Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor
Klebsiella pneumoniae strains are pathogenic to animals and humans, in which they are both a frequent cause of nosocomial infections and a re-emerging cause of severe community-acquired infections. K. pneumoniae isolates of the capsular serotype K2 are among the most virulent. In order to identify n...
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| Veröffentlicht in: | BMC biology 2014-05, Vol.12 (1), p.41-41, Article 41 |
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| creator | Lery, Letícia M S Frangeul, Lionel Tomas, Anna Passet, Virginie Almeida, Ana S Bialek-Davenet, Suzanne Barbe, Valérie Bengoechea, José A Sansonetti, Philippe Brisse, Sylvain Tournebize, Régis |
| description | Klebsiella pneumoniae strains are pathogenic to animals and humans, in which they are both a frequent cause of nosocomial infections and a re-emerging cause of severe community-acquired infections. K. pneumoniae isolates of the capsular serotype K2 are among the most virulent. In order to identify novel putative virulence factors that may account for the severity of K2 infections, the genome sequence of the K2 reference strain Kp52.145 was determined and compared to two K1 and K2 strains of low virulence and to the reference strains MGH 78578 and NTUH-K2044.
In addition to diverse functions related to host colonization and virulence encoded in genomic regions common to the four strains, four genomic islands specific for Kp52.145 were identified. These regions encoded genes for the synthesis of colibactin toxin, a putative cytotoxin outer membrane protein, secretion systems, nucleases and eukaryotic-like proteins. In addition, an insertion within a type VI secretion system locus included sel1 domain containing proteins and a phospholipase D family protein (PLD1). The pld1 mutant was avirulent in a pneumonia model in mouse. The pld1 mRNA was expressed in vivo and the pld1 gene was associated with K. pneumoniae isolates from severe infections. Analysis of lipid composition of a defective E. coli strain complemented with pld1 suggests an involvement of PLD1 in cardiolipin metabolism.
Determination of the complete genome of the K2 reference strain identified several genomic islands comprising putative elements of pathogenicity. The role of PLD1 in pathogenesis was demonstrated for the first time and suggests that lipid metabolism is a novel virulence mechanism of K. pneumoniae. |
| doi_str_mv | 10.1186/1741-7007-12-41 |
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In addition to diverse functions related to host colonization and virulence encoded in genomic regions common to the four strains, four genomic islands specific for Kp52.145 were identified. These regions encoded genes for the synthesis of colibactin toxin, a putative cytotoxin outer membrane protein, secretion systems, nucleases and eukaryotic-like proteins. In addition, an insertion within a type VI secretion system locus included sel1 domain containing proteins and a phospholipase D family protein (PLD1). The pld1 mutant was avirulent in a pneumonia model in mouse. The pld1 mRNA was expressed in vivo and the pld1 gene was associated with K. pneumoniae isolates from severe infections. Analysis of lipid composition of a defective E. coli strain complemented with pld1 suggests an involvement of PLD1 in cardiolipin metabolism.
Determination of the complete genome of the K2 reference strain identified several genomic islands comprising putative elements of pathogenicity. The role of PLD1 in pathogenesis was demonstrated for the first time and suggests that lipid metabolism is a novel virulence mechanism of K. pneumoniae.</description><identifier>ISSN: 1741-7007</identifier><identifier>EISSN: 1741-7007</identifier><identifier>DOI: 10.1186/1741-7007-12-41</identifier><identifier>PMID: 24885329</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Amino Acid Sequence ; Animals ; Bacterial Proteins - chemistry ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Bacterial Secretion Systems - genetics ; Bacteriology ; Comparative analysis ; DNA binding proteins ; Escherichia coli ; Genes ; Genes, Bacterial - genetics ; Genetic aspects ; Genome, Bacterial - genetics ; Genomic Islands - genetics ; Genomics ; Health aspects ; Klebsiella pneumoniae ; Klebsiella pneumoniae - genetics ; Klebsiella pneumoniae - isolation & purification ; Klebsiella pneumoniae - pathogenicity ; Life Sciences ; Lipid Metabolism - genetics ; Lipids ; Mice ; Molecular Sequence Annotation ; Molecular Sequence Data ; Multigene Family ; Mutagenesis, Insertional - genetics ; Nucleases ; Phospholipase D - chemistry ; Phospholipase D - genetics ; Phospholipases ; Physiological aspects ; Plasmids ; Plasmids - genetics ; Sequence Alignment ; Virulence (Microbiology) ; Virulence - genetics ; Virulence Factors - genetics</subject><ispartof>BMC biology, 2014-05, Vol.12 (1), p.41-41, Article 41</ispartof><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>2014 Lery et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2014 Lery et al.; licensee BioMed Central Ltd. 2014 Lery et al.; licensee BioMed Central Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c693t-c301bc15f1b9e35d01a761f2a9c5ca914fa6de49e6904185533cbd8e6f516b013</citedby><cites>FETCH-LOGICAL-c693t-c301bc15f1b9e35d01a761f2a9c5ca914fa6de49e6904185533cbd8e6f516b013</cites><orcidid>0000-0001-7542-4527 ; 0000-0002-8162-3343 ; 0000-0002-2516-2108 ; 