Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum
Clostridium thermocellum could potentially be used as a microbial biocatalyst to produce renewable fuels directly from lignocellulosic biomass due to its ability to rapidly solubilize plant cell walls. While the organism readily ferments sugars derived from cellulose, pentose sugars from xylan are n...
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| Veröffentlicht in: | Scientific reports 2017-02, Vol.7 (1), p.43355-43355, Article 43355 |
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| creator | Verbeke, Tobin J. Giannone, Richard J. Klingeman, Dawn M. Engle, Nancy L. Rydzak, Thomas Guss, Adam M. Tschaplinski, Timothy J. Brown, Steven D. Hettich, Robert L. Elkins, James G. |
| description | Clostridium thermocellum
could potentially be used as a microbial biocatalyst to produce renewable fuels directly from lignocellulosic biomass due to its ability to rapidly solubilize plant cell walls. While the organism readily ferments sugars derived from cellulose, pentose sugars from xylan are not metabolized. Here, we show that non-fermentable pentoses inhibit growth and end-product formation during fermentation of cellulose-derived sugars. Metabolomic experiments confirmed that xylose is transported intracellularly and reduced to the dead-end metabolite xylitol. Comparative RNA-seq analysis of xylose-inhibited cultures revealed several up-regulated genes potentially involved in pentose transport and metabolism, which were targeted for disruption. Deletion of the ATP-dependent transporter, CbpD partially alleviated xylose inhibition. A putative xylitol dehydrogenase, encoded by Clo1313_0076, was also deleted resulting in decreased total xylitol production and yield by 41% and 46%, respectively. Finally, xylose-induced inhibition corresponds with the up-regulation and biogenesis of a cyclical AgrD-type, pentapeptide. Medium supplementation with the mature cyclical pentapeptide also inhibits bacterial growth. Together, these findings provide new foundational insights needed for engineering improved pentose utilizing strains of
C. thermocellum
and reveal the first functional Agr-type cyclic peptide to be produced by a thermophilic member of the Firmicutes. |
| doi_str_mv | 10.1038/srep43355 |
| format | Article |
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could potentially be used as a microbial biocatalyst to produce renewable fuels directly from lignocellulosic biomass due to its ability to rapidly solubilize plant cell walls. While the organism readily ferments sugars derived from cellulose, pentose sugars from xylan are not metabolized. Here, we show that non-fermentable pentoses inhibit growth and end-product formation during fermentation of cellulose-derived sugars. Metabolomic experiments confirmed that xylose is transported intracellularly and reduced to the dead-end metabolite xylitol. Comparative RNA-seq analysis of xylose-inhibited cultures revealed several up-regulated genes potentially involved in pentose transport and metabolism, which were targeted for disruption. Deletion of the ATP-dependent transporter, CbpD partially alleviated xylose inhibition. A putative xylitol dehydrogenase, encoded by Clo1313_0076, was also deleted resulting in decreased total xylitol production and yield by 41% and 46%, respectively. Finally, xylose-induced inhibition corresponds with the up-regulation and biogenesis of a cyclical AgrD-type, pentapeptide. Medium supplementation with the mature cyclical pentapeptide also inhibits bacterial growth. Together, these findings provide new foundational insights needed for engineering improved pentose utilizing strains of
C. thermocellum
and reveal the first functional Agr-type cyclic peptide to be produced by a thermophilic member of the Firmicutes.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/srep43355</identifier><identifier>PMID: 28230109</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38 ; 38/91 ; 45/70 ; 60 APPLIED LIFE SCIENCES ; 631/326/252/318 ; 631/326/2522 ; 82/58 ; applied microbiology ; BASIC BIOLOGICAL SCIENCES ; Biomass ; Cell walls ; Cellulose ; Cellulose - metabolism ; Clonal deletion ; Clostridium thermocellum - drug effects ; Clostridium thermocellum - growth & development ; Clostridium thermocellum - metabolism ; Fermentation ; Gene deletion ; Gene Expression ; Gene Expression Profiling ; Gene Expression Regulation, Bacterial - drug effects ; Growth Inhibitors - metabolism ; Humanities and Social Sciences ; metabolic engineering ; Metabolic Networks and Pathways - drug effects ; Metabolism ; Metabolites ; Metabolomics ; multidisciplinary ; Oligopeptides - biosynthesis ; Pentoses - metabolism ; Peptides, Cyclic - biosynthesis ; Renewable fuels ; Ribonucleic acid ; RNA ; Science ; Sugar ; Supplements ; Xylan ; Xylitol ; Xylitol dehydrogenase ; Xylose</subject><ispartof>Scientific reports, 2017-02, Vol.7 (1), p.43355-43355, Article 43355</ispartof><rights>The Author(s) 2017</rights><rights>Copyright Nature Publishing Group Feb 2017</rights><rights>Copyright © 2017, The Author(s) 2017 The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c531t-3a36f33871074b47ace795ee5be5f6d5b747f81596025dc3029f7846c39e5f13</citedby><cites>FETCH-LOGICAL-c531t-3a36f33871074b47ace795ee5be5f6d5b747f81596025dc3029f7846c39e5f13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322536/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5322536/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,41096,42165,51551,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28230109$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1360049$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Verbeke, Tobin J.