Alternate thermoregulation and functional binding of Escherichia coli type 1 fimbriae in environmental and animal isolates
Abstract Type 1 fimbriae (T1F) are well characterised cell surface organelles expressed by Escherichia coli and required for adherence to mannosylated host tissue. They satisfy molecular Koch's postulates as a virulence determinant and a host-adapted role has been reinforced by reports that T1F...
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creator | Marshall, Jacqueline Rossez, Yannick Mainda, Geoffrey Gally, David L. Daniell, Tim J. Holden, Nicola J. |
description | Abstract
Type 1 fimbriae (T1F) are well characterised cell surface organelles expressed by Escherichia coli and required for adherence to mannosylated host tissue. They satisfy molecular Koch's postulates as a virulence determinant and a host-adapted role has been reinforced by reports that T1F expression is repressed at submammalian temperatures. Analysis of a group of 136 environmental and animal E. coli isolates that express T1F at 37°C showed that 28% are also capable of expression at 20°C, in a phase variable manner. The heterogeneous proportions varied widely, and although growth temperature impacted the total proportion expressing T1F, there was no direct correlation between growth at 37°C and 20°C, indicative of differences in thermoregulation of the genetic switch (fimS) that controls phase variation. Specificities of the adhesin (FimH) also varied between the isolates: most bound to α-(1-3) mannan and yeast extracts as expected, but some recognised β-(1-4)-mannans and N-linked glycoproteins from plants, and T1F from two of the isolates mediated binding to plant roots. The results expand our view of a well-described adherence factor to show alternative expression profiles and adhesin specificities, which in turn may confer an advantage for certain isolates in alternative hosts and habitats.
Our work challenges the dogma that a well-characterised adherence factor is only expressed at mammalian-relevant temperatures and provides evidence for alternative functional targets for binding. |
doi_str_mv | 10.1093/femsle/fnw251 |
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Type 1 fimbriae (T1F) are well characterised cell surface organelles expressed by Escherichia coli and required for adherence to mannosylated host tissue. They satisfy molecular Koch's postulates as a virulence determinant and a host-adapted role has been reinforced by reports that T1F expression is repressed at submammalian temperatures. Analysis of a group of 136 environmental and animal E. coli isolates that express T1F at 37°C showed that 28% are also capable of expression at 20°C, in a phase variable manner. The heterogeneous proportions varied widely, and although growth temperature impacted the total proportion expressing T1F, there was no direct correlation between growth at 37°C and 20°C, indicative of differences in thermoregulation of the genetic switch (fimS) that controls phase variation. Specificities of the adhesin (FimH) also varied between the isolates: most bound to α-(1-3) mannan and yeast extracts as expected, but some recognised β-(1-4)-mannans and N-linked glycoproteins from plants, and T1F from two of the isolates mediated binding to plant roots. The results expand our view of a well-described adherence factor to show alternative expression profiles and adhesin specificities, which in turn may confer an advantage for certain isolates in alternative hosts and habitats.
Our work challenges the dogma that a well-characterised adherence factor is only expressed at mammalian-relevant temperatures and provides evidence for alternative functional targets for binding.</description><identifier>ISSN: 1574-6968</identifier><identifier>ISSN: 0378-1097</identifier><identifier>EISSN: 1574-6968</identifier><identifier>DOI: 10.1093/femsle/fnw251</identifier><identifier>PMID: 27810882</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Adhesins, Escherichia coli - genetics ; Adhesins, Escherichia coli - metabolism ; Adhesion ; Bacteria ; Bacterial Adhesion - physiology ; Binding ; Cell Extracts - chemistry ; Cell surface ; E coli ; Escherichia coli ; Escherichia coli - genetics ; Escherichia coli - isolation & purification ; Escherichia coli - metabolism ; Fimbriae Proteins - metabolism ; Fimbriae, Bacterial - metabolism ; Glycoproteins ; Glycoproteins - metabolism ; Mannan ; Mannans - metabolism ; Mannose - metabolism ; Microbiology ; Organelles ; Phase variations ; Pili ; Plant roots ; Plant Roots - metabolism ; Plant Roots - microbiology ; Protein Binding ; Temperature ; Thermoregulation ; Virulence ; Yeast ; Yeasts</subject><ispartof>FEMS microbiology letters, 2016-11, Vol.363 (22), p.fnw251</ispartof><rights>FEMS 2016. