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Analysis of Acinetobacter P-type type IV secretion system-encoding plasmid diversity uncovers extensive secretion system conservation and diverse antibiotic resistance determinants
is globally recognized as a multi-drug-resistant pathogen of critical concern due to its capacity for horizontal gene transfer and resistance to antibiotics. Phylogenetically diverse species mediate human infection, including many considered as important emerging pathogens. While globally recognized...
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Published in: | Antimicrobial agents and chemotherapy 2024-12, Vol.68 (12), p.e0103824 |
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description | is globally recognized as a multi-drug-resistant pathogen of critical concern due to its capacity for horizontal gene transfer and resistance to antibiotics. Phylogenetically diverse
species mediate human infection, including many considered as important emerging pathogens. While globally recognized as a pathogen of concern, pathogenesis mechanisms are poorly understood. P-type type IV secretion systems (T4SSs) represent important drivers of pathogen evolution, responsible for horizontal gene transfer and secretion of proteins that mediate host-pathogen interactions, contributing to pathogen survival, antibiotic resistance, virulence, and biofilm formation. Genes encoding a P-type T4SS were previously identified on plasmids harboring the carbapenemase gene
in several clinically problematic
; however, their prevalence among the genus, geographical distribution, the conservation of T4SS proteins, and full capacity for resistance genes remain unclear. Using systematic analyses, we show that these plasmids belong to a group of 53 P-type T4SS-encoding plasmids in 20 established
species, the majority of clinical relevance, including diverse
sequence types and one strain of
. The strains were globally distributed in 14 countries spanning five continents, and the conjugative operon's T4SS proteins were highly conserved in most plasmids. A high proportion of plasmids harbored resistance genes, with 17 different genes spanning seven drug classes. Collectively, this demonstrates that P-type T4SS-encoding plasmids are more widespread among the
genus than previously anticipated, including strains of both clinical and environmental importance. This research provides insight into the spread of resistance genes among
and highlights a group of plasmids of importance for future surveillance. |
doi_str_mv | 10.1128/aac.01038-24 |
format | article |
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species mediate human infection, including many considered as important emerging pathogens. While globally recognized as a pathogen of concern, pathogenesis mechanisms are poorly understood. P-type type IV secretion systems (T4SSs) represent important drivers of pathogen evolution, responsible for horizontal gene transfer and secretion of proteins that mediate host-pathogen interactions, contributing to pathogen survival, antibiotic resistance, virulence, and biofilm formation. Genes encoding a P-type T4SS were previously identified on plasmids harboring the carbapenemase gene
in several clinically problematic
; however, their prevalence among the genus, geographical distribution, the conservation of T4SS proteins, and full capacity for resistance genes remain unclear. Using systematic analyses, we show that these plasmids belong to a group of 53 P-type T4SS-encoding plasmids in 20 established
species, the majority of clinical relevance, including diverse
sequence types and one strain of
. The strains were globally distributed in 14 countries spanning five continents, and the conjugative operon's T4SS proteins were highly conserved in most plasmids. A high proportion of plasmids harbored resistance genes, with 17 different genes spanning seven drug classes. Collectively, this demonstrates that P-type T4SS-encoding plasmids are more widespread among the
