Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter
Acinetobacter baumannii is an emergent and global nosocomial pathogen. In addition to A. baumannii, other Acinetobacter species, especially those in the Acinetobacter calcoaceticus-baumannii (Acb) complex, have also been associated with serious human infection. Although mechanisms of attachment, per...
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| description | Acinetobacter baumannii is an emergent and global nosocomial pathogen. In addition to A. baumannii, other Acinetobacter species, especially those in the Acinetobacter calcoaceticus-baumannii (Acb) complex, have also been associated with serious human infection. Although mechanisms of attachment, persistence on abiotic surfaces, and pathogenesis in A. baumannii have been identified, the genetic mechanisms that explain the emergence of A. baumannii as the most widespread and virulent Acinetobacter species are not fully understood. Recent whole genome sequencing has provided insight into the phylogenetic structure of the genus Acinetobacter. However, a global comparison of genomic features between Acinetobacter spp. has not been described in the literature. In this study, 136 Acinetobacter genomes, including 67 sequenced in this study, were compared to identify the acquisition and loss of genes in the expansion of the Acinetobacter genus. A whole genome phylogeny confirmed that A. baumannii is a monophyletic clade and that the larger Acb complex is also a well-supported monophyletic group. The whole genome phylogeny provided the framework for a global genomic comparison based on a blast score ratio (BSR) analysis. The BSR analysis demonstrated that specific genes have been both lost and acquired in the evolution of A. baumannii. In addition, several genes associated with A. baumannii pathogenesis were found to be more conserved in the Acb complex, and especially in A. baumannii, than in other Acinetobacter genomes; until recently, a global analysis of the distribution and conservation of virulence factors across the genus was not possible. The results demonstrate that the acquisition of specific virulence factors has likely contributed to the widespread persistence and virulence of A. baumannii. The identification of novel features associated with transcriptional regulation and acquired by clades in the Acb complex presents targets for better understanding the evolution of pathogenesis and virulence in the expansion of the genus. |
| doi_str_mv | 10.1371/journal.pone.0054287 |
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Ross</contributor><creatorcontrib>Sahl, Jason W ; Gillece, John D ; Schupp, James M ; Waddell, Victor G ; Driebe, Elizabeth M ; Engelthaler, David M ; Keim, Paul ; Fitzgerald, J. Ross</creatorcontrib><description>Acinetobacter baumannii is an emergent and global nosocomial pathogen. In addition to A. baumannii, other Acinetobacter species, especially those in the Acinetobacter calcoaceticus-baumannii (Acb) complex, have also been associated with serious human infection. Although mechanisms of attachment, persistence on abiotic surfaces, and pathogenesis in A. baumannii have been identified, the genetic mechanisms that explain the emergence of A. baumannii as the most widespread and virulent Acinetobacter species are not fully understood. Recent whole genome sequencing has provided insight into the phylogenetic structure of the genus Acinetobacter. However, a global comparison of genomic features between Acinetobacter spp. has not been described in the literature. In this study, 136 Acinetobacter genomes, including 67 sequenced in this study, were compared to identify the acquisition and loss of genes in the expansion of the Acinetobacter genus. A whole genome phylogeny confirmed that A. baumannii is a monophyletic clade and that the larger Acb complex is also a well-supported monophyletic group. The whole genome phylogeny provided the framework for a global genomic comparison based on a blast score ratio (BSR) analysis. The BSR analysis demonstrated that specific genes have been both lost and acquired in the evolution of A. baumannii. In addition, several genes associated with A. baumannii pathogenesis were found to be more conserved in the Acb complex, and especially in A. baumannii, than in other Acinetobacter genomes; until recently, a global analysis of the distribution and conservation of virulence factors across the genus was not possible. The results demonstrate that the acquisition of specific virulence factors has likely contributed to the widespread persistence and virulence of A. baumannii. The identification of novel features associated with transcriptional regulation and acquired by clades in the Acb complex presents targets for better understanding the evolution of pathogenesis and virulence in the expansion of the genus.