Rapid characterization of the activities of lignin-modifying enzymes based on nanostructure-initiator mass spectrometry (NIMS).
Identifieur interne : 000383 ( Main/Exploration ); précédent : 000382; suivant : 000384Rapid characterization of the activities of lignin-modifying enzymes based on nanostructure-initiator mass spectrometry (NIMS).
Auteurs : Kai Deng [États-Unis] ; Jijiao Zeng [États-Unis] ; Gang Cheng [République populaire de Chine] ; Jian Gao [États-Unis] ; Kenneth L. Sale [États-Unis] ; Blake A. Simmons [États-Unis] ; Anup K. Singh [États-Unis] ; Paul D. Adams [États-Unis] ; Trent R. Northen [États-Unis]Source :
- Biotechnology for biofuels [ 1754-6834 ] ; 2018.
Abstract
Background
Producing valuable fuels and chemicals from lignin is a key factor for making lignocellulosic biomass economically feasible; however, significant roadblocks exist due to our lack of detailed understanding of how lignin is enzymatically depolymerized and of the range of possible lignin fragments that can be produced. Development of suitable enzymatic assays for characterization of putative lignin active enzymes is an important step towards improving our understanding of the catalytic activities of relevant enzymes. Previously, we have successfully built an assay platform based on glycan substrates containing a charged perfluorinated tag and nanostructure-initiator mass spectrometry to study carbohydrate active enzymes, especially various glycosyl hydrolyses. Here, we extend this approach to develop a reliable and rapid assay to study lignin-modifying enzymes.
Results
Two β-aryl ether bond containing model lignin dimer substrates, designed to be suitable for studying the activities of lignin-modifying enzymes (LMEs) by nanostructure-initiator mass spectrometry (NIMS), were successful synthesized. Small-angle neutron scattering experiments showed that these substrates form micelles in solution. Two LMEs, laccase from the polypore mushroom
Conclusions
A new assay procedure has been developed for studying lignin-modifying enzymes by nanostructure-initiator mass spectrometry. Enzyme assays of a laccase and a MnP on phenolic and nonphenolic β-aryl ether substrates revealed different primary reaction pathways due to the availability of the phenoxy radical intermediates. Our assay provides a wealth of information on bond cleavage events not available using conventional colorimetric assays and can easily be carried out in microliter volumes and the quantitative analysis of product formation and kinetics is rapidly achieved by NIMS. This is the first time that NIMS technology was applied to study the activities of lignin-modifying enzymes. Unlike other previous works, our use of amphiphilic guaiacylglycerol β-
DOI: 10.1186/s13068-018-1261-2
PubMed: 30275906
PubMed Central: PMC6158898
Affiliations:
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Sale</name><affiliation wicri:level="2"><nlm:affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>1Joint BioEnergy Institute, Emeryville</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>2Sandia National Laboratories, Livermore, CA 94551 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>2Sandia National Laboratories, Livermore</wicri:cityArea></affiliation></author><author><name sortKey="Simmons, Blake A" sort="Simmons, Blake A" uniqKey="Simmons B" first="Blake A" last="Simmons">Blake A. Simmons</name><affiliation wicri:level="2"><nlm:affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>1Joint BioEnergy Institute, Emeryville</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>5Lawrence Berkeley National Laboratory, Berkeley</wicri:cityArea></affiliation></author><author><name sortKey="Singh, Anup K" sort="Singh, Anup K" uniqKey="Singh A" first="Anup K" last="Singh">Anup K. Singh</name><affiliation wicri:level="2"><nlm:affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>1Joint BioEnergy Institute, Emeryville</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>2Sandia National Laboratories, Livermore, CA 94551 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>2Sandia National Laboratories, Livermore</wicri:cityArea></affiliation></author><author><name sortKey="Adams, Paul D" sort="Adams, Paul D" uniqKey="Adams P" first="Paul D" last="Adams">Paul D. Adams</name><affiliation wicri:level="2"><nlm:affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>1Joint BioEnergy Institute, Emeryville</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>5Lawrence Berkeley National Laboratory, Berkeley</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>6University of California, Berkeley, CA 94720 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>6University of