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Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity

Robert J Goldstone, Roman Popat, Hans-Joachim Schuberth, Olivier Sandra, I Martin Sheldon, David GE Smith, Martin Sheldon Orcid Logo

BMC Genomics, Volume: 15, Issue: 1, Start page: 1075

Swansea University Author: Martin Sheldon Orcid Logo

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DOI (Published version): 10.1186/1471-2164-15-1075

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BackgroundStrains of Escherichia coli cause a wide variety of intestinal and extra-intestinal diseases in both humans and animals, and are also often found in healthy individuals or the environment. Broadly, a strong phylogenetic relationship exists that distinguishes most E. coli causing intestinal...

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Published in: BMC Genomics
Published: 2014
URI: https://cronfa.swan.ac.uk/Record/cronfa20050
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fullrecord <?xml version="1.0"?><rfc1807><datestamp>2019-08-28T14:30:14.6065574</datestamp><bib-version>v2</bib-version><id>20050</id><entry>2015-01-22</entry><title>Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity</title><swanseaauthors><author><sid>ab0f74b794e59cc270c69e63ee1d9748</sid><ORCID>0000-0001-7902-5558</ORCID><firstname>Martin</firstname><surname>Sheldon</surname><name>Martin Sheldon</name><active>true</active><ethesisStudent>false</ethesisStudent></author></swanseaauthors><date>2015-01-22</date><deptcode>BMS</deptcode><abstract>BackgroundStrains of Escherichia coli cause a wide variety of intestinal and extra-intestinal diseases in both humans and animals, and are also often found in healthy individuals or the environment. Broadly, a strong phylogenetic relationship exists that distinguishes most E. coli causing intestinal disease from those that cause extra-intestinal disease, however, isolates within a recently described subclass of Extra-Intestinal Pathogenic E. coli (ExPEC), termed endometrial pathogenic E. coli, tend to be phylogenetically distant from the vast majority of characterised ExPECs, and more closely related to human intestinal pathogens. In this work, we investigate the genetic basis for ExPEC infection in the prototypic endometrial pathogenic E. coli strain MS499. ResultsBy investigating the genome of MS499 in comparison with a range of other E. coli sequences, we have discovered that this bacterium has acquired substantial lengths of DNA which encode factors more usually associated with ExPECs and less frequently found in the phylogroup relatives of MS499. Many of these acquired factors, including several iron acquisition systems and a virulence plasmid similar to that found in several ExPECs such as APEC O1 and the neonatal meningitis E. coli S88, play characterised roles in a variety of typical ExPEC infections and appear to have been acquired recently by the evolutionary lineage leading to MS499. ConclusionsTaking advantage of the phylogenetic relationship we describe between MS499 and several other closely related E. coli isolates from across the globe, we propose a step-wise evolution of a novel clade of sequence type 453 ExPECs within phylogroup B1, involving the recruitment of ExPEC virulence factors into the genome of an ancestrally non-extraintestinal E. coli, which has repurposed this lineage with the capacity to cause extraintestinal disease. These data reveal the genetic components which may be involved in this phenotype switching, and argue that horizontal gene exchange may be a key factor in the emergence of novel lineages of ExPECs.</abstract><type>Journal Article</type><journal>BMC Genomics</journal><volume>15</volume><journalNumber>1</journalNumber><paginationStart>1075</paginationStart><publisher/><keywords/><publishedDay>6</publishedDay><publishedMonth>12</publishedMonth><publishedYear>2014</publishedYear><publishedDate>2014-12-06</publishedDate><doi>10.1186/1471-2164-15-1075</doi><url/><notes>This work was funded by 2 BBSRC grants to Smith and to Sheldon, under a programme ERA NET Animal Health grant, within the EU.</notes><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2019-08-28T14:30:14.6065574</lastEdited><Created>2015-01-22T11:07:23.7677480</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Medicine</level></path><authors><author><firstname>Robert J</firstname><surname>Goldstone</surname><order>1</order></author><author><firstname>Roman</firstname><surname>Popat</surname><order>2</order></author><author><firstname>Hans-Joachim</firstname><surname>Schuberth</surname><order>3</order></author><author><firstname>Olivier</firstname><surname>Sandra</surname><order>4</order></author><author><firstname>I Martin</firstname><surname>Sheldon</surname><order>5</order></author><author><firstname>David GE</firstname><surname>Smith</surname><order>6</order></author><author><firstname>Martin</firstname><surname>Sheldon</surname><orcid>0000-0001-7902-5558</orcid><order>7</order></author></authors><documents><document><filename>0020050-29032015220758.pdf</filename><originalFilename>Goldstone.pdf</originalFilename><uploaded>2015-03-29T22:07:58.3930000</uploaded><type>Output</type><contentLength>1534473</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><embargoDate>2015-01-15T12:55:30.4970000</embargoDate><documentNotes>Distributed under the terms of a Creative Commons Attribution (CC-BY-4.0)</documentNotes><copyrightCorrect>true</copyrightCorrect></document></documents><OutputDurs/></rfc1807>