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0054287</identifier><identifier>PMID: 23365658</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acinetobacter ; Acinetobacter - classification ; Acinetobacter - genetics ; Acinetobacter - isolation & purification ; Acinetobacter - pathogenicity ; Acinetobacter baumannii ; Acinetobacter baumannii - classification ; Acinetobacter baumannii - genetics ; Acinetobacter baumannii - isolation & purification ; Acinetobacter baumannii - pathogenicity ; Acinetobacter calcoaceticus ; Acinetobacter Infections - microbiology ; Antimicrobial agents ; Bacterial Proteins - classification ; Bacterial Proteins - genetics ; Base Sequence ; Biochemistry ; Biofilms ; Biological Evolution ; Biology ; Chromosome Mapping ; Chromosomes, Bacterial - genetics ; Conservation ; Deoxyribonucleic acid ; DNA ; Epidemiology ; Evolution ; Evolutionary genetics ; Gene regulation ; Gene sequencing ; Genes ; Genetic aspects ; Genetic testing ; Genome, Bacterial ; Genomes ; Genomics ; Genotypes ; Health aspects ; Hospitals ; Humans ; Infectious diseases ; Medicine ; Microbiology ; Multilocus Sequence Typing ; Nosocomial infection ; Nosocomial infections ; Pathogenesis ; Pathogens ; Phylogeny ; RNA, Ribosomal, 16S - classification ; RNA, Ribosomal, 16S - genetics ; Transcription ; Transcription (Genetics) ; Virulence ; Virulence (Microbiology) ; Virulence factors ; Virulence Factors - classification ; Virulence Factors - genetics</subject><ispartof>PloS one, 2013-01, Vol.8 (1), p.e54287-e54287</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Sahl et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://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>2013 Sahl et al 2013 Sahl et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c692t-7cad091a3bbab19aaf8b2453e42c95758c44ed25bbd817c958a051b819d9c9653</citedby><cites>FETCH-LOGICAL-c692t-7cad091a3bbab19aaf8b2453e42c95758c44ed25bbd817c958a051b819d9c9653</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/PMC3554770/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3554770/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23365658$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Fitzgerald, J. Ross</contributor><creatorcontrib>Sahl, Jason W</creatorcontrib><creatorcontrib>Gillece, John D</creatorcontrib><creatorcontrib>Schupp, James M</creatorcontrib><creatorcontrib>Waddell, Victor G</creatorcontrib><creatorcontrib>Driebe, Elizabeth M</creatorcontrib><creatorcontrib>Engelthaler, David M</creatorcontrib><creatorcontrib>Keim, Paul</creatorcontrib><title>Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Acinetobacter baumannii is an emergent and global nosocomial pathogen. In addition to A. baumannii, other Acinetobacter species, especially those in the Acinetobacter calcoaceticus-baumannii (Acb) complex, have also been associated with serious human infection. Although mechanisms of attachment, persistence on abiotic surfaces, and pathogenesis in A. baumannii have been identified, the genetic mechanisms that explain the emergence of A. baumannii as the most widespread and virulent Acinetobacter species are not fully understood. Recent whole genome sequencing has provided insight into the phylogenetic structure of the genus Acinetobacter. However, a global comparison of genomic features between Acinetobacter spp. has not been described in the literature. In this study, 136 Acinetobacter genomes, including 67 sequenced in this study, were compared to identify the acquisition and loss of genes in the expansion of the Acinetobacter genus. A whole genome phylogeny confirmed that A. baumannii is a monophyletic clade and that the larger Acb complex is also a well-supported monophyletic group. The whole genome phylogeny provided the framework for a global genomic comparison based on a blast score ratio (BSR) analysis. The BSR analysis demonstrated that specific genes have been both lost and acquired in the evolution of A. baumannii. In addition, several genes associated with A. baumannii pathogenesis were found to be more conserved in the Acb complex, and especially in A. baumannii, than in other Acinetobacter genomes; until recently, a global analysis of the distribution and conservation of virulence factors across the genus was not possible. The results demonstrate that the acquisition of specific virulence factors has likely contributed to the widespread persistence and virulence of A. baumannii. The identification of novel features associated with transcriptional regulation and acquired by clades in the Acb complex presents targets for better understanding the evolution of pathogenesis and virulence in the expansion of the genus.</description><subject>Acinetobacter</subject><subject>Acinetobacter - classification</subject><subject>Acinetobacter - genetics</subject><subject>Acinetobacter - isolation & purification</subject><subject>Acinetobacter - pathogenicity</subject><subject>Acinetobacter baumannii</subject><subject>Acinetobacter baumannii - classification</subject><subject>Acinetobacter baumannii - genetics</subject><subject>Acinetobacter baumannii - isolation & purification</subject><subject>Acinetobacter baumannii - pathogenicity</subject><subject>Acinetobacter calcoaceticus</subject><subject>Acinetobacter Infections - microbiology</subject><subject>Antimicrobial agents</subject><subject>Bacterial Proteins - classification</subject><subject>Bacterial Proteins - genetics</subject><subject>Base Sequence</subject><subject>Biochemistry</subject><subject>Biofilms</subject><subject>Biological Evolution</subject><subject>Biology</subject><subject>Chromosome Mapping</subject><subject>Chromosomes, Bacterial - genetics</subject><subject>Conservation</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Epidemiology</subject><subject>Evolution</subject><subject>Evolutionary genetics</subject><subject>Gene regulation</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genetic