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TonB Energy Transduction Systems of Riemerella anatipestifer Are Required for Iron and Hemin Utilization
Riemerella anatipestifer (R. anatipestifer) is one of the most important pathogens in ducks. The bacteria causes acute or chronic septicemia characterized by fibrinous pericarditis and meningitis. The R. anatipestifer genome encodes multiple iron/hemin-uptake systems that facilitate adaptation to ir...
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Published in: | PloS one 2015-05, Vol.10 (5), p.e0127506-e0127506 |
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description | Riemerella anatipestifer (R. anatipestifer) is one of the most important pathogens in ducks. The bacteria causes acute or chronic septicemia characterized by fibrinous pericarditis and meningitis. The R. anatipestifer genome encodes multiple iron/hemin-uptake systems that facilitate adaptation to iron-limited host environments. These systems include several TonB-dependent transporters and three TonB proteins responsible for energy transduction. These three tonB genes are present in all the R. anatipestifer genomes sequenced so far. Two of these genes are contained within the exbB-exbD-tonB1 and exbB-exbD-exbD-tonB2 operons. The third, tonB3, forms a monocistronic transcription unit. The inability to recover derivatives deleted for this gene suggests its product is essential for R. anatipestifer growth. Here, we show that deletion of tonB1 had no effect on hemin uptake of R. anatipestifer, though disruption of tonB2 strongly decreases hemin uptake, and disruption of both tonB1 and tonB2 abolishes the transport of exogenously added hemin. The ability of R. anatipestifer to grow on iron-depleted medium is decreased by tonB2 but not tonB1 disruption. When expressed in an E. coli model strain, the TonB1 complex, TonB2 complex, and TonB3 protein from R. anatipestifer cannot energize heterologous hemin transporters. Further, only the TonB1 complex can energize a R. anatipestifer hemin transporter when co-expressed in an E. coli model strain. |
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The bacteria causes acute or chronic septicemia characterized by fibrinous pericarditis and meningitis. The R. anatipestifer genome encodes multiple iron/hemin-uptake systems that facilitate adaptation to iron-limited host environments. These systems include several TonB-dependent transporters and three TonB proteins responsible for energy transduction. These three tonB genes are present in all the R. anatipestifer genomes sequenced so far. Two of these genes are contained within the exbB-exbD-tonB1 and exbB-exbD-exbD-tonB2 operons. The third, tonB3, forms a monocistronic transcription unit. The inability to recover derivatives deleted for this gene suggests its product is essential for R. anatipestifer growth. Here, we show that deletion of tonB1 had no effect on hemin uptake of R. anatipestifer, though disruption of tonB2 strongly decreases hemin uptake, and disruption of both tonB1 and tonB2 abolishes the transport of exogenously added hemin. The ability of R. anatipestifer to grow on iron-depleted medium is decreased by tonB2 but not tonB1 disruption. When expressed in an E. coli model strain, the TonB1 complex, TonB2 complex, and TonB3 protein from R. anatipestifer cannot energize heterologous hemin transporters. Further, only the TonB1 complex can energize a R. anatipestifer hemin transporter when co-expressed in an E. coli model strain.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0127506</identifier><identifier>PMID: 26017672</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activation ; Analysis ; Animal diseases ; Aquatic birds ; Archives & records ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacteriology ; Biological Transport - drug effects ; Chromosomes ; Disease prevention ; Disruption ; E coli ; Energy Metabolism - drug effects ; Energy transduction ; Escherichia coli - genetics ; Escherichia coli - growth & development ; Gene Knockout Techniques ; Genes ; Genetic aspects ; Genomes ; Genomics ; Gram-negative bacteria ; Hemin ; Infections ; Iron ; Iron - metabolism ; Iron Chelating Agents - pharmacology ; Laboratories ; Membrane Proteins - deficiency ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Meningitis ; Operons ; Pathogens ; Pericarditis ; Proteins ; Riemerella - genetics ; Riemerella - metabolism ; Septicemia ; Sequence Analysis ; Transcription ; Veterinarians ; Veterinary colleges ; Veterinary medicine ; Vibrio cholerae ; Waterfowl</subject><ispartof>PloS one, 2015-05, Vol.10 (5), p.e0127506-e0127506</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Liao 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 Liao et al 2015 Liao et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-7dcd05f3e2dfb868a7023e83540faa647e04923409be33e95f45af4ae9315e6c3</citedby><cites>FETCH-LOGICAL-c692t-7dcd05f3e2dfb868a7023e83540faa647e04923409be33e95f45af4ae9315e6c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1683578108/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1683578108?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26017672$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liao, HeBin</creatorcontrib><creatorcontrib>Cheng, XingJun</creatorcontrib><creatorcontrib>Zhu, DeKang</creatorcontrib><creatorcontrib>Wang, MingShu</creatorcontrib><creatorcontrib>Jia, RenYong</creatorcontrib><creatorcontrib>Chen, Shun</creatorcontrib><creatorcontrib>Chen, XiaoYue</creatorcontrib><creatorcontrib>Biville, Francis</creatorcontrib><creatorcontrib>Liu, MaFeng</creatorcontrib><creatorcontrib>Cheng, AnChun</creatorcontrib><title>TonB Energy Transduction Systems of Riemerella anatipestifer Are Required for Iron and Hemin Utilization</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Riemerella anatipestifer (R. anatipestifer) is one of the most important pathogens in ducks. The bacteria causes acute or chronic septicemia characterized by fibrinous pericarditis and meningitis. The R. anatipestifer genome encodes multiple iron/hemin-uptake systems that facilitate adaptation to iron-limited host environments. These systems include several TonB-dependent transporters and three TonB proteins responsible for energy transduction. These three tonB genes are present in all the R. anatipestifer genomes sequenced so far. Two of these genes are contained within the exbB-exbD-tonB1 and exbB-exbD-exbD-tonB2 operons. The third, tonB3, forms a monocistronic transcription unit. The inability to recover derivatives deleted for this gene suggests its product is essential for R. anatipestifer growth. Here, we show that deletion of tonB1 had no effect on hemin uptake of R. anatipestifer, though disruption of tonB2 strongly decreases hemin uptake, and disruption of both tonB1 and tonB2 abolishes the transport of exogenously added hemin. The ability of R. anatipestifer to grow on iron-depleted medium is decreased by tonB2 but not tonB1 disruption. When expressed in an E. coli model strain, the TonB1 complex, TonB2 complex, and TonB3 protein from R. anatipestifer cannot energize heterologous hemin transporters. Further, only the TonB1 complex can energize a R. anatipestifer hemin transporter when co-expressed in an E. coli model strain.</description><subject>Activation</subject><subject>Analysis</subject><subject>Animal diseases</subject><subject>Aquatic birds</subject><subject>Archives & records</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Biological Transport - drug effects</subject><subject>Chromosomes</subject><subject>Disease prevention</subject><subject>Disruption</subject><subject>E coli</subject><subject>Energy Metabolism - drug effects</subject><subject>Energy transduction</subject><subject>Escherichia coli - genetics</subject><subject>Escherichia coli - growth & development</subject><subject>Gene Knockout Techniques</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Gram-negative bacteria</subject><subject>Hemin</subject><subject>Infections</subject><subject>Iron</subject><subject>Iron - metabolism</subject><subject>Iron Chelating Agents - pharmacology</subject><subject>Laboratories</subject><subject>Membrane Proteins - deficiency</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Meningitis</subject><subject>Operons</subject><subject>Pathogens</subject><subject>Pericarditis</subject><subject>Proteins</subject><subject>Riemerella - genetics</subject><subject>Riemerella - metabolism</subject><subject>Septicemia</subject><subject>Sequence Analysis</subject><subject>Transcription</subject><subject>Veterinarians</subject><subject>Veterinary colleges</subject><subject>Veterinary medicine</subject><subject>Vibrio