0000-0002-0992-8775</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4068068/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4068068/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24885329$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://pasteur.hal.science/pasteur-01011838$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Lery, Letícia M S</creatorcontrib><creatorcontrib>Frangeul, Lionel</creatorcontrib><creatorcontrib>Tomas, Anna</creatorcontrib><creatorcontrib>Passet, Virginie</creatorcontrib><creatorcontrib>Almeida, Ana S</creatorcontrib><creatorcontrib>Bialek-Davenet, Suzanne</creatorcontrib><creatorcontrib>Barbe, Valérie</creatorcontrib><creatorcontrib>Bengoechea, José A</creatorcontrib><creatorcontrib>Sansonetti, Philippe</creatorcontrib><creatorcontrib>Brisse, Sylvain</creatorcontrib><creatorcontrib>Tournebize, Régis</creatorcontrib><title>Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor</title><title>BMC biology</title><addtitle>BMC Biol</addtitle><description>Klebsiella pneumoniae strains are pathogenic to animals and humans, in which they are both a frequent cause of nosocomial infections and a re-emerging cause of severe community-acquired infections. K. pneumoniae isolates of the capsular serotype K2 are among the most virulent. In order to identify novel putative virulence factors that may account for the severity of K2 infections, the genome sequence of the K2 reference strain Kp52.145 was determined and compared to two K1 and K2 strains of low virulence and to the reference strains MGH 78578 and NTUH-K2044.
In addition to diverse functions related to host colonization and virulence encoded in genomic regions common to the four strains, four genomic islands specific for Kp52.145 were identified. These regions encoded genes for the synthesis of colibactin toxin, a putative cytotoxin outer membrane protein, secretion systems, nucleases and eukaryotic-like proteins. In addition, an insertion within a type VI secretion system locus included sel1 domain containing proteins and a phospholipase D family protein (PLD1). The pld1 mutant was avirulent in a pneumonia model in mouse. The pld1 mRNA was expressed in vivo and the pld1 gene was associated with K. pneumoniae isolates from severe infections. Analysis of lipid composition of a defective E. coli strain complemented with pld1 suggests an involvement of PLD1 in cardiolipin metabolism.
Determination of the complete genome of the K2 reference strain identified several genomic islands comprising putative elements of pathogenicity. The role of PLD1 in pathogenesis was demonstrated for the first time and suggests that lipid metabolism is a novel virulence mechanism of K. pneumoniae.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Bacterial Proteins - chemistry</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Bacterial Secretion Systems - genetics</subject><subject>Bacteriology</subject><subject>Comparative analysis</subject><subject>DNA binding proteins</subject><subject>Escherichia coli</subject><subject>Genes</subject><subject>Genes, Bacterial - genetics</subject><subject>Genetic aspects</subject><subject>Genome, Bacterial - genetics</subject><subject>Genomic Islands - genetics</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Klebsiella pneumoniae</subject><subject>Klebsiella pneumoniae - genetics</subject><subject>Klebsiella pneumoniae - isolation & purification</subject><subject>Klebsiella pneumoniae - pathogenicity</subject><subject>Life Sciences</subject><subject>Lipid Metabolism - genetics</subject><subject>Lipids</subject><subject>Mice</subject><subject>Molecular Sequence Annotation</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Mutagenesis, Insertional - genetics</subject><subject>Nucleases</subject><subject>Phospholipase D - chemistry</subject><subject>Phospholipase D - genetics</subject><subject>Phospholipases</subject><subject>Physiological aspects</subject><subject>Plasmids</subject><subject>Plasmids - genetics</subject><subject>Sequence Alignment</subject><subject>Virulence (Microbiology)</subject><subject>Virulence - genetics</subject><subject>Virulence Factors - 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analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor</title><author>Lery, Letícia M S ; Frangeul, Lionel ; Tomas, Anna ; Passet, Virginie ; Almeida, Ana S ; Bialek-Davenet, Suzanne ; Barbe, Valérie ; Bengoechea, José A ; Sansonetti, Philippe ; Brisse, Sylvain ; Tournebize, Régis</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c693t-c301bc15f1b9e35d01a761f2a9c5ca914fa6de49e6904185533cbd8e6f516b013</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Bacterial Proteins - chemistry</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Bacterial Secretion Systems - genetics</topic><topic>Bacteriology</topic><topic>Comparative analysis</topic><topic>DNA binding proteins</topic><topic>Escherichia 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Biol</addtitle><date>2014-05-29</date><risdate>2014</risdate><volume>12</volume><issue>1</issue><spage>41</spage><epage>41</epage><pages>41-41</pages><artnum>41</artnum><issn>1741-7007</issn><eissn>1741-7007</eissn><abstract>Klebsiella pneumoniae strains are pathogenic to animals and humans, in which they are both a frequent cause of nosocomial infections and a re-emerging cause of severe community-acquired infections. K. pneumoniae isolates of the capsular serotype K2 are among the most virulent. In order to identify novel putative virulence factors that may account for the severity of K2 infections, the genome sequence of the K2 reference strain Kp52.145 was determined and compared to two K1 and K2 strains of low virulence and to the reference strains MGH 78578 and NTUH-K2044.
