.jp.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810</wicri:regionArea><wicri:noRegion>060-0810</wicri:noRegion></affiliation><affiliation wicri:level="4"><nlm:affiliation>Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan. yoshikazu.tanaka@tohoku.ac.jp.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577</wicri:regionArea><orgName type="university">Université du Tōhoku</orgName><placeName><settlement type="city">Sendai</settlement><region type="province">Région de Tōhoku</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Japan Science and Technology Agency, PRESTO, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan. yoshikazu.tanaka@tohoku.ac.jp.</nlm:affiliation><country xml:lang="fr">Japon</country><wicri:regionArea>Japan Science and Technology Agency, PRESTO, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577</wicri:regionArea><wicri:noRegion>980-8577</wicri:noRegion></affiliation></author></analytic><series><title level="j">Communications biology</title><idno type="eISSN">2399-3642</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">TtuA and TtuB are the sulfurtransferase and sulfur donor proteins, respectively, for biosynthesis of 2-thioribothymidine (s<sup>2</sup>T) at position 54 of transfer RNA (tRNA), which is responsible for adaptation to high temperature environments in Thermus thermophilus. The enzymatic activity of TtuA requires an iron-sulfur (Fe-S) cluster, by which a sulfur atom supplied by TtuB is transferred to the tRNA substrate. Here, we demonstrate that the Fe-S cluster directly receives sulfur from TtuB through its inherent coordination ability. TtuB forms a [4Fe-4S]-TtuB intermediate, but that sulfur is not immediately released from TtuB. Further desulfurization assays and mutation studies demonstrated that the release of sulfur from the thiocarboxylated C-terminus of TtuB is dependent on adenylation of the substrate tRNA, and the essential residue for TtuB desulfurization was identified. Based on these findings, the molecular mechanism of sulfur transfer from TtuB to Fe-S cluster is proposed.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">32265486</PMID><DateRevised><Year>2020</Year><Month>04</Month><Day>14</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2399-3642</ISSN><JournalIssue CitedMedium="Internet"><Volume>3</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>Apr</Month><Day>07</Day></PubDate></JournalIssue><Title>Communications biology</Title><ISOAbbreviation>Commun Biol</ISOAbbreviation></Journal><ArticleTitle>The [4Fe-4S] cluster of sulfurtransferase TtuA desulfurizes TtuB during tRNA modification in Thermus thermophilus.</ArticleTitle><Pagination><MedlinePgn>168</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s42003-020-0895-3</ELocationID><Abstract><AbstractText>TtuA and TtuB are the sulfurtransferase and sulfur donor proteins, respectively, for biosynthesis of 2-thioribothymidine (s<sup>2</sup>T) at position 54 of transfer RNA (tRNA), which is responsible for adaptation to high temperature environments in Thermus thermophilus. The enzymatic activity of TtuA requires an iron-sulfur (Fe-S) cluster, by which a sulfur atom supplied by TtuB is transferred to the tRNA substrate. Here, we demonstrate that the Fe-S cluster directly receives sulfur from TtuB through its inherent coordination ability. TtuB forms a [4Fe-4S]-TtuB intermediate, but that sulfur is not immediately released from TtuB. Further desulfurization assays and mutation studies demonstrated that the release of sulfur from the thiocarboxylated C-terminus of TtuB is dependent on adenylation of the substrate tRNA, and the essential residue for TtuB desulfurization was identified. Based on these findings, the molecular mechanism of sulfur transfer from TtuB to Fe-S cluster is proposed.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Minghao</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-7668-3974</Identifier><AffiliationInfo><Affiliation>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ishizaka</LastName><ForeName>Masato</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Graduate School of Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Narai</LastName><ForeName>Shun</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Graduate School of Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Horitani</LastName><ForeName>Masaki</ForeName><Initials>M</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-8881-0600</Identifier><AffiliationInfo><Affiliation>Faculty of Agriculture, Department of Applied Biochemistry and Food Science, Saga University, 1 Honjo-machi, Saga, 840-8502, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shigi</LastName><ForeName>Naoki</ForeName><Initials>N</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-4452-8264</Identifier><AffiliationInfo><Affiliation>Biotechnology Research Institute for Drug Discovery, National Institute of Advanced Industrial Science and Technology, 2-4-7 Aomi, Koto-ku, Tokyo, 135-0064, Japan.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Yao</LastName><ForeName>Min</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan. yao@castor.sci.hokudai.ac.jp.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tanaka</LastName><ForeName>Yoshikazu</ForeName><Initials>Y</Initials><Identifier Source="ORCID">http://orcid.org/0000-0002-7893-3236</Identifier><AffiliationInfo><Affiliation>Faculty of Advanced Life Science, Hokkaido University, Kita 8, Nishi 5, Kita-ku, Sapporo, Hokkaido, 060-0810, Japan. yoshikazu.tanaka@tohoku.ac.jp.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Graduate School of Life Sciences, Tohoku University, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan. yoshikazu.tanaka@tohoku.ac.jp.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Japan Science and Technology Agency, PRESTO, 2-1-1 Katahira, Aoba-ku, Sendai, 980-8577, Japan. yoshikazu.tanaka@tohoku.ac.jp.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>17H06955</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>18H02412</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>17H05424</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>19H02519</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>19H03511</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>19H03040</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>19H02831</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>19H00918</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>Bilateral Programs</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>19H02519</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>24000011</GrantID><Agency>MEXT | Japan Society for the Promotion of Science (JSPS)</Agency><Country></Country></Grant><Grant><GrantID>JPMJPR1517</GrantID><Agency>MEXT | JST | Precursory Research for Embryonic Science and Technology (PRESTO)</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>07</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Commun 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Chen</name></noRegion><name sortKey="Horitani, Masaki" sort="Horitani, Masaki" uniqKey="Horitani M" first="Masaki" last="Horitani">Masaki Horitani</name><name sortKey="Ishizaka, Masato" sort="Ishizaka, Masato" uniqKey="Ishizaka M" first="Masato" last="Ishizaka">Masato Ishizaka</name><name sortKey="Narai, Shun" sort="Narai, Shun" uniqKey="Narai S" first="Shun" last="Narai">Shun Narai</name><name sortKey="Shigi, Naoki" sort="Shigi, Naoki" uniqKey="Shigi N" first="Naoki" last="Shigi">Naoki Shigi</name><name sortKey="Tanaka, Yoshikazu" sort="Tanaka, Yoshikazu" uniqKey="Tanaka Y" first="Yoshikazu" last="Tanaka">Yoshikazu Tanaka</name><name sortKey="Tanaka, Yoshikazu" sort="Tanaka, Yoshikazu" uniqKey="Tanaka Y" first="Yoshikazu" last="Tanaka">Yoshikazu Tanaka</name><name sortKey="Tanaka, Yoshikazu" sort="Tanaka, Yoshikazu" uniqKey="Tanaka Y" first="Yoshikazu" last="Tanaka">Yoshikazu Tanaka</name><name sortKey="Yao, Min" sort="Yao, Min" uniqKey="Yao M" first="Min" last="Yao">Min 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