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2016</rights><rights>FEMS 2016. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><rights>Copyright Oxford University Press, UK Nov 2016</rights><rights>FEMS 2016. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c382t-608bc8c45fb8e0a7658d0780a7762193d1c7c5774b396ce865dd9243b2de1fa03</citedby><cites>FETCH-LOGICAL-c382t-608bc8c45fb8e0a7658d0780a7762193d1c7c5774b396ce865dd9243b2de1fa03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27810882$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Boden, Rich</contributor><creatorcontrib>Marshall, Jacqueline</creatorcontrib><creatorcontrib>Rossez, Yannick</creatorcontrib><creatorcontrib>Mainda, Geoffrey</creatorcontrib><creatorcontrib>Gally, David L.</creatorcontrib><creatorcontrib>Daniell, Tim J.</creatorcontrib><creatorcontrib>Holden, Nicola J.</creatorcontrib><title>Alternate thermoregulation and functional binding of Escherichia coli type 1 fimbriae in environmental and animal isolates</title><title>FEMS microbiology letters</title><addtitle>FEMS Microbiol Lett</addtitle><description>Abstract
Type 1 fimbriae (T1F) are well characterised cell surface organelles expressed by Escherichia coli and required for adherence to mannosylated host tissue. They satisfy molecular Koch's postulates as a virulence determinant and a host-adapted role has been reinforced by reports that T1F expression is repressed at submammalian temperatures. Analysis of a group of 136 environmental and animal E. coli isolates that express T1F at 37°C showed that 28% are also capable of expression at 20°C, in a phase variable manner. The heterogeneous proportions varied widely, and although growth temperature impacted the total proportion expressing T1F, there was no direct correlation between growth at 37°C and 20°C, indicative of differences in thermoregulation of the genetic switch (fimS) that controls phase variation. Specificities of the adhesin (FimH) also varied between the isolates: most bound to α-(1-3) mannan and yeast extracts as expected, but some recognised β-(1-4)-mannans and N-linked glycoproteins from plants, and T1F from two of the isolates mediated binding to plant roots. The results expand our view of a well-described adherence factor to show alternative expression profiles and adhesin specificities, which in turn may confer an advantage for certain isolates in alternative hosts and habitats.
Our work challenges the dogma that a well-characterised adherence factor is only expressed at mammalian-relevant temperatures and provides evidence for alternative functional targets for binding.</description><subject>Adhesins, Escherichia coli - genetics</subject><subject>Adhesins, Escherichia coli - metabolism</subject><subject>Adhesion</subject><subject>Bacteria</subject><subject>Bacterial Adhesion - physiology</subject><subject>Binding</subject><subject>Cell Extracts - chemistry</subject><subject>Cell surface</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - isolation & purification</subject><subject>Escherichia coli - metabolism</subject><subject>Fimbriae Proteins - metabolism</subject><subject>Fimbriae, Bacterial - metabolism</subject><subject>Glycoproteins</subject><subject>Glycoproteins - metabolism</subject><subject>Mannan</subject><subject>Mannans - metabolism</subject><subject>Mannose - metabolism</subject><subject>Microbiology</subject><subject>Organelles</subject><subject>Phase variations</subject><subject>Pili</subject><subject>Plant roots</subject><subject>Plant Roots - metabolism</subject><subject>Plant Roots - microbiology</subject><subject>Protein Binding</subject><subject>Temperature</subject><subject>Thermoregulation</subject><subject>Virulence</subject><subject>Yeast</subject><subject>Yeasts</subject><issn>1574-6968</issn><issn>0378-1097</issn><issn>1574-6968</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNqFkUtPxCAURonR-F66NSRu3FSBtkCXxvhKTNzouqH0MoOhMEKr0V8vk_EVF7riIzkccu-H0AElJ5Q05amBITk4Nf6F1XQNbdNaVAVvuFz_kbfQTkqPhJCKEb6JtpiQlEjJttHbmRshejUCHucQhxBhNjk12uCx8j02k9fLi3K4s763foaDwRdJZ9jquVVYB2fx-LoATLGxQxetAmw9Bv9sY_AD-DE_XrqUt0OONoX8AaQ9tGGUS7D_ce6ih8uL-_Pr4vbu6ub87LbQpWRjwYnstNRVbToJRAley54ImZPgjDZlT7XQtRBVVzZcg-R13zesKjvWAzWKlLvoeOVdxPA0QRrbwSYNzikPYUotlSUXZd3UPKNHv9DHMOXtuNRmIyWsYpz8SeUVN4KQhmWqWFE6hpQimHYR8_zxtaWkXVbXrqprV9Vl_vDDOnUD9F_0Z1ffc4Rp8Y_rHfoUpLo</recordid><startdate>201611</startdate><enddate>201611</enddate><creator>Marshall, Jacqueline</creator><creator>Rossez, Yannick</creator><creator>Mainda, Geoffrey</creator><creator>Gally, David L.