</creatorcontrib><creatorcontrib>Giannone, Richard J.</creatorcontrib><creatorcontrib>Klingeman, Dawn M.</creatorcontrib><creatorcontrib>Engle, Nancy L.</creatorcontrib><creatorcontrib>Rydzak, Thomas</creatorcontrib><creatorcontrib>Guss, Adam M.</creatorcontrib><creatorcontrib>Tschaplinski, Timothy J.</creatorcontrib><creatorcontrib>Brown, Steven D.</creatorcontrib><creatorcontrib>Hettich, Robert L.</creatorcontrib><creatorcontrib>Elkins, James G.</creatorcontrib><creatorcontrib>Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)</creatorcontrib><title>Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Clostridium thermocellum
could potentially be used as a microbial biocatalyst to produce renewable fuels directly from lignocellulosic biomass due to its ability to rapidly solubilize plant cell walls. While the organism readily ferments sugars derived from cellulose, pentose sugars from xylan are not metabolized. Here, we show that non-fermentable pentoses inhibit growth and end-product formation during fermentation of cellulose-derived sugars. Metabolomic experiments confirmed that xylose is transported intracellularly and reduced to the dead-end metabolite xylitol. Comparative RNA-seq analysis of xylose-inhibited cultures revealed several up-regulated genes potentially involved in pentose transport and metabolism, which were targeted for disruption. Deletion of the ATP-dependent transporter, CbpD partially alleviated xylose inhibition. A putative xylitol dehydrogenase, encoded by Clo1313_0076, was also deleted resulting in decreased total xylitol production and yield by 41% and 46%, respectively. Finally, xylose-induced inhibition corresponds with the up-regulation and biogenesis of a cyclical AgrD-type, pentapeptide. Medium supplementation with the mature cyclical pentapeptide also inhibits bacterial growth. Together, these findings provide new foundational insights needed for engineering improved pentose utilizing strains of
C. thermocellum
and reveal the first functional Agr-type cyclic peptide to be produced by a thermophilic member of the Firmicutes.</description><subject>38</subject><subject>38/91</subject><subject>45/70</subject><subject>60 APPLIED LIFE SCIENCES</subject><subject>631/326/252/318</subject><subject>631/326/2522</subject><subject>82/58</subject><subject>applied microbiology</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biomass</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Cellulose - metabolism</subject><subject>Clonal deletion</subject><subject>Clostridium thermocellum - drug effects</subject><subject>Clostridium thermocellum - growth & development</subject><subject>Clostridium thermocellum - metabolism</subject><subject>Fermentation</subject><subject>Gene deletion</subject><subject>Gene Expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Bacterial - drug effects</subject><subject>Growth Inhibitors - metabolism</subject><subject>Humanities and Social Sciences</subject><subject>metabolic engineering</subject><subject>Metabolic Networks and Pathways - drug effects</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metabolomics</subject><subject>multidisciplinary</subject><subject>Oligopeptides - biosynthesis</subject><subject>Pentoses - metabolism</subject><subject>Peptides, Cyclic - biosynthesis</subject><subject>Renewable fuels</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Science</subject><subject>Sugar</subject><subject>Supplements</subject><subject>Xylan</subject><subject>Xylitol</subject><subject>Xylitol dehydrogenase</subject><subject>Xylose</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNplkU1v1DAQhi0EolXpgT-ALLgAUsCO4zi-IFXLp1QJDr1bjjPZdZXYwXYQ---ZsmW1gC-2Zh6_8_ES8pSzN5yJ7m1OsDRCSPmAnNeskVUt6vrhyfuMXOZ8y_DIWjdcPyZndVcLxpk-J_tvEErMQPO6tSlTH3a-94XOUGwfJ59nasOAYZfAIgY_lwQ5-xhoHDFFr7bpfVX2C1C3d5N3dEFBu8BS_AD4j26mmEvyg19nWnaQ5uhgmtb5CXk02inD5f19QW4-frjZfK6uv376srm6rpwUvFTCinYUolOcqaZvlHWgtASQPcixHWSvGjV2XOqW1XJwgtV6VF3TOqER4OKCvDvILms_w-Cwu2QnsyQ_27Q30Xrzdyb4ndnGH0bi6qRoUeD5QQDH8CY7X8DtXAwBXDFctIw1GqGX91VS_L5CLmb2-W5OGyCu2XDsX0rJuUL0xT_obVxTwBUYrhlXvG1-U68OlEsxo8XjsWPOzJ3v5ug7ss9ORzySf1xG4PUByJgKW0gnJf9T-wWu47iC</recordid><startdate>20170223</startdate><enddate>20170223</enddate><creator>Verbeke, Tobin J.</creator><creator>Giannone, Richard J.</creator><creator>Klingeman, Dawn M.</creator><creator>Engle, Nancy L.</creator><creator>Rydzak, Thomas</creator><creator>Guss, Adam M.</creator><creator>Tschaplinski, Timothy J.</creator><creator>Brown, Steven D.</creator><creator>Hettich, Robert L.</creator><creator>Elkins, James G.