genus than previously anticipated, including strains of both clinical and environmental importance. This research provides insight into the spread of resistance genes among
and highlights a group of plasmids of importance for future surveillance.</description><identifier>ISSN: 0066-4804</identifier><identifier>ISSN: 1098-6596</identifier><identifier>EISSN: 1098-6596</identifier><identifier>DOI: 10.1128/aac.01038-24</identifier><identifier>PMID: 39494882</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Acinetobacter - drug effects ; Acinetobacter - genetics ; Acinetobacter baumannii - drug effects ; Acinetobacter baumannii - genetics ; Acinetobacter Infections - microbiology ; Anti-Bacterial Agents - pharmacology ; Antimicrobial Chemotherapy ; Bacterial Proteins - genetics ; beta-Lactamases - genetics ; Drug Resistance, Multiple, Bacterial - genetics ; Epidemiology and Surveillance ; Gene Transfer, Horizontal ; Humans ; Microbial Sensitivity Tests ; Phylogeny ; Plasmids - genetics ; Type IV Secretion Systems - genetics</subject><ispartof>Antimicrobial agents and chemotherapy, 2024-12, Vol.68 (12), p.e0103824</ispartof><rights>Copyright © 2024 Oke et al.</rights><rights>Copyright © 2024 Oke et al. 2024 Oke et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a306t-49a0a0ac963fa3f3df472eb03bda6c9eef453284281c05257b11159f09e926133</cites><orcidid>0000-0003-4340-7778</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/aac.01038-24$$EPDF$$P50$$Gasm2$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/aac.01038-24$$EHTML$$P50$$Gasm2$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3174,27903,27904,52730,52731,52732</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39494882$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Carattoli, Alessandra</contributor><creatorcontrib>Oke, Mosopefoluwa T</creatorcontrib><creatorcontrib>Martz, Kailey</creatorcontrib><creatorcontrib>Mocăniță, Mădălina</creatorcontrib><creatorcontrib>Knezevic, Sara</creatorcontrib><creatorcontrib>D'Costa, Vanessa M</creatorcontrib><title>Analysis of Acinetobacter P-type type IV secretion system-encoding plasmid diversity uncovers extensive secretion system conservation and diverse antibiotic resistance determinants</title><title>Antimicrobial agents and chemotherapy</title><addtitle>Antimicrob Agents Chemother</addtitle><addtitle>Antimicrob Agents Chemother</addtitle><description>is globally recognized as a multi-drug-resistant pathogen of critical concern due to its capacity for horizontal gene transfer and resistance to antibiotics. Phylogenetically diverse
species mediate human infection, including many considered as important emerging pathogens. While globally recognized as a pathogen of concern, pathogenesis mechanisms are poorly understood. P-type type IV secretion systems (T4SSs) represent important drivers of pathogen evolution, responsible for horizontal gene transfer and secretion of proteins that mediate host-pathogen interactions, contributing to pathogen survival, antibiotic resistance, virulence, and biofilm formation. Genes encoding a P-type T4SS were previously identified on plasmids harboring the carbapenemase gene
in several clinically problematic
; however, their prevalence among the genus, geographical distribution, the conservation of T4SS proteins, and full capacity for resistance genes remain unclear. Using systematic analyses, we show that these plasmids belong to a group of 53 P-type T4SS-encoding plasmids in 20 established
species, the majority of clinical relevance, including diverse
sequence types and one strain of
. The strains were globally distributed in 14 countries spanning five continents, and the conjugative operon's T4SS proteins were highly conserved in most plasmids. A high proportion of plasmids harbored resistance genes, with 17 different genes spanning seven drug classes. Collectively, this demonstrates that P-type T4SS-encoding plasmids are more widespread among the
genus than previously anticipated, including strains of both clinical and environmental importance. This research provides insight into the spread of resistance genes among
