The Escherichia coli MarA protein regulates the ycgZ‐ymgABC operon to inhibit biofilm formation
Summary The Escherichia coli marRAB operon is a paradigm for chromosomally encoded antibiotic resistance. The operon exerts its effect via an encoded transcription factor called MarA that modulates efflux pump and porin expression. In this work, we show that MarA is also a regulator of biofilm forma...
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| Veröffentlicht in: | Molecular microbiology 2019-11, Vol.112 (5), p.1609-1625 |
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| creator | Kettles, Rachel A. Tschowri, Natalia Lyons, Kevin J. Sharma, Prateek Hengge, Regine Webber, Mark A. Grainger, David C. |
| description | Summary
The Escherichia coli marRAB operon is a paradigm for chromosomally encoded antibiotic resistance. The operon exerts its effect via an encoded transcription factor called MarA that modulates efflux pump and porin expression. In this work, we show that MarA is also a regulator of biofilm formation. Control is mediated by binding of MarA to the intergenic region upstream of the ycgZ‐ymgABC operon. The operon, known to influence the formation of curli fibres and colanic acid, is usually expressed during periods of starvation. Hence, the ycgZ‐ymgABC promoter is recognised by σ38 (RpoS)‐associated RNA polymerase (RNAP). Surprisingly, MarA does not influence σ38‐dependent transcription. Instead, MarA drives transcription by the housekeeping σ70‐associated RNAP. The effects of MarA on ycgZ‐ymgABC expression are coupled with biofilm formation by the rcsCDB phosphorelay system, with YcgZ, YmgA and YmgB forming a complex that directly interacts with the histidine kinase domain of RcsC.
Expression of the multiple antibiotic resistance activator (MarA) protein can give rise to clinically relevant drug resistance in Escherichia coli. Counterintuitively, we showed that MarA production inhibits the formation of biofilms. Inhibition is mediated by the activation of the ycgZ‐ymgABC operon. To activate these genes, MarA acts selectively thus enhancing transcription by RNAP associated with the σ70 but not with the σ38 factor. |
| doi_str_mv | 10.1111/mmi.14386 |
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The Escherichia coli marRAB operon is a paradigm for chromosomally encoded antibiotic resistance. The operon exerts its effect via an encoded transcription factor called MarA that modulates efflux pump and porin expression. In this work, we show that MarA is also a regulator of biofilm formation. Control is mediated by binding of MarA to the intergenic region upstream of the ycgZ‐ymgABC operon. The operon, known to influence the formation of curli fibres and colanic acid, is usually expressed during periods of starvation. Hence, the ycgZ‐ymgABC promoter is recognised by σ38 (RpoS)‐associated RNA polymerase (RNAP). Surprisingly, MarA does not influence σ38‐dependent transcription. Instead, MarA drives transcription by the housekeeping σ70‐associated RNAP. The effects of MarA on ycgZ‐ymgABC expression are coupled with biofilm formation by the rcsCDB phosphorelay system, with YcgZ, YmgA and YmgB forming a complex that directly interacts with the histidine kinase domain of RcsC.
Expression of the multiple antibiotic resistance activator (MarA) protein can give rise to clinically relevant drug resistance in Escherichia coli. Counterintuitively, we showed that MarA production inhibits the formation of biofilms. Inhibition is mediated by the activation of the ycgZ‐ymgABC operon. To activate these genes, MarA acts selectively thus enhancing transcription by RNAP associated with the σ70 but not with the σ38 factor.</description><identifier>ISSN: 0950-382X</identifier><identifier>EISSN: 1365-2958</identifier><identifier>DOI: 10.1111/mmi.14386</identifier><identifier>PMID: 31518447</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Antibiotic resistance ; Antibiotics ; Bacteria ; Bacterial Proteins - genetics ; Biofilms ; Biofilms - growth & development ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; DNA-directed RNA polymerase ; DNA-Directed RNA Polymerases - genetics ; Drug Resistance, Multiple, Bacterial - genetics ; E coli ; Efflux ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli - growth & development ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Fibers ; Histidine ; Histidine kinase ; Kinases ; MarA protein ; Multienzyme Complexes - genetics ; Multienzyme Complexes - metabolism ; Phosphoprotein Phosphatases - genetics ; Phosphoprotein Phosphatases - metabolism ; Porins - genetics ; Porins - metabolism ; Protein Kinases - genetics ; Protein Kinases - metabolism ; RNA polymerase ; Sigma Factor - genetics ; Transcription, Genetic - genetics</subject><ispartof>Molecular microbiology, 2019-11, Vol.112 (5), p.1609-1625</ispartof><rights>2019 The Authors. published by John Wiley & Sons Ltd</rights><rights>2019 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.