California, Berkeley</wicri:cityArea></affiliation></author><author><name sortKey="Northen, Trent R" sort="Northen, Trent R" uniqKey="Northen T" first="Trent R" last="Northen">Trent R. Northen</name><affiliation wicri:level="2"><nlm:affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>1Joint BioEnergy Institute, Emeryville</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>5Lawrence Berkeley National Laboratory, Berkeley</wicri:cityArea></affiliation></author></analytic><series><title level="j">Biotechnology for biofuels</title><idno type="ISSN">1754-6834</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>Background</b></p><p>Producing valuable fuels and chemicals from lignin is a key factor for making lignocellulosic biomass economically feasible; however, significant roadblocks exist due to our lack of detailed understanding of how lignin is enzymatically depolymerized and of the range of possible lignin fragments that can be produced. Development of suitable enzymatic assays for characterization of putative lignin active enzymes is an important step towards improving our understanding of the catalytic activities of relevant enzymes. Previously, we have successfully built an assay platform based on glycan substrates containing a charged perfluorinated tag and nanostructure-initiator mass spectrometry to study carbohydrate active enzymes, especially various glycosyl hydrolyses. Here, we extend this approach to develop a reliable and rapid assay to study lignin-modifying enzymes.</p></div><div type="abstract" xml:lang="en"><p><b>Results</b></p><p>Two β-aryl ether bond containing model lignin dimer substrates, designed to be suitable for studying the activities of lignin-modifying enzymes (LMEs) by nanostructure-initiator mass spectrometry (NIMS), were successful synthesized. Small-angle neutron scattering experiments showed that these substrates form micelles in solution. Two LMEs, laccase from the polypore mushroom </p></div><div type="abstract" xml:lang="en"><p><b>Conclusions</b></p><p>A new assay procedure has been developed for studying lignin-modifying enzymes by nanostructure-initiator mass spectrometry. Enzyme assays of a laccase and a MnP on phenolic and nonphenolic β-aryl ether substrates revealed different primary reaction pathways due to the availability of the phenoxy radical intermediates. Our assay provides a wealth of information on bond cleavage events not available using conventional colorimetric assays and can easily be carried out in microliter volumes and the quantitative analysis of product formation and kinetics is rapidly achieved by NIMS. This is the first time that NIMS technology was applied to study the activities of lignin-modifying enzymes. Unlike other previous works, our use of amphiphilic guaiacylglycerol β-</p></div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">30275906</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>01</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1754-6834</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2018</Year></PubDate></JournalIssue><Title>Biotechnology for biofuels</Title><ISOAbbreviation>Biotechnol Biofuels</ISOAbbreviation></Journal><ArticleTitle>Rapid characterization of the activities of lignin-modifying enzymes based on nanostructure-initiator mass spectrometry (NIMS).</ArticleTitle><Pagination><MedlinePgn>266</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s13068-018-1261-2</ELocationID><Abstract><AbstractText Label="Background" NlmCategory="UNASSIGNED">Producing valuable fuels and chemicals from lignin is a key factor for making lignocellulosic biomass economically feasible; however, significant roadblocks exist due to our lack of detailed understanding of how lignin is enzymatically depolymerized and of the range of possible lignin fragments that can be produced. Development of suitable enzymatic assays for characterization of putative lignin active enzymes is an important step towards improving our understanding of the catalytic activities of relevant enzymes. Previously, we have successfully built an assay platform based on glycan substrates containing a charged perfluorinated tag and nanostructure-initiator mass spectrometry to study carbohydrate active enzymes, especially various glycosyl hydrolyses. Here, we extend this approach to develop a reliable and rapid assay to study lignin-modifying enzymes.