Improved biotin, thiamine, and lipoic acid biosynthesis by engineering the global regulator IscR.
Identifieur interne : 000104 ( Main/Exploration ); précédent : 000103; suivant : 000105Improved biotin, thiamine, and lipoic acid biosynthesis by engineering the global regulator IscR.
Auteurs : Anne P. Bali [Danemark] ; David Lennox-Hvenekilde [Danemark] ; Nils Myling-Petersen [Danemark] ; Josi Buerger [Danemark] ; Bo Salomonsen [Danemark] ; Luisa S. Gronenberg [Danemark] ; Morten O A. Sommer [Danemark] ; Hans J. Genee [Danemark]Source :
- Metabolic engineering [ 1096-7184 ] ; 2020.
Abstract
Biotin, thiamine, and lipoic acid are industrially important molecules naturally synthesized by microorganisms via biosynthetic pathways requiring iron-sulfur (FeS) clusters. Current production is exclusively by chemistry because pathway complexity hinders development of fermentation processes. For biotin, the main bottleneck is biotin synthase, BioB, a S-adenosyl methionine-dependent radical enzyme that converts dethiobiotin (DTB) to biotin. BioB overexpression is toxic, though the mechanism remains unclear. We identified single mutations in the global regulator IscR that substantially improve cellular tolerance to BioB overexpression, increasing Escherichia coli DTB-to-biotin biocatalysis by more than 2.2-fold. Based on proteomics and targeted overexpression of FeS-cluster biosynthesis genes, FeS-cluster depletion is the main reason for toxicity. We demonstrate that IscR mutations significantly affect cell viability and improve cell factories for de novo biosynthesis of thiamine by 1.3-fold and lipoic acid by 1.8-fold. We illuminate a novel engineering target for enhancing biosynthesis of complex FeS-cluster-dependent molecules, paving the way for industrial fermentation processes.
DOI: 10.1016/j.ymben.2020.03.005
PubMed: 32220614
Affiliations:
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Electronic address: hjg@biosyntia.com.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32220614</idno><idno type="pmid">32220614</idno><idno type="doi">10.1016/j.ymben.2020.03.005</idno><idno type="wicri:Area/Main/Corpus">000121</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000121</idno><idno type="wicri:Area/Main/Curation">000121</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000121</idno><idno type="wicri:Area/Main/Exploration">000121</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Improved biotin, thiamine, and lipoic acid biosynthesis by engineering the global regulator IscR.</title><author><name sortKey="Bali, Anne P" sort="Bali, Anne P" uniqKey="Bali A" first="Anne P" last="Bali">Anne P. Bali</name><affiliation wicri:level="1"><nlm:affiliation>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark; Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark; Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author><author><name sortKey="Lennox Hvenekilde, David" sort="Lennox Hvenekilde, David" uniqKey="Lennox Hvenekilde D" first="David" last="Lennox-Hvenekilde">David Lennox-Hvenekilde</name><affiliation wicri:level="1"><nlm:affiliation>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark; Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark; Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author><author><name sortKey="Myling Petersen, Nils" sort="Myling Petersen, Nils" uniqKey="Myling Petersen N" first="Nils" last="Myling-Petersen">Nils Myling-Petersen</name><affiliation wicri:level="1"><nlm:affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author><author><name sortKey="Buerger, Josi" sort="Buerger, Josi" uniqKey="Buerger J" first="Josi" last="Buerger">Josi Buerger</name><affiliation wicri:level="1"><nlm:affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author><author><name sortKey="Salomonsen, Bo" sort="Salomonsen, Bo" uniqKey="Salomonsen B" first="Bo" last="Salomonsen">Bo Salomonsen</name><affiliation wicri:level="1"><nlm:affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author><author><name sortKey="Gronenberg, Luisa S" sort="Gronenberg, Luisa S" uniqKey="Gronenberg L" first="Luisa S" last="Gronenberg">Luisa S. Gronenberg</name><affiliation wicri:level="1"><nlm:affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author><author><name sortKey="Sommer, Morten O A" sort="Sommer, Morten O A" uniqKey="Sommer M" first="Morten O A" last="Sommer">Morten O A. Sommer</name><affiliation wicri:level="1"><nlm:affiliation>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby</wicri:regionArea><wicri:noRegion>Kgs. Lyngby</wicri:noRegion></affiliation></author><author><name sortKey="Genee, Hans J" sort="Genee, Hans J" uniqKey="Genee H" first="Hans J" last="Genee">Hans J. Genee</name><affiliation wicri:level="1"><nlm:affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark. Electronic address: hjg@biosyntia.com.</nlm:affiliation><country xml:lang="fr">Danemark</country><wicri:regionArea>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100</wicri:regionArea><wicri:noRegion>2100</wicri:noRegion></affiliation></author></analytic><series><title level="j">Metabolic engineering</title><idno type="eISSN">1096-7184</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">Biotin, thiamine, and lipoic acid are industrially important molecules naturally synthesized by microorganisms via biosynthetic pathways requiring iron-sulfur (FeS) clusters. Current production is exclusively by chemistry because pathway complexity hinders development of fermentation processes. For biotin, the main bottleneck is biotin synthase, BioB, a S-adenosyl methionine-dependent radical enzyme that converts dethiobiotin (DTB) to biotin. BioB overexpression is toxic, though the mechanism remains unclear. We identified single mutations in the global regulator IscR that substantially improve cellular tolerance to BioB overexpression, increasing Escherichia coli DTB-to-biotin biocatalysis by more than 2.2-fold. Based on proteomics and targeted overexpression of FeS-cluster biosynthesis genes, FeS-cluster depletion is the main reason for toxicity. We demonstrate that IscR mutations significantly affect cell viability and improve cell factories for de novo biosynthesis of thiamine by 1.3-fold and lipoic acid by 1.8-fold. We illuminate a novel engineering target for enhancing biosynthesis of complex FeS-cluster-dependent molecules, paving the way for industrial fermentation processes.