Internalization and accumulation of model lignin breakdown products in bacteria and fungi.
Identifieur interne : 000063 ( Main/Exploration ); précédent : 000062; suivant : 000064Internalization and accumulation of model lignin breakdown products in bacteria and fungi.
Auteurs : Meghan C. Barnhart-Dailey [États-Unis] ; Dongmei Ye [États-Unis] ; Dulce C. Hayes [États-Unis] ; Danae Maes [États-Unis] ; Casey T. Simoes [États-Unis] ; Leah Appelhans [États-Unis] ; Amanda Carroll-Portillo [États-Unis] ; Michael S. Kent [États-Unis] ; Jerilyn A. Timlin [États-Unis]Source :
- Biotechnology for biofuels [ 1754-6834 ] ; 2019.
Abstract
Background
Valorization of lignin has the potential to significantly improve the economics of lignocellulosic biorefineries. However, its complex structure makes conversion to useful products elusive. One promising approach is depolymerization of lignin and subsequent bioconversion of breakdown products into value-added compounds. Optimizing transport of these depolymerization products into one or more organism(s) for biological conversion is important to maximize carbon utilization and minimize toxicity. Current methods assess internalization of depolymerization products indirectly-for example, growth on, or toxicity of, a substrate. Furthermore, no method has been shown to provide visualization of depolymerization products in individual cells.
Results
We applied mass spectrometry to provide direct measurements of relative internalized concentrations of several lignin depolymerization compounds and single-cell microscopy methods to visualize cell-to-cell differences in internalized amounts of two lignin depolymerization compounds. We characterized internalization of 4-hydroxybenzoic acid, vanillic acid,
Conclusions
Mass spectrometry and single-cell microscopy methods were developed to establish a toolset for providing direct measurement and visualization of relative internal concentrations of mono- and di-aryl compounds in microbes. Utilizing these methods, we observed broad variation in intracellular concentration between organisms and within populations and this may have important consequences for the efficiency and productivity of an industrial process for bioconversion. Subsequent application of this toolset will be useful in identifying and characterizing specific transporters for lignin-derived mono- and di-aryl compounds.
DOI: 10.1186/s13068-019-1494-8
PubMed: 31303895
PubMed Central: PMC6607601
Affiliations:
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Barnhart-Dailey</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Ye, Dongmei" sort="Ye, Dongmei" uniqKey="Ye D" first="Dongmei" last="Ye">Dongmei Ye</name><affiliation wicri:level="2"><nlm:affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>3Department of Nanobiology, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Hayes, Dulce C" sort="Hayes, Dulce C" uniqKey="Hayes D" first="Dulce C" last="Hayes">Dulce C. Hayes</name><affiliation wicri:level="2"><nlm:affiliation>2Department of Nano and Bio-Sensors, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>2Department of Nano and Bio-Sensors, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Maes, Danae" sort="Maes, Danae" uniqKey="Maes D" first="Danae" last="Maes">Danae Maes</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Simoes, Casey T" sort="Simoes, Casey T" uniqKey="Simoes C" first="Casey T" last="Simoes">Casey T. Simoes</name><affiliation wicri:level="2"><nlm:affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>3Department of Nanobiology, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Appelhans, Leah" sort="Appelhans, Leah" uniqKey="Appelhans L" first="Leah" last="Appelhans">Leah Appelhans</name><affiliation wicri:level="2"><nlm:affiliation>4Department of Organic Materials Science, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>4Department of Organic Materials Science, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Carroll Portillo, Amanda" sort="Carroll Portillo, Amanda" uniqKey="Carroll Portillo A" first="Amanda" last="Carroll-Portillo">Amanda Carroll-Portillo</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>5Present Address: Section of Gastroenterology, New Mexico VA Health Care System, Albuquerque, NM 87108 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>5Present Address: Section of Gastroenterology, New Mexico VA Health Care System, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Kent, Michael S" sort="Kent, Michael S" uniqKey="Kent M" first="Michael S" last="Kent">Michael S. 