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope></search><sort><creationdate>20170223</creationdate><title>Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum</title><author>Verbeke, Tobin J. ; Giannone, Richard J. ; Klingeman, Dawn M. ; Engle, Nancy L. ; Rydzak, Thomas ; Guss, Adam M. ; Tschaplinski, Timothy J. ; Brown, Steven D. ; Hettich, Robert L. ; Elkins, James G.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c531t-3a36f33871074b47ace795ee5be5f6d5b747f81596025dc3029f7846c39e5f13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>38</topic><topic>38/91</topic><topic>45/70</topic><topic>60 APPLIED LIFE SCIENCES</topic><topic>631/326/252/318</topic><topic>631/326/2522</topic><topic>82/58</topic><topic>applied microbiology</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Biomass</topic><topic>Cell walls</topic><topic>Cellulose</topic><topic>Cellulose - metabolism</topic><topic>Clonal deletion</topic><topic>Clostridium thermocellum - drug effects</topic><topic>Clostridium thermocellum - growth & development</topic><topic>Clostridium thermocellum - metabolism</topic><topic>Fermentation</topic><topic>Gene deletion</topic><topic>Gene Expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Bacterial - drug effects</topic><topic>Growth Inhibitors - metabolism</topic><topic>Humanities and Social Sciences</topic><topic>metabolic engineering</topic><topic>Metabolic Networks and Pathways - drug effects</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Metabolomics</topic><topic>multidisciplinary</topic><topic>Oligopeptides - biosynthesis</topic><topic>Pentoses - metabolism</topic><topic>Peptides, Cyclic - biosynthesis</topic><topic>Renewable fuels</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Science</topic><topic>Sugar</topic><topic>Supplements</topic><topic>Xylan</topic><topic>Xylitol</topic><topic>Xylitol dehydrogenase</topic><topic>Xylose</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Verbeke, Tobin J.</creatorcontrib><creatorcontrib>Giannone, Richard J.</creatorcontrib><creatorcontrib>Klingeman, Dawn M.</creatorcontrib><creatorcontrib>Engle, Nancy L.</creatorcontrib><creatorcontrib>Rydzak, Thomas</creatorcontrib><creatorcontrib>Guss, Adam M.</creatorcontrib><creatorcontrib>Tschaplinski, Timothy J.</creatorcontrib><creatorcontrib>Brown, Steven D.</creatorcontrib><creatorcontrib>Hettich, Robert L.</creatorcontrib><creatorcontrib>Elkins, James G.</creatorcontrib><creatorcontrib>Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). 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BioEnergy Science Center (BESC)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2017-02-23</date><risdate>2017</risdate><volume>7</volume><issue>1</issue><spage>43355</spage><epage>43355</epage><pages>43355-43355</pages><artnum>43355</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Clostridium thermocellum
could potentially be used as a microbial biocatalyst to produce renewable fuels directly from lignocellulosic biomass due to its ability to rapidly solubilize plant cell walls. While the organism readily ferments sugars derived from cellulose, pentose sugars from xylan are not metabolized. Here, we show that non-fermentable pentoses inhibit growth and end-product formation during fermentation of cellulose-derived sugars. Metabolomic experiments confirmed that xylose is transported intracellularly and reduced to the dead-end metabolite xylitol. Comparative RNA-seq analysis of xylose-inhibited cultures revealed several up-regulated genes potentially involved in pentose transport and metabolism, which were targeted for disruption. Deletion of the ATP-dependent transporter, CbpD partially alleviated xylose inhibition. A putative xylitol dehydrogenase, encoded by Clo1313_0076, was also deleted resulting in decreased total xylitol production and yield by 41% and 46%, respectively. Finally, xylose-induced inhibition corresponds with the up-regulation and biogenesis of a cyclical AgrD-type, pentapeptide. Medium supplementation with the mature cyclical pentapeptide also inhibits bacterial growth. Together, these findings provide new foundational insights needed for engineering improved pentose utilizing strains of
C. thermocellum
and reveal the first functional Agr-type cyclic peptide to be produced by a thermophilic member of the Firmicutes.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>28230109</pmid><doi>10.1038/srep43355</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 38 38/91 45/70 60 APPLIED LIFE SCIENCES 631/326/252/318 631/326/2522 82/58 applied microbiology BASIC BIOLOGICAL SCIENCES Biomass Cell walls Cellulose Cellulose - metabolism Clonal deletion Clostridium thermocellum - drug effects Clostridium thermocellum - growth & development Clostridium thermocellum - metabolism Fermentation Gene deletion Gene Expression Gene Expression Profiling Gene Expression Regulation, Bacterial - drug effects Growth Inhibitors - metabolism Humanities and Social Sciences metabolic engineering Metabolic Networks and Pathways - drug effects Metabolism Metabolites Metabolomics multidisciplinary Oligopeptides - biosynthesis Pentoses - metabolism Peptides, Cyclic - biosynthesis Renewable fuels Ribonucleic acid RNA Science Sugar Supplements Xylan Xylitol Xylitol dehydrogenase Xylose |
| title | Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum |
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