testing</subject><subject>Genome, Bacterial</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotypes</subject><subject>Health aspects</subject><subject>Hospitals</subject><subject>Humans</subject><subject>Infectious diseases</subject><subject>Medicine</subject><subject>Microbiology</subject><subject>Multilocus Sequence Typing</subject><subject>Nosocomial infection</subject><subject>Nosocomial infections</subject><subject>Pathogenesis</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>RNA, Ribosomal, 16S - classification</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><subject>Virulence factors</subject><subject>Virulence Factors - 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Ross</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-01-24</date><risdate>2013</risdate><volume>8</volume><issue>1</issue><spage>e54287</spage><epage>e54287</epage><pages>e54287-e54287</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Acinetobacter baumannii is an emergent and global nosocomial pathogen. In addition to A. baumannii, other Acinetobacter species, especially those in the Acinetobacter calcoaceticus-baumannii (Acb) complex, have also been associated with serious human infection. Although mechanisms of attachment, persistence on abiotic surfaces, and pathogenesis in A. baumannii have been identified, the genetic mechanisms that explain the emergence of A. baumannii as the most widespread and virulent Acinetobacter species are not fully understood. Recent whole genome sequencing has provided insight into the phylogenetic structure of the genus Acinetobacter. However, a global comparison of genomic features between Acinetobacter spp. has not been described in the literature. In this study, 136 Acinetobacter genomes, including 67 sequenced in this study, were compared to identify the acquisition and loss of genes in the expansion of the Acinetobacter genus. A whole genome phylogeny confirmed that A. baumannii is a monophyletic clade and that the larger Acb complex is also a well-supported monophyletic group. The whole genome phylogeny provided the framework for a global genomic comparison based on a blast score ratio (BSR) analysis. The BSR analysis demonstrated that specific genes have been both lost and acquired in the evolution of A. baumannii. In addition, several genes associated with A. baumannii pathogenesis were found to be more conserved in the Acb complex, and especially in A. baumannii, than in other Acinetobacter genomes; until recently, a global analysis of the distribution and conservation of virulence factors across the genus was not possible. The results demonstrate that the acquisition of specific virulence factors has likely contributed to the widespread persistence and virulence of A. baumannii. The identification of novel features associated with transcriptional regulation and acquired by clades in the Acb complex presents targets for better understanding the evolution of pathogenesis and virulence in the expansion of the genus.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23365658</pmid><doi>10.1371/journal.pone.0054287</doi><tpages>e54287</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | PloS one, 2013-01, Vol.8 (1), p.e54287-e54287 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1327799956 |
| source | Public Library of Science (PLoS) Journals Open Access; MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Acinetobacter Acinetobacter - classification Acinetobacter - genetics Acinetobacter - isolation & purification Acinetobacter - pathogenicity Acinetobacter baumannii Acinetobacter baumannii - classification Acinetobacter baumannii - genetics Acinetobacter baumannii - isolation & purification Acinetobacter baumannii - pathogenicity Acinetobacter calcoaceticus Acinetobacter Infections - microbiology Antimicrobial agents Bacterial Proteins - classification Bacterial Proteins - genetics Base Sequence Biochemistry Biofilms Biological Evolution Biology Chromosome Mapping Chromosomes, Bacterial - genetics Conservation Deoxyribonucleic acid DNA Epidemiology Evolution Evolutionary genetics Gene regulation Gene sequencing Genes Genetic aspects Genetic testing Genome, Bacterial Genomes Genomics Genotypes Health aspects Hospitals Humans Infectious diseases Medicine Microbiology Multilocus Sequence Typing Nosocomial infection Nosocomial infections Pathogenesis Pathogens Phylogeny RNA, Ribosomal, 16S - classification RNA, Ribosomal, 16S - genetics Transcription Transcription (Genetics) Virulence Virulence (Microbiology) Virulence factors Virulence Factors - classification Virulence Factors - genetics |
| title | Evolution of a pathogen: a comparative genomics analysis identifies a genetic pathway to pathogenesis in Acinetobacter |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-28T23%3A22%3A08IST&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=Evolution%20of%20a%20pathogen:%20a%20comparative%20genomics%20analysis%20identifies%20a%20genetic%20pathway%20to%20pathogenesis%20in%20Acinetobacter&rft.jtitle=PloS%20one&rft.au=Sahl,%20Jason%20W&rft.date=2013-01-24&rft.volume=8&rft.issue=1&rft.spage=e54287&rft.epage=e54287&rft.pages=e54287-e54287&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0054287&rft_dat=%3Cgale_plos_%3EA478023261%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=1327799956&rft_id=info:pmid/23365658&rft_galeid=A478023261&rft_doaj_id=oai_doaj_org_article_782037bfff984c298cabe2da415766e5&rfr_iscdi=true |