spelling 2019-08-28T14:30:14.6065574 v2 20050 2015-01-22 Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity ab0f74b794e59cc270c69e63ee1d9748 0000-0001-7902-5558 Martin Sheldon Martin Sheldon true false 2015-01-22 BMS BackgroundStrains of Escherichia coli cause a wide variety of intestinal and extra-intestinal diseases in both humans and animals, and are also often found in healthy individuals or the environment. Broadly, a strong phylogenetic relationship exists that distinguishes most E. coli causing intestinal disease from those that cause extra-intestinal disease, however, isolates within a recently described subclass of Extra-Intestinal Pathogenic E. coli (ExPEC), termed endometrial pathogenic E. coli, tend to be phylogenetically distant from the vast majority of characterised ExPECs, and more closely related to human intestinal pathogens. In this work, we investigate the genetic basis for ExPEC infection in the prototypic endometrial pathogenic E. coli strain MS499. ResultsBy investigating the genome of MS499 in comparison with a range of other E. coli sequences, we have discovered that this bacterium has acquired substantial lengths of DNA which encode factors more usually associated with ExPECs and less frequently found in the phylogroup relatives of MS499. Many of these acquired factors, including several iron acquisition systems and a virulence plasmid similar to that found in several ExPECs such as APEC O1 and the neonatal meningitis E. coli S88, play characterised roles in a variety of typical ExPEC infections and appear to have been acquired recently by the evolutionary lineage leading to MS499. ConclusionsTaking advantage of the phylogenetic relationship we describe between MS499 and several other closely related E. coli isolates from across the globe, we propose a step-wise evolution of a novel clade of sequence type 453 ExPECs within phylogroup B1, involving the recruitment of ExPEC virulence factors into the genome of an ancestrally non-extraintestinal E. coli, which has repurposed this lineage with the capacity to cause extraintestinal disease. These data reveal the genetic components which may be involved in this phenotype switching, and argue that horizontal gene exchange may be a key factor in the emergence of novel lineages of ExPECs. Journal Article BMC Genomics 15 1 1075 6 12 2014 2014-12-06 10.1186/1471-2164-15-1075 This work was funded by 2 BBSRC grants to Smith and to Sheldon, under a programme ERA NET Animal Health grant, within the EU. COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University 2019-08-28T14:30:14.6065574 2015-01-22T11:07:23.7677480 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Robert J Goldstone 1 Roman Popat 2 Hans-Joachim Schuberth 3 Olivier Sandra 4 I Martin Sheldon 5 David GE Smith 6 Martin Sheldon 0000-0001-7902-5558 7 0020050-29032015220758.pdf Goldstone.pdf 2015-03-29T22:07:58.3930000 Output 1534473 application/pdf Version of Record true 2015-01-15T12:55:30.4970000 Distributed under the terms of a Creative Commons Attribution (CC-BY-4.0) true
title Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
spellingShingle Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
Martin Sheldon
title_short Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
title_full Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
title_fullStr Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
title_full_unstemmed Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
title_sort Genomic characterisation of an endometrial pathogenic Escherichia coli strain reveals the acquisition of genetic elements associated with extra-intestinal pathogenicity
author_id_str_mv ab0f74b794e59cc270c69e63ee1d9748
author_id_fullname_str_mv ab0f74b794e59cc270c69e63ee1d9748_***_Martin Sheldon
author Martin Sheldon
author2 Robert J Goldstone
Roman Popat
Hans-Joachim Schuberth
Olivier Sandra
I Martin Sheldon
David GE Smith
Martin Sheldon
format Journal article
container_title BMC Genomics
container_volume 15
container_issue 1
container_start_page 1075
publishDate 2014
institution Swansea University
doi_str_mv 10.1186/1471-2164-15-1075
college_str Faculty of Medicine, Health and Life Sciences
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hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
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description BackgroundStrains of Escherichia coli cause a wide variety of intestinal and extra-intestinal diseases in both humans and animals, and are also often found in healthy individuals or the environment. Broadly, a strong phylogenetic relationship exists that distinguishes most E. coli causing intestinal disease from those that cause extra-intestinal disease, however, isolates within a recently described subclass of Extra-Intestinal Pathogenic E. coli (ExPEC), termed endometrial pathogenic E. coli, tend to be phylogenetically distant from the vast majority of characterised ExPECs, and more closely related to human intestinal pathogens. In this work, we investigate the genetic basis for ExPEC infection in the prototypic endometrial pathogenic E. coli strain MS499. ResultsBy investigating the genome of MS499 in comparison with a range of other E. coli sequences, we have discovered that this bacterium has acquired substantial lengths of DNA which encode factors more usually associated with ExPECs and less frequently found in the phylogroup relatives of MS499. Many of these acquired factors, including several iron acquisition systems and a virulence plasmid similar to that found in several ExPECs such as APEC O1 and the neonatal meningitis E. coli S88, play characterised roles in a variety of typical ExPEC infections and appear to have been acquired recently by the evolutionary lineage leading to MS499. ConclusionsTaking advantage of the phylogenetic relationship we describe between MS499 and several other closely related E. coli isolates from across the globe, we propose a step-wise evolution of a novel clade of sequence type 453 ExPECs within phylogroup B1, involving the recruitment of ExPEC virulence factors into the genome of an ancestrally non-extraintestinal E. coli, which has repurposed this lineage with the capacity to cause extraintestinal disease. These data reveal the genetic components which may be involved in this phenotype switching, and argue that horizontal gene exchange may be a key factor in the emergence of novel lineages of ExPECs.
published_date 2014-12-06T03:23:37Z
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