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Cellulose production, activated by cyclic di‐GMP through BcsA and BcsZ, is a virulence factor and an essential determinant of the three‐dimensional architectures of biofilms formed by Erwinia amylovora Ea1189
Summary Bacterial biofilms are multicellular aggregates encased in an extracellular matrix mainly composed of exopolysaccharides (EPSs), protein and nucleic acids, which determines the architecture of the biofilm. Erwinia amylovora Ea1189 forms a biofilm inside the xylem of its host, which results i...
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Published in: | Molecular plant pathology 2018-01, Vol.19 (1), p.90-103 |
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Bacterial biofilms are multicellular aggregates encased in an extracellular matrix mainly composed of exopolysaccharides (EPSs), protein and nucleic acids, which determines the architecture of the biofilm. Erwinia amylovora Ea1189 forms a biofilm inside the xylem of its host, which results in vessel plugging and water transport impairment. The production of the EPSs amylovoran and levan is critical for the formation of a mature biofilm. In addition, cyclic dimeric GMP (c‐di‐GMP) has been reported to positively regulate amylovoran biosynthesis and biofilm formation in E. amylovora Ea1189. In this study, we demonstrate that cellulose is synthesized by E. amylovora Ea1189 and is a major modulator of the three‐dimensional characteristics of biofilms formed by this bacterium, and also contributes to virulence during systemic host invasion. In addition, we demonstrate that the activation of cellulose biosynthesis in E. amylovora is a c‐di‐GMP‐dependent process, through allosteric binding to the cellulose catalytic subunit BcsA. We also report that the endoglucanase BcsZ is a key player in c‐di‐GMP activation of cellulose biosynthesis. Our results provide evidence of the complex composition of the extracellular matrix produced by E. amylovora and the implications of cellulose biosynthesis in shaping the architecture of the biofilm and in the expression of one of the main virulence phenotypes of this pathogen. |
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Bacterial biofilms are multicellular aggregates encased in an extracellular matrix mainly composed of exopolysaccharides (EPSs), protein and nucleic acids, which determines the architecture of the biofilm. Erwinia amylovora Ea1189 forms a biofilm inside the xylem of its host, which results in vessel plugging and water transport impairment. The production of the EPSs amylovoran and levan is critical for the formation of a mature biofilm. In addition, cyclic dimeric GMP (c‐di‐GMP) has been reported to positively regulate amylovoran biosynthesis and biofilm formation in E. amylovora Ea1189. In this study, we demonstrate that cellulose is synthesized by E. amylovora Ea1189 and is a major modulator of the three‐dimensional characteristics of biofilms formed by this bacterium, and also contributes to virulence during systemic host invasion. In addition, we demonstrate that the activation of cellulose biosynthesis in E. amylovora is a c‐di‐GMP‐dependent process, through allosteric binding to the cellulose catalytic subunit BcsA. We also report that the endoglucanase BcsZ is a key player in c‐di‐GMP activation of cellulose biosynthesis. Our results provide evidence of the complex composition of the extracellular matrix produced by E. amylovora and the implications of cellulose biosynthesis in shaping the architecture of the biofilm and in the expression of one of the main virulence phenotypes of this pathogen.