</AbstractText><AbstractText Label="Results" NlmCategory="UNASSIGNED">Two β-aryl ether bond containing model lignin dimer substrates, designed to be suitable for studying the activities of lignin-modifying enzymes (LMEs) by nanostructure-initiator mass spectrometry (NIMS), were successful synthesized. Small-angle neutron scattering experiments showed that these substrates form micelles in solution. Two LMEs, laccase from the polypore mushroom <i>Trametes versicolor</i>, and manganese peroxidase (MnP) from white rot fungus <i>Nematoloma frowardii</i>, were tested for catalytic activity against the two model substrates. We show that the reaction of laccase and MnP with phenolic substrate yields products that arise from the cleavage of the carbon-carbon single bond between the α-carbon and the adjacent aryl carbon, consistent with the mechanism for producing phenoxy radical as reaction intermediates. Reactions of the nonphenolic substrate with laccase, on the other hand, adopt a different pathway by producing an α-oxidation product; as well as the cleavage of the β-aryl ether bond. No cleavage of the carbon-carbon bond between the α-carbon and the aryl carbon was observed. To facilitate understanding of reaction kinetics, the reaction time course for laccase activity on the phenolic substrate (I) was generated by the simultaneous measurement of all products at different time points of the reaction. Withdrawal of only a small sample aliquot (0.2 μL at each time point) ensured minimum perturbation of the reaction. The time course can help us to understand the enzyme kinetics.</AbstractText><AbstractText Label="Conclusions" NlmCategory="UNASSIGNED">A new assay procedure has been developed for studying lignin-modifying enzymes by nanostructure-initiator mass spectrometry. Enzyme assays of a laccase and a MnP on phenolic and nonphenolic β-aryl ether substrates revealed different primary reaction pathways due to the availability of the phenoxy radical intermediates. Our assay provides a wealth of information on bond cleavage events not available using conventional colorimetric assays and can easily be carried out in microliter volumes and the quantitative analysis of product formation and kinetics is rapidly achieved by NIMS. This is the first time that NIMS technology was applied to study the activities of lignin-modifying enzymes. Unlike other previous works, our use of amphiphilic guaiacylglycerol β-<i>O</i>-4 substrate (I) enables the formation of micelles. This approach helps avoid the re-polymerization of the resulting monomeric product. As a result, our assay can clearly demonstrate the degradation pathways of phenolic guaiacylglycerol β-<i>O</i>-4 type of molecules with laccase and MnP.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Deng</LastName><ForeName>Kai</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0003-2937-8931</Identifier><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>2Sandia National Laboratories, Livermore, CA 94551 USA.</Affiliation><Identifier Source="ISNI">0000000403888279</Identifier><Identifier Source="GRID">grid.474523.3</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zeng</LastName><ForeName>Jijiao</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>2Sandia National Laboratories, Livermore, CA 94551 USA.</Affiliation><Identifier Source="ISNI">0000000403888279</Identifier><Identifier Source="GRID">grid.474523.3</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>3Sichuan University of Science & Engineering, Zigong, 643000 Sichuan China.</Affiliation><Identifier Source="ISNI">0000 0004 1798 1351</Identifier><Identifier Source="GRID">grid.412605.4</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Cheng</LastName><ForeName>Gang</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>4Beijing University of Chemical Technology, Beijing, 100080 China.</Affiliation><Identifier Source="ISNI">0000 0000 9931 8406</Identifier><Identifier Source="GRID">grid.48166.3d</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gao</LastName><ForeName>Jian</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</Affiliation><Identifier Source="ISNI">0000 0001 2231 4551</Identifier><Identifier Source="GRID">grid.184769.5</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sale</LastName><ForeName>Kenneth L</ForeName><Initials>KL</Initials><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>2Sandia National Laboratories, Livermore, CA 94551 USA.</Affiliation><Identifier Source="ISNI">0000000403888279</Identifier><Identifier Source="GRID">grid.474523.3</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Simmons</LastName><ForeName>Blake A</ForeName><Initials>BA</Initials><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</Affiliation><Identifier Source="ISNI">0000 0001 2231 4551</Identifier><Identifier Source="GRID">grid.184769.5</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Singh</LastName><ForeName>Anup K</ForeName><Initials>AK</Initials><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>2Sandia National Laboratories, Livermore, CA 94551 USA.