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Timlin</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2019">2019</date><idno type="RBID">pubmed:31303895</idno><idno type="pmid">31303895</idno><idno type="doi">10.1186/s13068-019-1494-8</idno><idno type="pmc">PMC6607601</idno><idno type="wicri:Area/Main/Corpus">000058</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000058</idno><idno type="wicri:Area/Main/Curation">000058</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000058</idno><idno type="wicri:Area/Main/Exploration">000058</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Internalization and accumulation of model lignin breakdown products in bacteria and fungi.</title><author><name sortKey="Barnhart Dailey, Meghan C" sort="Barnhart Dailey, Meghan C" uniqKey="Barnhart Dailey M" first="Meghan C" last="Barnhart-Dailey">Meghan C. Barnhart-Dailey</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Ye, Dongmei" sort="Ye, Dongmei" uniqKey="Ye D" first="Dongmei" last="Ye">Dongmei Ye</name><affiliation wicri:level="2"><nlm:affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>3Department of Nanobiology, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Hayes, Dulce C" sort="Hayes, Dulce C" uniqKey="Hayes D" first="Dulce C" last="Hayes">Dulce C. Hayes</name><affiliation wicri:level="2"><nlm:affiliation>2Department of Nano and Bio-Sensors, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>2Department of Nano and Bio-Sensors, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Maes, Danae" sort="Maes, Danae" uniqKey="Maes D" first="Danae" last="Maes">Danae Maes</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Simoes, Casey T" sort="Simoes, Casey T" uniqKey="Simoes C" first="Casey T" last="Simoes">Casey T. Simoes</name><affiliation wicri:level="2"><nlm:affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>3Department of Nanobiology, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Appelhans, Leah" sort="Appelhans, Leah" uniqKey="Appelhans L" first="Leah" last="Appelhans">Leah Appelhans</name><affiliation wicri:level="2"><nlm:affiliation>4Department of Organic Materials Science, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>4Department of Organic Materials Science, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Carroll Portillo, Amanda" sort="Carroll Portillo, Amanda" uniqKey="Carroll Portillo A" first="Amanda" last="Carroll-Portillo">Amanda Carroll-Portillo</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:affiliation>5Present Address: Section of Gastroenterology, New Mexico VA Health Care System, Albuquerque, NM 87108 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>5Present Address: Section of Gastroenterology, New Mexico VA Health Care System, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Kent, Michael S" sort="Kent, Michael S" uniqKey="Kent M" first="Michael S" last="Kent">Michael S. Kent</name><affiliation wicri:level="2"><nlm:affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>3Department of Nanobiology, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author><author><name sortKey="Timlin, Jerilyn A" sort="Timlin, Jerilyn A" uniqKey="Timlin J" first="Jerilyn A" last="Timlin">Jerilyn A. Timlin</name><affiliation wicri:level="2"><nlm:affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><placeName><region type="state">Nouveau-Mexique</region></placeName><wicri:cityArea>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque</wicri:cityArea></affiliation></author></analytic><series><title level="j">Biotechnology for biofuels</title><idno type="ISSN">1754-6834</idno><imprint><date when="2019" type="published">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p><b>Background</b></p><p>Valorization of lignin has the potential to significantly improve the economics of lignocellulosic biorefineries. However, its complex structure makes conversion to useful products elusive. One promising approach is depolymerization of lignin and subsequent bioconversion of breakdown products into value-added compounds. Optimizing transport of these depolymerization products into one or more organism(s) for biological conversion is important to maximize carbon utilization and minimize toxicity. Current methods assess internalization of depolymerization products indirectly-for example, growth on, or toxicity of, a substrate. Furthermore, no method has been shown to provide visualization of depolymerization products in individual cells.