</rights><rights>2019. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4436-d49d11cd072747257a5d306ed614f27b634be08289b29a0030b3926f6b2854053</citedby><cites>FETCH-LOGICAL-c4436-d49d11cd072747257a5d306ed614f27b634be08289b29a0030b3926f6b2854053</cites><orcidid>0000-0003-3375-5154</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmmi.14386$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmmi.14386$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31518447$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kettles, Rachel A.</creatorcontrib><creatorcontrib>Tschowri, Natalia</creatorcontrib><creatorcontrib>Lyons, Kevin J.</creatorcontrib><creatorcontrib>Sharma, Prateek</creatorcontrib><creatorcontrib>Hengge, Regine</creatorcontrib><creatorcontrib>Webber, Mark A.</creatorcontrib><creatorcontrib>Grainger, David C.</creatorcontrib><title>The Escherichia coli MarA protein regulates the ycgZ‐ymgABC operon to inhibit biofilm formation</title><title>Molecular microbiology</title><addtitle>Mol Microbiol</addtitle><description>Summary
The Escherichia coli marRAB operon is a paradigm for chromosomally encoded antibiotic resistance. The operon exerts its effect via an encoded transcription factor called MarA that modulates efflux pump and porin expression. In this work, we show that MarA is also a regulator of biofilm formation. Control is mediated by binding of MarA to the intergenic region upstream of the ycgZ‐ymgABC operon. The operon, known to influence the formation of curli fibres and colanic acid, is usually expressed during periods of starvation. Hence, the ycgZ‐ymgABC promoter is recognised by σ38 (RpoS)‐associated RNA polymerase (RNAP). Surprisingly, MarA does not influence σ38‐dependent transcription. Instead, MarA drives transcription by the housekeeping σ70‐associated RNAP. The effects of MarA on ycgZ‐ymgABC expression are coupled with biofilm formation by the rcsCDB phosphorelay system, with YcgZ, YmgA and YmgB forming a complex that directly interacts with the histidine kinase domain of RcsC.
Expression of the multiple antibiotic resistance activator (MarA) protein can give rise to clinically relevant drug resistance in Escherichia coli. Counterintuitively, we showed that MarA production inhibits the formation of biofilms. Inhibition is mediated by the activation of the ycgZ‐ymgABC operon. To activate these genes, MarA acts selectively thus enhancing transcription by RNAP associated with the σ70 but not with the σ38 factor.</description><subject>Antibiotic resistance</subject><subject>Antibiotics</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Biofilms</subject><subject>Biofilms - growth & development</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>DNA-directed RNA polymerase</subject><subject>DNA-Directed RNA Polymerases - genetics</subject><subject>Drug Resistance, Multiple, Bacterial - genetics</subject><subject>E coli</subject><subject>Efflux</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - growth & development</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Fibers</subject><subject>Histidine</subject><subject>Histidine kinase</subject><subject>Kinases</subject><subject>MarA protein</subject><subject>Multienzyme Complexes - genetics</subject><subject>Multienzyme Complexes - metabolism</subject><subject>Phosphoprotein Phosphatases - genetics</subject><subject>Phosphoprotein Phosphatases - metabolism</subject><subject>Porins - genetics</subject><subject>Porins - metabolism</subject><subject>Protein Kinases - genetics</subject><subject>Protein Kinases - metabolism</subject><subject>RNA polymerase</subject><subject>Sigma Factor - genetics</subject><subject>Transcription, Genetic - genetics</subject><issn>0950-382X</issn><issn>1365-2958</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kctO3DAUhi3UCobLgheoLHUDi4BvcewN0jCiBYkRG5AQG8txnIlREk_tBDQ7HqHP2Cepy1AESHhzFv706T_nB2AfoyOc3nHXuSPMqOAbYIIpzzMic_EFTJDMUUYFud0C2zHeI4Qp4nQTbFGcY8FYMQH6urHwLJrGBmcap6HxrYNzHaZwGfxgXQ-DXYytHmyEQ2JXZnH35-n3qltMT2fQL23wPRw8dH3jSjfA0vnatR2sfej04Hy_C77Wuo1272XugJsfZ9ez8-zy6ufFbHqZGcYozyomK4xNhQpSsILkhc6rlNZWHLOaFCWnrLRIECFLIjVCFJVUEl7zkoicoZzugJO1dzmWna2M7YegW7UMrtNhpbx26v1P7xq18A-Ky3QYwZLg4EUQ_K_RxkF1Lhrbtrq3foyKEIkETXGKhH7_gN77MfRpPUUoJlJygmSiDteUCT7GYOvXMBipf8WpVJx6Li6x396mfyX_N5WA4zXw6Fq7-tyk5vOLtfIvDqSimQ</recordid><startdate>201911</startdate><enddate>201911</enddate><creator>Kettles, Rachel A.</creator><creator>Tschowri, Natalia</creator><creator>Lyons, Kevin J.</creator><creator>Sharma, Prateek</creator><creator>Hengge, Regine</creator><creator>Webber, Mark A.</creator><creator>Grainger, David C.