</description><identifier>ISSN: 1464-6722</identifier><identifier>EISSN: 1364-3703</identifier><identifier>DOI: 10.1111/mpp.12501</identifier><identifier>PMID: 27753193</identifier><language>eng</language><publisher>Oxford: John Wiley & Sons, Inc</publisher><subject>Activation ; Allosteric properties ; Architecture ; Bacteria ; bacterial cellulose ; Biofilms ; Biosynthesis ; Casing (process) ; Catalysis ; Cellulose ; cyclic di‐GMP ; Endoglucanase ; Erwinia amylovora ; Exopolysaccharides ; Extracellular matrix ; Levan ; Nucleic acids ; Original ; PilZ domain ; Virulence ; Virulence factors ; Water transport ; Xylem</subject><ispartof>Molecular plant pathology, 2018-01, Vol.19 (1), p.90-103</ispartof><rights>2016 BSPP AND JOHN WILEY & SONS LTD</rights><rights>2018 BSPP AND JOHN WILEY & SONS LTD</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4431-b2148f5c6b359e8eb100ca62d73e16b124ca50591a2034a404aab63285b795313</citedby><cites>FETCH-LOGICAL-c4431-b2148f5c6b359e8eb100ca62d73e16b124ca50591a2034a404aab63285b795313</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/PMC6638026/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6638026/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,11562,27924,27925,46052,46476,53791,53793</link.rule.ids><linktorsrc>$$Uhttps://onlinelibrary.wiley.com/doi/abs/10.1111%2Fmpp.12501$$EView_record_in_Wiley-Blackwell$$FView_record_in_$$GWiley-Blackwell</linktorsrc></links><search><creatorcontrib>Castiblanco, Luisa F.</creatorcontrib><creatorcontrib>Sundin, George W.</creatorcontrib><title>Cellulose production, activated by cyclic di‐GMP through BcsA and BcsZ, is a virulence factor and an essential determinant of the three‐dimensional architectures of biofilms formed by Erwinia amylovora Ea1189</title><title>Molecular plant pathology</title><description>Summary
Bacterial biofilms are multicellular aggregates encased in an extracellular matrix mainly composed of exopolysaccharides (EPSs), protein and nucleic acids, which determines the architecture of the biofilm. Erwinia amylovora Ea1189 forms a biofilm inside the xylem of its host, which results in vessel plugging and water transport impairment. The production of the EPSs amylovoran and levan is critical for the formation of a mature biofilm. In addition, cyclic dimeric GMP (c‐di‐GMP) has been reported to positively regulate amylovoran biosynthesis and biofilm formation in E. amylovora Ea1189. In this study, we demonstrate that cellulose is synthesized by E. amylovora Ea1189 and is a major modulator of the three‐dimensional characteristics of biofilms formed by this bacterium, and also contributes to virulence during systemic host invasion. In addition, we demonstrate that the activation of cellulose biosynthesis in E. amylovora is a c‐di‐GMP‐dependent process, through allosteric binding to the cellulose catalytic subunit BcsA. We also report that the endoglucanase BcsZ is a key player in c‐di‐GMP activation of cellulose biosynthesis. Our results provide evidence of the complex composition of the extracellular matrix produced by E. amylovora and the implications of cellulose biosynthesis in shaping the architecture of the biofilm and in the expression of one of the main virulence phenotypes of this pathogen.</description><subject>Activation</subject><subject>Allosteric properties</subject><subject>Architecture</subject><subject>Bacteria</subject><subject>bacterial cellulose</subject><subject>Biofilms</subject><subject>Biosynthesis</subject><subject>Casing (process)</subject><subject>Catalysis</subject><subject>Cellulose</subject><subject>cyclic di‐GMP</subject><subject>Endoglucanase</subject><subject>Erwinia amylovora</subject><subject>Exopolysaccharides</subject><subject>Extracellular matrix</subject><subject>Levan</subject><subject>Nucleic acids</subject><subject>Original</subject><subject>PilZ domain</subject><subject>Virulence</subject><subject>Virulence factors</subject><subject>Water transport</subject><subject>Xylem</subject><issn>1464-6722</issn><issn>1364-3703</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1ks1u1DAQgCMEoj9w4A0scULqtv7L3wWprJaC1Io9wIWLNXEmXVeOHexkq9x4BB6uT8CT4G0qJA744pHm8-cZe7LsDaPnLK2LfhjOGc8pe5YdM1HIlSipeJ5imeKi5PwoO4nxjlJW1jx_mR3xsswFq8Vx9rBGayfrI5Ih-HbSo_HujEDa9zBiS5qZ6Flbo0lrfv_8dXWzJeMu-Ol2Rz7oeEnAtYfg-xkxkQDZmzBZdBpJlxw-PObBEYwR3WjAkhZHDL1x4EbiuyTDgxAxyVvTo4upgIRB0Dszoh6ngPEANsZ3xvaRdD70S2GbcG-cAQL9bP3eByAbYKyqX2UvOrARXz_tp9m3j5uv60-r6y9Xn9eX1ystpWCrhjNZdbkuGpHXWGHDKNVQ8LYUyIqGcakhp3nNgFMhQVIJ0BSCV3lT1un9xGn2fvEOU5NK0qnDAFYNwfQQZuXBqH8zzuzUrd-rohAV5UUSvH0SBP9jwjiqOz-F1H5UrC5l-qyypol6t1A6-BgDdn9vYFQdBkClAVCPA5DYi4W9Nxbn_4PqZrtdTvwBnCu2OA</recordid><startdate>201801</startdate><enddate>201801</enddate><creator>Castiblanco, Luisa F.</creator><creator>Sundin, George W.