</p></div><div type="abstract" xml:lang="en"><p><b>Results</b></p><p>We applied mass spectrometry to provide direct measurements of relative internalized concentrations of several lignin depolymerization compounds and single-cell microscopy methods to visualize cell-to-cell differences in internalized amounts of two lignin depolymerization compounds. We characterized internalization of 4-hydroxybenzoic acid, vanillic acid, </p></div><div type="abstract" xml:lang="en"><p><b>Conclusions</b></p><p>Mass spectrometry and single-cell microscopy methods were developed to establish a toolset for providing direct measurement and visualization of relative internal concentrations of mono- and di-aryl compounds in microbes. Utilizing these methods, we observed broad variation in intracellular concentration between organisms and within populations and this may have important consequences for the efficiency and productivity of an industrial process for bioconversion. Subsequent application of this toolset will be useful in identifying and characterizing specific transporters for lignin-derived mono- and di-aryl compounds.</p></div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">31303895</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>29</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1754-6834</ISSN><JournalIssue CitedMedium="Print"><Volume>12</Volume><PubDate><Year>2019</Year></PubDate></JournalIssue><Title>Biotechnology for biofuels</Title><ISOAbbreviation>Biotechnol Biofuels</ISOAbbreviation></Journal><ArticleTitle>Internalization and accumulation of model lignin breakdown products in bacteria and fungi.</ArticleTitle><Pagination><MedlinePgn>175</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s13068-019-1494-8</ELocationID><Abstract><AbstractText Label="Background" NlmCategory="UNASSIGNED">Valorization of lignin has the potential to significantly improve the economics of lignocellulosic biorefineries. However, its complex structure makes conversion to useful products elusive. One promising approach is depolymerization of lignin and subsequent bioconversion of breakdown products into value-added compounds. Optimizing transport of these depolymerization products into one or more organism(s) for biological conversion is important to maximize carbon utilization and minimize toxicity. Current methods assess internalization of depolymerization products indirectly-for example, growth on, or toxicity of, a substrate. Furthermore, no method has been shown to provide visualization of depolymerization products in individual cells.</AbstractText><AbstractText Label="Results" NlmCategory="UNASSIGNED">We applied mass spectrometry to provide direct measurements of relative internalized concentrations of several lignin depolymerization compounds and single-cell microscopy methods to visualize cell-to-cell differences in internalized amounts of two lignin depolymerization compounds. We characterized internalization of 4-hydroxybenzoic acid, vanillic acid, <i>p</i>-coumaric acid, syringic acid, and the model dimer guaiacylglycerol-beta-guaiacyl ether (GGE) in the lignolytic organisms <i>Phanerochaete chrysosporium</i> and <i>Enterobacter lignolyticus</i> and in the non-lignolytic but genetically tractable organisms <i>Saccharomyces cerevisiae</i> and <i>Escherichia coli</i>. The results show varying degrees of internalization in all organisms for all the tested compounds, including the model dimer, GGE. <i>Phanerochaete chrysosporium</i> internalizes all compounds in non-lignolytic and lignolytic conditions at comparable levels, indicating that the transporters for these compounds are not specific to the lignolytic secondary metabolic system. Single-cell microscopy shows that internalization of vanillic acid and 4-hydroxybenzoic acid analogs varies greatly among individual fungal and bacterial cells in a given population. Glucose starvation and chemical inhibition of ATP hydrolysis during internalization significantly reduced the internalized amount of vanillic acid in bacteria.</AbstractText><AbstractText Label="Conclusions" NlmCategory="UNASSIGNED">Mass spectrometry and single-cell microscopy methods were developed to establish a toolset for providing direct measurement and visualization of relative internal concentrations of mono- and di-aryl compounds in microbes. Utilizing these methods, we observed broad variation in intracellular concentration between organisms and within populations and this may have important consequences for the efficiency and productivity of an industrial process for bioconversion. Subsequent application of this toolset will be useful in identifying and characterizing specific transporters for lignin-derived mono- and di-aryl compounds.