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3375-5154</orcidid></search><sort><creationdate>201911</creationdate><title>The Escherichia coli MarA protein regulates the ycgZ‐ymgABC operon to inhibit biofilm formation</title><author>Kettles, Rachel A. ; Tschowri, Natalia ; Lyons, Kevin J. ; Sharma, Prateek ; Hengge, Regine ; Webber, Mark A. ; Grainger, David C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4436-d49d11cd072747257a5d306ed614f27b634be08289b29a0030b3926f6b2854053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Antibiotic resistance</topic><topic>Antibiotics</topic><topic>Bacteria</topic><topic>Bacterial Proteins - genetics</topic><topic>Biofilms</topic><topic>Biofilms - growth & development</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>DNA-directed RNA polymerase</topic><topic>DNA-Directed RNA Polymerases - genetics</topic><topic>Drug Resistance, Multiple, Bacterial - genetics</topic><topic>E coli</topic><topic>Efflux</topic><topic>Escherichia coli</topic><topic>Escherichia coli - genetics</topic><topic>Escherichia coli - growth & development</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Fibers</topic><topic>Histidine</topic><topic>Histidine kinase</topic><topic>Kinases</topic><topic>MarA protein</topic><topic>Multienzyme Complexes - genetics</topic><topic>Multienzyme Complexes - metabolism</topic><topic>Phosphoprotein Phosphatases - genetics</topic><topic>Phosphoprotein Phosphatases - metabolism</topic><topic>Porins - genetics</topic><topic>Porins - metabolism</topic><topic>Protein Kinases - genetics</topic><topic>Protein Kinases - metabolism</topic><topic>RNA polymerase</topic><topic>Sigma Factor - genetics</topic><topic>Transcription, Genetic - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kettles, Rachel A.</creatorcontrib><creatorcontrib>Tschowri, Natalia</creatorcontrib><creatorcontrib>Lyons, Kevin J.</creatorcontrib><creatorcontrib>Sharma, Prateek</creatorcontrib><creatorcontrib>Hengge, Regine</creatorcontrib><creatorcontrib>Webber, Mark A.</creatorcontrib><creatorcontrib>Grainger, David C.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kettles, Rachel A.</au><au>Tschowri, Natalia</au><au>Lyons, Kevin J.</au><au>Sharma, Prateek</au><au>Hengge, Regine</au><au>Webber, Mark A.</au><au>Grainger, David C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Escherichia coli MarA protein regulates the ycgZ‐ymgABC operon to inhibit biofilm formation</atitle><jtitle>Molecular microbiology</jtitle><addtitle>Mol Microbiol</addtitle><date>2019-11</date><risdate>2019</risdate><volume>112</volume><issue>5</issue><spage>1609</spage><epage>1625</epage><pages>1609-1625</pages><issn>0950-382X</issn><eissn>1365-2958</eissn><abstract>Summary
The Escherichia coli marRAB operon is a paradigm for chromosomally encoded antibiotic resistance. The operon exerts its effect via an encoded transcription factor called MarA that modulates efflux pump and porin expression. In this work, we show that MarA is also a regulator of biofilm formation. Control is mediated by binding of MarA to the intergenic region upstream of the ycgZ‐ymgABC operon. The operon, known to influence the formation of curli fibres and colanic acid, is usually expressed during periods of starvation. Hence, the ycgZ‐ymgABC promoter is recognised by σ38 (RpoS)‐associated RNA polymerase (RNAP). Surprisingly, MarA does not influence σ38‐dependent transcription. Instead, MarA drives transcription by the housekeeping σ70‐associated RNAP. The effects of MarA on ycgZ‐ymgABC expression are coupled with biofilm formation by the rcsCDB phosphorelay system, with YcgZ, YmgA and YmgB forming a complex that directly interacts with the histidine kinase domain of RcsC.
Expression of the multiple antibiotic resistance activator (MarA) protein can give rise to clinically relevant drug resistance in Escherichia coli. Counterintuitively, we showed that MarA production inhibits the formation of biofilms. Inhibition is mediated by the activation of the ycgZ‐ymgABC operon. To activate these genes, MarA acts selectively thus enhancing transcription by RNAP associated with the σ70 but not with the σ38 factor.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31518447</pmid><doi>10.1111/mmi.14386</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0003-3375-5154</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Antibiotic resistance Antibiotics Bacteria Bacterial Proteins - genetics Biofilms Biofilms - growth & development DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism DNA-directed RNA polymerase DNA-Directed RNA Polymerases - genetics Drug Resistance, Multiple, Bacterial - genetics E coli Efflux Escherichia coli Escherichia coli - genetics Escherichia coli - growth & development Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Fibers Histidine Histidine kinase Kinases MarA protein Multienzyme Complexes - genetics Multienzyme Complexes - metabolism Phosphoprotein Phosphatases - genetics Phosphoprotein Phosphatases - metabolism Porins - genetics Porins - metabolism Protein Kinases - genetics Protein Kinases - metabolism RNA polymerase Sigma Factor - genetics Transcription, Genetic - genetics |
| title | The Escherichia coli MarA protein regulates the ycgZ‐ymgABC operon to inhibit biofilm formation |
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