cholerae</subject><subject>Waterfowl</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11v0zAUhiMEYqPwDxBYQkJw0WLHjpPcIJVpsEqTJnUdt5YbH7eeEruzE0T59ThrNjVoFygXiZznfc-Hz0mStwTPCM3Jl1vXeSvr2c5ZmGGS5hnmz5JTUtJ0ylNMnx99nySvQrjFOKMF5y-Tk5RjkvM8PU22K2e_oXMLfrNHKy9tUF3VGmfR9T600ATkNFoaaMBDXUskrWzNDkJrNHg094CWcNcZDwpp59HCR6W0Cl1AYyy6aU1t_sje73XyQss6wJvhPUluvp-vzi6ml1c_Fmfzy2nFy7Sd5qpSONMUUqXXBS9kjlMKBc0Y1lJylgNmZUoZLtdAKZSZZpnUTEJJSQa8opPk_cF3V7sghiYFQXj0yAuCi0gsDoRy8lbsvGmk3wsnjbg_cH4jpG9NVYNQRLIog1yxjCmmimJNOI5ZZYRhVcjo9XWI1q0bUBXY1st6ZDr-Y81WbNwvwRjjNJY2ST4NBt7ddbGvojGh6lttwXX3ebOYAs9xRD_8gz5d3UBtZCzAWO1i3Ko3FXNGUxZngPZhZ09Q8VHx3qo4UdrE85Hg80gQmRZ-txvZhSAW18v_Z69-jtmPR-wWZN1ug6u7fmTCGGQHsPIuBA_6sckEi34hHroh-oUQw0JE2bvjC3oUPWwA_QsmQgUk</recordid><startdate>20150527</startdate><enddate>20150527</enddate><creator>Liao, HeBin</creator><creator>Cheng, XingJun</creator><creator>Zhu, DeKang</creator><creator>Wang, MingShu</creator><creator>Jia, RenYong</creator><creator>Chen, Shun</creator><creator>Chen, XiaoYue</creator><creator>Biville, Francis</creator><creator>Liu, MaFeng</creator><creator>Cheng, AnChun</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>20150527</creationdate><title>TonB Energy Transduction Systems of Riemerella anatipestifer Are Required for Iron and Hemin Utilization</title><author>Liao, HeBin ; Cheng, XingJun ; Zhu, DeKang ; Wang, MingShu ; Jia, RenYong ; Chen, Shun ; Chen, XiaoYue ; Biville, Francis ; Liu, MaFeng ; Cheng, AnChun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-7dcd05f3e2dfb868a7023e83540faa647e04923409be33e95f45af4ae9315e6c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Activation</topic><topic>Analysis</topic><topic>Animal diseases</topic><topic>Aquatic birds</topic><topic>Archives & records</topic><topic>Bacteria</topic><topic>Bacterial Proteins - 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The bacteria causes acute or chronic septicemia characterized by fibrinous pericarditis and meningitis. The R. anatipestifer genome encodes multiple iron/hemin-uptake systems that facilitate adaptation to iron-limited host environments. These systems include several TonB-dependent transporters and three TonB proteins responsible for energy transduction. These three tonB genes are present in all the R. anatipestifer genomes sequenced so far. Two of these genes are contained within the exbB-exbD-tonB1 and exbB-exbD-exbD-tonB2 operons. The third, tonB3, forms a monocistronic transcription unit. The inability to recover derivatives deleted for this gene suggests its product is essential for R. anatipestifer growth. Here, we show that deletion of tonB1 had no effect on hemin uptake of R. anatipestifer, though disruption of tonB2 strongly decreases hemin uptake, and disruption of both tonB1 and tonB2 abolishes the transport of exogenously added hemin. The ability of R. anatipestifer to grow on iron-depleted medium is decreased by tonB2 but not tonB1 disruption. When expressed in an E. coli model strain, the TonB1 complex, TonB2 complex, and TonB3 protein from R. anatipestifer cannot energize heterologous hemin transporters. Further, only the TonB1 complex can energize a R. anatipestifer hemin transporter when co-expressed in an E. coli model strain.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26017672</pmid><doi>10.1371/journal.pone.0127506</doi><oa>free_for_read</oa></addata></record> |
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subjects | Activation Analysis Animal diseases Aquatic birds Archives & records Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacteriology Biological Transport - drug effects Chromosomes Disease prevention Disruption E coli Energy Metabolism - drug effects Energy transduction Escherichia coli - genetics Escherichia coli - growth & development Gene Knockout Techniques Genes Genetic aspects Genomes Genomics Gram-negative bacteria Hemin Infections Iron Iron - metabolism Iron Chelating Agents - pharmacology Laboratories Membrane Proteins - deficiency Membrane Proteins - genetics Membrane Proteins - metabolism Meningitis Operons Pathogens Pericarditis Proteins Riemerella - genetics Riemerella - metabolism Septicemia Sequence Analysis Transcription Veterinarians Veterinary colleges Veterinary medicine Vibrio cholerae Waterfowl |
title | TonB Energy Transduction Systems of Riemerella anatipestifer Are Required for Iron and Hemin Utilization |
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