</creator><creator>Daniell, Tim J.</creator><creator>Holden, Nicola J.</creator><general>Oxford University Press</general><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>7QL</scope><scope>7T7</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</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>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201611</creationdate><title>Alternate thermoregulation and functional binding of Escherichia coli type 1 fimbriae in environmental and animal isolates</title><author>Marshall, Jacqueline ; Rossez, Yannick ; Mainda, Geoffrey ; Gally, David L. ; Daniell, Tim J. ; Holden, Nicola J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c382t-608bc8c45fb8e0a7658d0780a7762193d1c7c5774b396ce865dd9243b2de1fa03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adhesins, Escherichia coli - 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Academic</collection><jtitle>FEMS microbiology letters</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Marshall, Jacqueline</au><au>Rossez, Yannick</au><au>Mainda, Geoffrey</au><au>Gally, David L.</au><au>Daniell, Tim J.</au><au>Holden, Nicola J.</au><au>Boden, Rich</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Alternate thermoregulation and functional binding of Escherichia coli type 1 fimbriae in environmental and animal isolates</atitle><jtitle>FEMS microbiology letters</jtitle><addtitle>FEMS Microbiol Lett</addtitle><date>2016-11</date><risdate>2016</risdate><volume>363</volume><issue>22</issue><spage>fnw251</spage><pages>fnw251-</pages><issn>1574-6968</issn><issn>0378-1097</issn><eissn>1574-6968</eissn><abstract>Abstract
Type 1 fimbriae (T1F) are well characterised cell surface organelles expressed by Escherichia coli and required for adherence to mannosylated host tissue. They satisfy molecular Koch's postulates as a virulence determinant and a host-adapted role has been reinforced by reports that T1F expression is repressed at submammalian temperatures. Analysis of a group of 136 environmental and animal E. coli isolates that express T1F at 37°C showed that 28% are also capable of expression at 20°C, in a phase variable manner. The heterogeneous proportions varied widely, and although growth temperature impacted the total proportion expressing T1F, there was no direct correlation between growth at 37°C and 20°C, indicative of differences in thermoregulation of the genetic switch (fimS) that controls phase variation. Specificities of the adhesin (FimH) also varied between the isolates: most bound to α-(1-3) mannan and yeast extracts as expected, but some recognised β-(1-4)-mannans and N-linked glycoproteins from plants, and T1F from two of the isolates mediated binding to plant roots. The results expand our view of a well-described adherence factor to show alternative expression profiles and adhesin specificities, which in turn may confer an advantage for certain isolates in alternative hosts and habitats.
Our work challenges the dogma that a well-characterised adherence factor is only expressed at mammalian-relevant temperatures and provides evidence for alternative functional targets for binding.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>27810882</pmid><doi>10.1093/femsle/fnw251</doi></addata></record> |
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subjects | Adhesins, Escherichia coli - genetics Adhesins, Escherichia coli - metabolism Adhesion Bacteria Bacterial Adhesion - physiology Binding Cell Extracts - chemistry Cell surface E coli Escherichia coli Escherichia coli - genetics Escherichia coli - isolation & purification Escherichia coli - metabolism Fimbriae Proteins - metabolism Fimbriae, Bacterial - metabolism Glycoproteins Glycoproteins - metabolism Mannan Mannans - metabolism Mannose - metabolism Microbiology Organelles Phase variations Pili Plant roots Plant Roots - metabolism Plant Roots - microbiology Protein Binding Temperature Thermoregulation Virulence Yeast Yeasts |
title | Alternate thermoregulation and functional binding of Escherichia coli type 1 fimbriae in environmental and animal isolates |
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