In addition to diverse functions related to host colonization and virulence encoded in genomic regions common to the four strains, four genomic islands specific for Kp52.145 were identified. These regions encoded genes for the synthesis of colibactin toxin, a putative cytotoxin outer membrane protein, secretion systems, nucleases and eukaryotic-like proteins. In addition, an insertion within a type VI secretion system locus included sel1 domain containing proteins and a phospholipase D family protein (PLD1). The pld1 mutant was avirulent in a pneumonia model in mouse. The pld1 mRNA was expressed in vivo and the pld1 gene was associated with K. pneumoniae isolates from severe infections. Analysis of lipid composition of a defective E. coli strain complemented with pld1 suggests an involvement of PLD1 in cardiolipin metabolism.
Determination of the complete genome of the K2 reference strain identified several genomic islands comprising putative elements of pathogenicity. The role of PLD1 in pathogenesis was demonstrated for the first time and suggests that lipid metabolism is a novel virulence mechanism of K. pneumoniae.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>24885329</pmid><doi>10.1186/1741-7007-12-41</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-7542-4527</orcidid><orcidid>https://orcid.org/0000-0002-8162-3343</orcidid><orcidid>https://orcid.org/0000-0002-2516-2108</orcidid><orcidid>https://orcid.org/0000-0002-0992-8775</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | BMC biology, 2014-05, Vol.12 (1), p.41-41, Article 41 |
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| source | MEDLINE; Springer Nature - Complete Springer Journals; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; PubMed Central Open Access; Springer Nature OA Free Journals |
| subjects | Amino Acid Sequence Animals Bacterial Proteins - chemistry Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Secretion Systems - genetics Bacteriology Comparative analysis DNA binding proteins Escherichia coli Genes Genes, Bacterial - genetics Genetic aspects Genome, Bacterial - genetics Genomic Islands - genetics Genomics Health aspects Klebsiella pneumoniae Klebsiella pneumoniae - genetics Klebsiella pneumoniae - isolation & purification Klebsiella pneumoniae - pathogenicity Life Sciences Lipid Metabolism - genetics Lipids Mice Molecular Sequence Annotation Molecular Sequence Data Multigene Family Mutagenesis, Insertional - genetics Nucleases Phospholipase D - chemistry Phospholipase D - genetics Phospholipases Physiological aspects Plasmids Plasmids - genetics Sequence Alignment Virulence (Microbiology) Virulence - genetics Virulence Factors - genetics |
| title | Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-20T20%3A44%3A19IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Comparative%20analysis%20of%20Klebsiella%20pneumoniae%20genomes%20identifies%20a%20phospholipase%20D%20family%20protein%20as%20a%20novel%20virulence%20factor&rft.jtitle=BMC%20biology&rft.au=Lery,%20Let%C3%ADcia%20M%20S&rft.date=2014-05-29&rft.volume=12&rft.issue=1&rft.spage=41&rft.epage=41&rft.pages=41-41&rft.artnum=41&rft.issn=1741-7007&rft.eissn=1741-7007&rft_id=info:doi/10.1186/1741-7007-12-41&rft_dat=%3Cgale_pubme%3EA539610809%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1539974496&rft_id=info:pmid/24885329&rft_galeid=A539610809&rfr_iscdi=true |