</Affiliation><Identifier Source="ISNI">0000000403888279</Identifier><Identifier Source="GRID">grid.474523.3</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Adams</LastName><ForeName>Paul D</ForeName><Initials>PD</Initials><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</Affiliation><Identifier Source="ISNI">0000 0001 2231 4551</Identifier><Identifier Source="GRID">grid.184769.5</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>6University of California, Berkeley, CA 94720 USA.</Affiliation><Identifier Source="ISNI">0000 0001 2181 7878</Identifier><Identifier Source="GRID">grid.47840.3f</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Northen</LastName><ForeName>Trent R</ForeName><Initials>TR</Initials><AffiliationInfo><Affiliation>1Joint BioEnergy Institute, Emeryville, CA 94608 USA.</Affiliation><Identifier Source="ISNI">0000 0004 0407 8980</Identifier><Identifier Source="GRID">grid.451372.6</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>5Lawrence Berkeley National Laboratory, Berkeley, CA 94720 USA.</Affiliation><Identifier Source="ISNI">0000 0001 2231 4551</Identifier><Identifier Source="GRID">grid.184769.5</Identifier></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>09</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Biotechnol Biofuels</MedlineTA><NlmUniqueID>101316935</NlmUniqueID><ISSNLinking>1754-6834</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Enzyme assays</Keyword><Keyword MajorTopicYN="N">Lignin</Keyword><Keyword MajorTopicYN="N">Lignin-modifying enzymes</Keyword><Keyword MajorTopicYN="N">NIMS</Keyword><Keyword MajorTopicYN="N">β-Aryl ether</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>04</Month><Day>11</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>09</Month><Day>19</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>10</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>10</Month><Day>3</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>10</Month><Day>3</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">30275906</ArticleId><ArticleId IdType="doi">10.1186/s13068-018-1261-2</ArticleId><ArticleId 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IdType="pubmed">27311348</ArticleId></ArticleIdList></Reference></ReferenceList></PubmedData></pubmed><affiliations><list><country><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Californie</li></region><settlement><li>Pékin</li></settlement></list><tree><country name="États-Unis"><region name="Californie"><name sortKey="Deng, Kai" sort="Deng, Kai" uniqKey="Deng K" first="Kai" last="Deng">Kai Deng</name></region><name sortKey="Adams, Paul D" sort="Adams, Paul D" uniqKey="Adams P" first="Paul D" last="Adams">Paul D. Adams</name><name sortKey="Adams, Paul D" sort="Adams, Paul D" uniqKey="Adams P" first="Paul D" last="Adams">Paul D. Adams</name><name sortKey="Adams, Paul D" sort="Adams, Paul D" uniqKey="Adams P" first="Paul D" last="Adams">Paul D. Adams</name><name sortKey="Deng, Kai" sort="Deng, Kai" uniqKey="Deng K" first="Kai" last="Deng">Kai Deng</name><name sortKey="Gao, Jian" sort="Gao, Jian" uniqKey="Gao J" first="Jian" last="Gao">Jian Gao</name><name sortKey="Northen, Trent R" sort="Northen, Trent R" uniqKey="Northen T" first="Trent R" last="Northen">Trent R. Northen</name><name sortKey="Northen, Trent R" sort="Northen, Trent R" uniqKey="Northen T" first="Trent R" last="Northen">Trent R. Northen</name><name sortKey="Sale, Kenneth L" sort="Sale, Kenneth L" uniqKey="Sale K" first="Kenneth L" last="Sale">Kenneth L. Sale</name><name sortKey="Sale, Kenneth L" sort="Sale, Kenneth L" uniqKey="Sale K" first="Kenneth L" last="Sale">Kenneth L. Sale</name><name sortKey="Simmons, Blake A" sort="Simmons, Blake A" uniqKey="Simmons B" first="Blake A" last="Simmons">Blake A. Simmons</name><name sortKey="Simmons, Blake A" sort="Simmons, Blake A" uniqKey="Simmons B" first="Blake A" last="Simmons">Blake A. Simmons</name><name sortKey="Singh, Anup K" sort="Singh, Anup K" uniqKey="Singh A" first="Anup K" last="Singh">Anup K. Singh</name><name sortKey="Singh, Anup K" sort="Singh, Anup K" uniqKey="Singh A" first="Anup K" last="Singh">Anup K. Singh</name><name sortKey="Zeng, Jijiao" sort="Zeng, Jijiao" uniqKey="Zeng J" first="Jijiao" last="Zeng">Jijiao Zeng</name><name sortKey="Zeng, Jijiao" sort="Zeng, Jijiao" uniqKey="Zeng J" first="Jijiao" last="Zeng">Jijiao Zeng</name></country><country name="République populaire de Chine"><noRegion><name sortKey="Cheng, Gang" sort="Cheng, Gang" uniqKey="Cheng G" first="Gang" last="Cheng">Gang Cheng</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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