Relationship between heat-labile enterotoxin secretion capacity and virulence in wild type porcine-origin enterotoxigenic Escherichia coli strains
Heat-labile enterotoxin (LT) is an important virulence factor secreted by some strains of enterotoxigenic Escherichia coli (ETEC). The prototypic human-origin strain H10407 secretes LT via a type II secretion system (T2SS). We sought to determine the relationship between the capacity to secrete LT a...
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| creator | Wijemanne, Prageeth Xing, Jun Berberov, Emil M Marx, David B Francis, David H Moxley, Rodney A |
| description | Heat-labile enterotoxin (LT) is an important virulence factor secreted by some strains of enterotoxigenic Escherichia coli (ETEC). The prototypic human-origin strain H10407 secretes LT via a type II secretion system (T2SS). We sought to determine the relationship between the capacity to secrete LT and virulence in porcine-origin wild type (WT) ETEC strains. Sixteen WT ETEC strains isolated from cases of severe diarrheal disease were analyzed by GM1ganglioside enzyme-linked immunosorbent assay to measure LT concentrations in culture supernatants. All strains had detectable LT in supernatants by 2 h of culture and 1 strain, which was particularly virulent in gnotobiotic piglets (3030-2), had the highest LT secretion level all porcine-origin WT strains tested (P |
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The prototypic human-origin strain H10407 secretes LT via a type II secretion system (T2SS). We sought to determine the relationship between the capacity to secrete LT and virulence in porcine-origin wild type (WT) ETEC strains. Sixteen WT ETEC strains isolated from cases of severe diarrheal disease were analyzed by GM1ganglioside enzyme-linked immunosorbent assay to measure LT concentrations in culture supernatants. All strains had detectable LT in supernatants by 2 h of culture and 1 strain, which was particularly virulent in gnotobiotic piglets (3030-2), had the highest LT secretion level all porcine-origin WT strains tested (P<0.05). The level of LT secretion (concentration in supernatants at 6-h culture) explained 92% of the variation in time-to-a-moribund-condition (R2 = 0.92, P<0.0001) in gnotobiotic piglets inoculated with either strain 3030-2, or an ETEC strain of lesser virulence (2534-86), or a non-enterotoxigenic WT strain (G58-1). All 16 porcine ETEC strains were positive by PCR analysis for the T2SS genes, gspD and gspK, and bioinformatic analysis of 4 porcine-origin strains for which complete genomic sequences were available revealed a T2SS with a high degree of homology to that of H10407. Maximum Likelihood phylogenetic trees constructed using T2SS genes gspC, gspD, gspE and homologs showed that strains 2534-86 and 3030-2 clustered together in the same clade with other porcine-origin ETEC strains in the database, UMNK88 and UMN18. Protein modeling of the ATPase gene (gspE) further revealed a direct relationship between the predicted ATP-binding capacities and LT secretion levels as follows: H10407, -8.8 kcal/mol and 199 ng/ml; 3030-2, -8.6 kcal/mol and 133 ng/ml; and 2534-86, -8.5 kcal/mol and 80 ng/ml. This study demonstrated a direct relationship between predicted ATP-binding capacity of GspE and LT secretion, and between the latter and virulence.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0117663</identifier><identifier>PMID: 25768732</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adenosine triphosphatase ; Analysis ; Animals ; ATP ; ATPases ; Bacteria ; Bacterial Secretion Systems - genetics ; Bacterial Secretion Systems - metabolism ; Bacterial Toxins - genetics ; Binding ; Culture ; Developing countries ; Diarrhea ; Diarrhea - microbiology ; Diarrhea - veterinary ; E coli ; Enterotoxigenic Escherichia coli - genetics ; Enterotoxigenic Escherichia coli - pathogenicity ; Enterotoxigenic Escherichia coli - physiology ; Enterotoxins - genetics ; Enterotoxins - metabolism ; Enzyme-linked immunosorbent assay ; Escherichia coli ; Escherichia coli Infections - microbiology ; Escherichia coli Infections - veterinary ; Escherichia coli Proteins - genetics ; Escherichia coli Proteins - metabolism ; Experiments ; Genes ; Gnotobiotic ; Heat-labile enterotoxin ; Hogs ; Homology ; Humans ; LDCs ; Mitochondrial DNA ; Pathogens ; Phylogeny ; Proteins ; Swine ; Swine Diseases - microbiology ; Veterinary colleges ; Veterinary medicine ; Vibrio cholerae ; Virulence ; Virulence (Microbiology) ; Virulence factors</subject><ispartof>PloS one, 2015-03, Vol.10 (3), p.e0117663-e0117663</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Wijemanne et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Wijemanne et al 2015 Wijemanne et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-412e7f2a8e1a2550fee194030e0d55d73ceaf5865f5885bb890e0088dbc0a0323</citedby><cites>FETCH-LOGICAL-c692t-412e7f2a8e1a2550fee194030e0d55d73ceaf5865f5885bb890e0088dbc0a0323</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/PMC4358887/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4358887/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25768732$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Rajashekara, Gireesh</contributor><creatorcontrib>Wijemanne, Prageeth</creatorcontrib><creatorcontrib>Xing, Jun</creatorcontrib><creatorcontrib>Berberov, Emil M</creatorcontrib><creatorcontrib>Marx, David B</creatorcontrib><creatorcontrib>Francis, David H</creatorcontrib><creatorcontrib>Moxley, Rodney A</creatorcontrib><title>Relationship between heat-labile enterotoxin secretion capacity and virulence in wild type porcine-origin enterotoxigenic Escherichia coli strains</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Heat-labile enterotoxin (LT) is an important virulence factor secreted by some strains of enterotoxigenic Escherichia coli (ETEC). The prototypic human-origin strain H10407 secretes LT via a type II secretion system (T2SS). We sought to determine the relationship between the capacity to secrete LT and virulence in porcine-origin wild type (WT) ETEC strains. Sixteen WT ETEC strains isolated from cases of severe diarrheal disease were analyzed by GM1ganglioside enzyme-linked immunosorbent assay to measure LT concentrations in culture supernatants. All strains had detectable LT in supernatants by 2 h of culture and 1 strain, which was particularly virulent in gnotobiotic piglets (3030-2), had the highest LT secretion level all porcine-origin WT strains tested (P<0.05). The level of LT secretion (concentration in supernatants at 6-h culture) explained 92% of the variation in time-to-a-moribund-condition (R2 = 0.92, P<0.0001) in gnotobiotic piglets inoculated with either strain 3030-2, or an ETEC strain of lesser virulence (2534-86), or a non-enterotoxigenic WT strain (G58-1). All 16 porcine ETEC strains were positive by PCR analysis for the T2SS genes, gspD and gspK, and bioinformatic analysis of 4 porcine-origin strains for which complete genomic sequences were available revealed a T2SS with a high degree of homology to that of H10407. Maximum Likelihood phylogenetic trees constructed using T2SS genes gspC, gspD, gspE and homologs showed that strains 2534-86 and 3030-2 clustered together in the same clade with other porcine-origin ETEC strains in the database, UMNK88 and UMN18. Protein modeling of the ATPase gene (gspE) further revealed a direct relationship between the predicted ATP-binding capacities and LT secretion levels as follows: H10407, -8.8 kcal/mol and 199 ng/ml; 3030-2, -8.6 kcal/mol and 133 ng/ml; and 2534-86, -8.5 kcal/mol and 80 ng/ml. This study demonstrated a direct relationship between predicted ATP-binding capacity of GspE and LT secretion, and between the latter and virulence.</description><subject>Adenosine triphosphatase</subject><subject>Analysis</subject><subject>Animals</subject><subject>ATP</subject><subject>ATPases</subject><subject>Bacteria</subject><subject>Bacterial Secretion Systems - genetics</subject><subject>Bacterial Secretion Systems - metabolism</subject><subject>Bacterial Toxins - genetics</subject><subject>Binding</subject><subject>Culture</subject><subject>Developing countries</subject><subject>Diarrhea</subject><subject>Diarrhea - microbiology</subject><subject>Diarrhea - veterinary</subject><subject>E coli</subject><subject>Enterotoxigenic Escherichia coli - genetics</subject><subject>Enterotoxigenic Escherichia coli - pathogenicity</subject><subject>Enterotoxigenic Escherichia coli - physiology</subject><subject>Enterotoxins - genetics</subject><subject>Enterotoxins - metabolism</subject><subject>Enzyme-linked immunosorbent assay</subject><subject>Escherichia