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Barnhart-Dailey</LastName><ForeName>Meghan C</ForeName><Initials>MC</Initials><AffiliationInfo><Affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ye</LastName><ForeName>Dongmei</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hayes</LastName><ForeName>Dulce C</ForeName><Initials>DC</Initials><AffiliationInfo><Affiliation>2Department of Nano and Bio-Sensors, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maes</LastName><ForeName>Danae</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Simoes</LastName><ForeName>Casey T</ForeName><Initials>CT</Initials><AffiliationInfo><Affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Appelhans</LastName><ForeName>Leah</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>4Department of Organic Materials Science, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Carroll-Portillo</LastName><ForeName>Amanda</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo><AffiliationInfo><Affiliation>5Present Address: Section of Gastroenterology, New Mexico VA Health Care System, Albuquerque, NM 87108 USA.</Affiliation><Identifier Source="ISNI">0000 0000 9831 362X</Identifier><Identifier Source="GRID">grid.413580.b</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kent</LastName><ForeName>Michael S</ForeName><Initials>MS</Initials><AffiliationInfo><Affiliation>3Department of Nanobiology, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Timlin</LastName><ForeName>Jerilyn A</ForeName><Initials>JA</Initials><Identifier Source="ORCID">0000-0003-2953-1721</Identifier><AffiliationInfo><Affiliation>1Department of Bioenergy and Defense Technologies, Sandia National Laboratories, Albuquerque, NM 87123 USA.</Affiliation><Identifier Source="ISNI">0000000121519272</Identifier><Identifier Source="GRID">grid.474520.0</Identifier></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2019</Year><Month>07</Month><Day>03</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">Bioconversion</Keyword><Keyword MajorTopicYN="N">Di-aryl</Keyword><Keyword MajorTopicYN="N">Lignin</Keyword><Keyword MajorTopicYN="N">Mass spectrometry</Keyword><Keyword MajorTopicYN="N">Mono-aryl</Keyword><Keyword MajorTopicYN="N">Single-cell analysis</Keyword><Keyword MajorTopicYN="N">Transport</Keyword></KeywordList><CoiStatement>Competing interestsThe authors declare that they have no competing interests.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>01</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2019</Year><Month>06</Month><Day>09</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2019</Year><Month>7</Month><Day>16</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2019</Year><Month>7</Month><Day>16</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2019</Year><Month>7</Month><Day>16</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">31303895</ArticleId><ArticleId IdType="doi">10.1186/s13068-019-1494-8</ArticleId><ArticleId IdType="pii">1494</ArticleId><ArticleId IdType="pmc">PMC6607601</ArticleId></ArticleIdList><ReferenceList><Reference><Citation>Microbiol Mol Biol Rev. 2001 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Barnhart-Dailey</name></region><name sortKey="Appelhans, Leah" sort="Appelhans, Leah" uniqKey="Appelhans L" first="Leah" last="Appelhans">Leah Appelhans</name><name sortKey="Carroll Portillo, Amanda" sort="Carroll Portillo, Amanda" uniqKey="Carroll Portillo A" first="Amanda" last="Carroll-Portillo">Amanda Carroll-Portillo</name><name sortKey="Carroll Portillo, Amanda" sort="Carroll Portillo, Amanda" uniqKey="Carroll Portillo A" first="Amanda" last="Carroll-Portillo">Amanda Carroll-Portillo</name><name sortKey="Hayes, Dulce C" sort="Hayes, Dulce C" uniqKey="Hayes D" first="Dulce C" last="Hayes">Dulce C. Hayes</name><name sortKey="Kent, Michael S" sort="Kent, Michael S" uniqKey="Kent M" first="Michael S" last="Kent">Michael S. Kent</name><name sortKey="Maes, Danae" sort="Maes, Danae" uniqKey="Maes D" first="Danae" last="Maes">Danae Maes</name><name sortKey="Simoes, Casey T" sort="Simoes, Casey T" uniqKey="Simoes C" first="Casey T" last="Simoes">Casey T. Simoes</name><name sortKey="Timlin, Jerilyn A" sort="Timlin, Jerilyn A" uniqKey="Timlin J" first="Jerilyn A" last="Timlin">Jerilyn A. Timlin</name><name sortKey="Ye, Dongmei" sort="Ye, Dongmei" uniqKey="Ye D" first="Dongmei" last="Ye">Dongmei Ye</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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