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32220614</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>30</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1096-7184</ISSN><JournalIssue CitedMedium="Internet"><Volume>60</Volume><PubDate><Year>2020</Year><Month>07</Month></PubDate></JournalIssue><Title>Metabolic engineering</Title><ISOAbbreviation>Metab Eng</ISOAbbreviation></Journal><ArticleTitle>Improved biotin, thiamine, and lipoic acid biosynthesis by engineering the global regulator IscR.</ArticleTitle><Pagination><MedlinePgn>97-109</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S1096-7176(20)30054-9</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.ymben.2020.03.005</ELocationID><Abstract><AbstractText>Biotin, thiamine, and lipoic acid are industrially important molecules naturally synthesized by microorganisms via biosynthetic pathways requiring iron-sulfur (FeS) clusters. Current production is exclusively by chemistry because pathway complexity hinders development of fermentation processes. For biotin, the main bottleneck is biotin synthase, BioB, a S-adenosyl methionine-dependent radical enzyme that converts dethiobiotin (DTB) to biotin. BioB overexpression is toxic, though the mechanism remains unclear. We identified single mutations in the global regulator IscR that substantially improve cellular tolerance to BioB overexpression, increasing Escherichia coli DTB-to-biotin biocatalysis by more than 2.2-fold. Based on proteomics and targeted overexpression of FeS-cluster biosynthesis genes, FeS-cluster depletion is the main reason for toxicity. We demonstrate that IscR mutations significantly affect cell viability and improve cell factories for de novo biosynthesis of thiamine by 1.3-fold and lipoic acid by 1.8-fold. We illuminate a novel engineering target for enhancing biosynthesis of complex FeS-cluster-dependent molecules, paving the way for industrial fermentation processes.</AbstractText><CopyrightInformation>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Bali</LastName><ForeName>Anne P</ForeName><Initials>AP</Initials><AffiliationInfo><Affiliation>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark; Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lennox-Hvenekilde</LastName><ForeName>David</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark; Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Myling-Petersen</LastName><ForeName>Nils</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Buerger</LastName><ForeName>Josi</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Salomonsen</LastName><ForeName>Bo</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gronenberg</LastName><ForeName>Luisa S</ForeName><Initials>LS</Initials><AffiliationInfo><Affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sommer</LastName><ForeName>Morten O A</ForeName><Initials>MOA</Initials><AffiliationInfo><Affiliation>The Novo Nordisk Foundation Center for Biosustainability, Technical University of Denmark, 2800, Kgs. Lyngby, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Genee</LastName><ForeName>Hans J</ForeName><Initials>HJ</Initials><AffiliationInfo><Affiliation>Biosyntia ApS, Fruebjergvej 3, Copenhagen E, 2100, Denmark. Electronic address: hjg@biosyntia.com.</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>2020</Year><Month>03</Month><Day>25</Day></ArticleDate></Article><MedlineJournalInfo><Country>Belgium</Country><MedlineTA>Metab Eng</MedlineTA><NlmUniqueID>9815657</NlmUniqueID><ISSNLinking>1096-7176</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Biotin</Keyword><Keyword MajorTopicYN="Y">Iron-sulfur cluster</Keyword><Keyword MajorTopicYN="Y">IscR</Keyword><Keyword MajorTopicYN="Y">Lipoic acid</Keyword><Keyword MajorTopicYN="Y">Thiamine</Keyword><Keyword MajorTopicYN="Y">Vitamins</Keyword></KeywordList><CoiStatement>Declaration of competing interest Biosyntia ApS has filed a patent application based on the results of this paper.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>12</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>02</Month><Day>24</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>03</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>3</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>3</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>3</Month><Day>30</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32220614</ArticleId><ArticleId IdType="pii">S1096-7176(20)30054-9</ArticleId><ArticleId IdType="doi">10.1016/j.ymben.2020.03.005</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Danemark</li></country></list><tree><country name="Danemark"><noRegion><name sortKey="Bali, Anne P" sort="Bali, Anne P" uniqKey="Bali A" first="Anne P" last="Bali">Anne P. Bali</name></noRegion><name sortKey="Buerger, Josi" sort="Buerger, Josi" uniqKey="Buerger J" first="Josi" last="Buerger">Josi Buerger</name><name sortKey="Genee, Hans J" sort="Genee, Hans J" uniqKey="Genee H" first="Hans J" last="Genee">Hans J. Genee</name><name sortKey="Gronenberg, Luisa S" sort="Gronenberg, Luisa S" uniqKey="Gronenberg L" first="Luisa S" last="Gronenberg">Luisa S. Gronenberg</name><name sortKey="Lennox Hvenekilde, David" sort="Lennox Hvenekilde, David" uniqKey="Lennox Hvenekilde D" first="David" last="Lennox-Hvenekilde">David Lennox-Hvenekilde</name><name sortKey="Myling Petersen, Nils" sort="Myling Petersen, Nils" uniqKey="Myling Petersen N" first="Nils" last="Myling-Petersen">Nils Myling-Petersen</name><name sortKey="Salomonsen, Bo" sort="Salomonsen, Bo" uniqKey="Salomonsen B" first="Bo" last="Salomonsen">Bo Salomonsen</name><name sortKey="Sommer, Morten O A" sort="Sommer, Morten O A" uniqKey="Sommer M" first="Morten O A" last="Sommer">Morten O A. 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