coli</subject><subject>Escherichia coli Infections - microbiology</subject><subject>Escherichia coli Infections - veterinary</subject><subject>Escherichia coli Proteins - genetics</subject><subject>Escherichia coli Proteins - metabolism</subject><subject>Experiments</subject><subject>Genes</subject><subject>Gnotobiotic</subject><subject>Heat-labile enterotoxin</subject><subject>Hogs</subject><subject>Homology</subject><subject>Humans</subject><subject>LDCs</subject><subject>Mitochondrial DNA</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>Proteins</subject><subject>Swine</subject><subject>Swine Diseases - microbiology</subject><subject>Veterinary colleges</subject><subject>Veterinary medicine</subject><subject>Vibrio cholerae</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence factors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</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><sourceid>DOA</sourceid><recordid>eNqNk9tqGzEQhpfS0qRu36C0gkJpL-zquIebQghpawgE0sOtkLWztowsbSRtEr9Gn7iy46R2yUVZ0ArNN7-kXzNF8ZrgCWEV-bT0Q3DKTnrvYIIJqcqSPSmOScPouKSYPd2bHxUvYlxiLFhdls-LIyqqsq4YPS5-X4JVyXgXF6ZHM0g3AA4tQKWxVTNjAYFLEHzyt8ahCDrAhkZa9UqbtEbKtejahMGC04Ayc2Nsi9K6B9T7oI2DsQ9mngN_hebgjEZnUS8gGL0wCmlvDYopKOPiy-JZp2yEV7v_qPj55ezH6bfx-cXX6enJ-ViXDU1jTihUHVU1EEWFwB0AaThmGHArRFsxDaoTdSnyUIvZrG5yBNd1O9NYYUbZqHh7p9tbH-XOzihJ9pHxsm5EJqZ3ROvVUvbBrFRYS6-M3C74MJcqJKMtyK7TSuOKd03d8A7zRuuON4TTigvaEp61Pu92G2YraHV2Iyh7IHoYcWYh5_5acpbPnx9rVHzYCQR_NUBMcmWiBmuVAz9sz80pqQgjGX33D_r47XbUXOULGNf5vK_eiMoTTimmpRBNpiaPUPlrYWV0rr0uF8lhwseDhMwkuE1zNcQop98v_5-9-HXIvt9jc4XatIjeDtviPQT5HaiDjzFA92AywXLTOvduyE3ryF3r5LQ3-w_0kHTfK-wP8tkXAw</recordid><startdate>20150313</startdate><enddate>20150313</enddate><creator>Wijemanne, Prageeth</creator><creator>Xing, Jun</creator><creator>Berberov, Emil M</creator><creator>Marx, David B</creator><creator>Francis, David H</creator><creator>Moxley, Rodney A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</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>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20150313</creationdate><title>Relationship between heat-labile enterotoxin secretion capacity and virulence in wild type porcine-origin enterotoxigenic Escherichia coli strains</title><author>Wijemanne, Prageeth ; Xing, Jun ; Berberov, Emil M ; Marx, David B ; Francis, David H ; Moxley, Rodney A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-412e7f2a8e1a2550fee194030e0d55d73ceaf5865f5885bb890e0088dbc0a0323</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adenosine triphosphatase</topic><topic>Analysis</topic><topic>Animals</topic><topic>ATP</topic><topic>ATPases</topic><topic>Bacteria</topic><topic>Bacterial Secretion Systems - genetics</topic><topic>Bacterial Secretion Systems - metabolism</topic><topic>Bacterial Toxins - genetics</topic><topic>Binding</topic><topic>Culture</topic><topic>Developing countries</topic><topic>Diarrhea</topic><topic>Diarrhea - microbiology</topic><topic>Diarrhea - veterinary</topic><topic>E coli</topic><topic>Enterotoxigenic Escherichia coli - genetics</topic><topic>Enterotoxigenic Escherichia coli - pathogenicity</topic><topic>Enterotoxigenic Escherichia coli - physiology</topic><topic>Enterotoxins - genetics</topic><topic>Enterotoxins - metabolism</topic><topic>Enzyme-linked immunosorbent assay</topic><topic>Escherichia coli</topic><topic>Escherichia coli Infections - microbiology</topic><topic>Escherichia coli Infections - veterinary</topic><topic>Escherichia coli Proteins - genetics</topic><topic>Escherichia coli Proteins - metabolism</topic><topic>Experiments</topic><topic>Genes</topic><topic>Gnotobiotic</topic><topic>Heat-labile enterotoxin</topic><topic>Hogs</topic><topic>Homology</topic><topic>Humans</topic><topic>LDCs</topic><topic>Mitochondrial DNA</topic><topic>Pathogens</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Swine</topic><topic>Swine Diseases - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wijemanne, Prageeth</au><au>Xing, Jun</au><au>Berberov, Emil M</au><au>Marx, David B</au><au>Francis, David H</au><au>Moxley, Rodney A</au><au>Rajashekara, Gireesh</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Relationship between heat-labile enterotoxin secretion capacity and virulence in wild type porcine-origin enterotoxigenic Escherichia coli