</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>5PM</scope></search><sort><creationdate>201801</creationdate><title>Cellulose production, activated by cyclic di‐GMP through BcsA and BcsZ, is a virulence factor and an essential determinant of the three‐dimensional architectures of biofilms formed by Erwinia amylovora Ea1189</title><author>Castiblanco, Luisa F. ; Sundin, George W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4431-b2148f5c6b359e8eb100ca62d73e16b124ca50591a2034a404aab63285b795313</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Activation</topic><topic>Allosteric properties</topic><topic>Architecture</topic><topic>Bacteria</topic><topic>bacterial cellulose</topic><topic>Biofilms</topic><topic>Biosynthesis</topic><topic>Casing (process)</topic><topic>Catalysis</topic><topic>Cellulose</topic><topic>cyclic di‐GMP</topic><topic>Endoglucanase</topic><topic>Erwinia amylovora</topic><topic>Exopolysaccharides</topic><topic>Extracellular matrix</topic><topic>Levan</topic><topic>Nucleic acids</topic><topic>Original</topic><topic>PilZ domain</topic><topic>Virulence</topic><topic>Virulence factors</topic><topic>Water transport</topic><topic>Xylem</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Castiblanco, Luisa F.</creatorcontrib><creatorcontrib>Sundin, George W.</creatorcontrib><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</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>PubMed Central (Full Participant titles)</collection><jtitle>Molecular plant pathology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Castiblanco, Luisa F.</au><au>Sundin, George W.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cellulose production, activated by cyclic di‐GMP through BcsA and BcsZ, is a virulence factor and an essential determinant of the three‐dimensional architectures of biofilms formed by Erwinia amylovora Ea1189</atitle><jtitle>Molecular plant pathology</jtitle><date>2018-01</date><risdate>2018</risdate><volume>19</volume><issue>1</issue><spage>90</spage><epage>103</epage><pages>90-103</pages><issn>1464-6722</issn><eissn>1364-3703</eissn><abstract>Summary
Bacterial biofilms are multicellular aggregates encased in an extracellular matrix mainly composed of exopolysaccharides (EPSs), protein and nucleic acids, which determines the architecture of the biofilm. Erwinia amylovora Ea1189 forms a biofilm inside the xylem of its host, which results in vessel plugging and water transport impairment. The production of the EPSs amylovoran and levan is critical for the formation of a mature biofilm. In addition, cyclic dimeric GMP (c‐di‐GMP) has been reported to positively regulate amylovoran biosynthesis and biofilm formation in E. amylovora Ea1189. In this study, we demonstrate that cellulose is synthesized by E. amylovora Ea1189 and is a major modulator of the three‐dimensional characteristics of biofilms formed by this bacterium, and also contributes to virulence during systemic host invasion. In addition, we demonstrate that the activation of cellulose biosynthesis in E. amylovora is a c‐di‐GMP‐dependent process, through allosteric binding to the cellulose catalytic subunit BcsA. We also report that the endoglucanase BcsZ is a key player in c‐di‐GMP activation of cellulose biosynthesis. Our results provide evidence of the complex composition of the extracellular matrix produced by E. amylovora and the implications of cellulose biosynthesis in shaping the architecture of the biofilm and in the expression of one of the main virulence phenotypes of this pathogen.</abstract><cop>Oxford</cop><pub>John Wiley & Sons, Inc</pub><pmid>27753193</pmid><doi>10.1111/mpp.12501</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Activation Allosteric properties Architecture Bacteria bacterial cellulose Biofilms Biosynthesis Casing (process) Catalysis Cellulose cyclic di‐GMP Endoglucanase Erwinia amylovora Exopolysaccharides Extracellular matrix Levan Nucleic acids Original PilZ domain Virulence Virulence factors Water transport Xylem |
title | Cellulose production, activated by cyclic di‐GMP through BcsA and BcsZ, is a virulence factor and an essential determinant of the three‐dimensional architectures of biofilms formed by Erwinia amylovora Ea1189 |
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