strains</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-03-13</date><risdate>2015</risdate><volume>10</volume><issue>3</issue><spage>e0117663</spage><epage>e0117663</epage><pages>e0117663-e0117663</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Heat-labile enterotoxin (LT) is an important virulence factor secreted by some strains of enterotoxigenic Escherichia coli (ETEC). The prototypic human-origin strain H10407 secretes LT via a type II secretion system (T2SS). We sought to determine the relationship between the capacity to secrete LT and virulence in porcine-origin wild type (WT) ETEC strains. Sixteen WT ETEC strains isolated from cases of severe diarrheal disease were analyzed by GM1ganglioside enzyme-linked immunosorbent assay to measure LT concentrations in culture supernatants. All strains had detectable LT in supernatants by 2 h of culture and 1 strain, which was particularly virulent in gnotobiotic piglets (3030-2), had the highest LT secretion level all porcine-origin WT strains tested (P<0.05). The level of LT secretion (concentration in supernatants at 6-h culture) explained 92% of the variation in time-to-a-moribund-condition (R2 = 0.92, P<0.0001) in gnotobiotic piglets inoculated with either strain 3030-2, or an ETEC strain of lesser virulence (2534-86), or a non-enterotoxigenic WT strain (G58-1). All 16 porcine ETEC strains were positive by PCR analysis for the T2SS genes, gspD and gspK, and bioinformatic analysis of 4 porcine-origin strains for which complete genomic sequences were available revealed a T2SS with a high degree of homology to that of H10407. Maximum Likelihood phylogenetic trees constructed using T2SS genes gspC, gspD, gspE and homologs showed that strains 2534-86 and 3030-2 clustered together in the same clade with other porcine-origin ETEC strains in the database, UMNK88 and UMN18. Protein modeling of the ATPase gene (gspE) further revealed a direct relationship between the predicted ATP-binding capacities and LT secretion levels as follows: H10407, -8.8 kcal/mol and 199 ng/ml; 3030-2, -8.6 kcal/mol and 133 ng/ml; and 2534-86, -8.5 kcal/mol and 80 ng/ml. This study demonstrated a direct relationship between predicted ATP-binding capacity of GspE and LT secretion, and between the latter and virulence.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25768732</pmid><doi>10.1371/journal.pone.0117663</doi><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_1663346895 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adenosine triphosphatase Analysis Animals ATP ATPases Bacteria Bacterial Secretion Systems - genetics Bacterial Secretion Systems - metabolism Bacterial Toxins - genetics Binding Culture Developing countries Diarrhea Diarrhea - microbiology Diarrhea - veterinary E coli Enterotoxigenic Escherichia coli - genetics Enterotoxigenic Escherichia coli - pathogenicity Enterotoxigenic Escherichia coli - physiology Enterotoxins - genetics Enterotoxins - metabolism Enzyme-linked immunosorbent assay Escherichia coli Escherichia coli Infections - microbiology Escherichia coli Infections - veterinary Escherichia coli Proteins - genetics Escherichia coli Proteins - metabolism Experiments Genes Gnotobiotic Heat-labile enterotoxin Hogs Homology Humans LDCs Mitochondrial DNA Pathogens Phylogeny Proteins Swine Swine Diseases - microbiology Veterinary colleges Veterinary medicine Vibrio cholerae Virulence Virulence (Microbiology) Virulence factors |
| title | Relationship between heat-labile enterotoxin secretion capacity and virulence in wild type porcine-origin enterotoxigenic Escherichia coli strains |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-26T13%3A13%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Relationship%20between%20heat-labile%20enterotoxin%20secretion%20capacity%20and%20virulence%20in%20wild%20type%20porcine-origin%20enterotoxigenic%20Escherichia%20coli%20strains&rft.jtitle=PloS%20one&rft.au=Wijemanne,%20Prageeth&rft.date=2015-03-13&rft.volume=10&rft.issue=3&rft.spage=e0117663&rft.epage=e0117663&rft.pages=e0117663-e0117663&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0117663&rft_dat=%3Cgale_plos_%3EA422026559%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1663346895&rft_id=info:pmid/25768732&rft_galeid=A422026559&rft_doaj_id=oai_doaj_org_article_ffcac074f9894f049ccf491427452d14&rfr_iscdi=true |