and highlights a group of plasmids of importance for future surveillance.</description><subject>Acinetobacter - drug effects</subject><subject>Acinetobacter - genetics</subject><subject>Acinetobacter baumannii - drug effects</subject><subject>Acinetobacter baumannii - genetics</subject><subject>Acinetobacter Infections - microbiology</subject><subject>Anti-Bacterial Agents - pharmacology</subject><subject>Antimicrobial Chemotherapy</subject><subject>Bacterial Proteins - genetics</subject><subject>beta-Lactamases - genetics</subject><subject>Drug Resistance, Multiple, Bacterial - genetics</subject><subject>Epidemiology and Surveillance</subject><subject>Gene Transfer, Horizontal</subject><subject>Humans</subject><subject>Microbial Sensitivity Tests</subject><subject>Phylogeny</subject><subject>Plasmids - genetics</subject><subject>Type IV Secretion Systems - genetics</subject><issn>0066-4804</issn><issn>1098-6596</issn><issn>1098-6596</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp1Ul1vFCEUJcbGrtU3nw2PmjgtX8PCk9k0fjRp0j6or4Rh7lSaGViB2Tj_yx8o3W0bjTEkcLnn3MOFA0KvKDmllKkza90poYSrhoknaEWJVo1stXyKVoRI2QhFxDF6nvMtqftWk2fomGuhhVJshX5tgh2X7DOOA944H6DEzroCCV83ZdkC3k8X33AGl6D4GHBecoGpgeBi78MN3o42T77Hvd9Byr4seK7QXYzhZ4GQa_6fcuxiyJB2dp-z4aEcalx852PxDieonRUbHOAeak-TDxXNL9DRYMcML-_XE_T144cv55-by6tPF-eby8ZyIksjtCV1OC35YPnA-0GsGXSEd72VTgMMouVMCaaoIy1r1x2ltNUD0aCZpJyfoPcH3e3cTdA7CCXZ0WyTn2xaTLTe_I0E_93cxJ2hVFLNW1oV3twrpPhjhlzM5LODcbQB4pwNp4wrsiZKVuq7A9WlmHOC4fEcSsyd06Y6bfZOGyYq_e2BXt-emds4p2pk_h_39Z_3eBR--Ab8N4FuuF0</recordid><startdate>20241205</startdate><enddate>20241205</enddate><creator>Oke, Mosopefoluwa T</creator><creator>Martz, Kailey</creator><creator>Mocăniță, Mădălina</creator><creator>Knezevic, Sara</creator><creator>D'Costa, Vanessa M</creator><general>American Society for Microbiology</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4340-7778</orcidid></search><sort><creationdate>20241205</creationdate><title>Analysis of Acinetobacter P-type type IV secretion system-encoding plasmid diversity uncovers extensive secretion system conservation and diverse antibiotic resistance determinants</title><author>Oke, Mosopefoluwa T ; Martz, Kailey ; Mocăniță, Mădălina ; Knezevic, Sara ; D'Costa, Vanessa M</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a306t-49a0a0ac963fa3f3df472eb03bda6c9eef453284281c05257b11159f09e926133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acinetobacter - drug effects</topic><topic>Acinetobacter - genetics</topic><topic>Acinetobacter baumannii - drug effects</topic><topic>Acinetobacter baumannii - genetics</topic><topic>Acinetobacter Infections - microbiology</topic><topic>Anti-Bacterial Agents - pharmacology</topic><topic>Antimicrobial Chemotherapy</topic><topic>Bacterial Proteins - genetics</topic><topic>beta-Lactamases - genetics</topic><topic>Drug Resistance, Multiple, Bacterial - genetics</topic><topic>Epidemiology and Surveillance</topic><topic>Gene Transfer, Horizontal</topic><topic>Humans</topic><topic>Microbial Sensitivity Tests</topic><topic>Phylogeny</topic><topic>Plasmids - genetics</topic><topic>Type IV Secretion Systems - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oke, Mosopefoluwa T</creatorcontrib><creatorcontrib>Martz, Kailey</creatorcontrib><creatorcontrib>Mocăniță, Mădălina</creatorcontrib><creatorcontrib>Knezevic, Sara</creatorcontrib><creatorcontrib>D'Costa, Vanessa M</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Antimicrobial agents and chemotherapy</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oke, Mosopefoluwa T</au><au>Martz, Kailey</au><au>Mocăniță, Mădălina</au><au>Knezevic, Sara</au><au>D'Costa, Vanessa M</au><au>Carattoli, Alessandra</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Analysis of Acinetobacter P-type type IV secretion system-encoding plasmid diversity uncovers extensive secretion system conservation and diverse antibiotic resistance determinants</atitle><jtitle>Antimicrobial agents and chemotherapy</jtitle><stitle>Antimicrob Agents Chemother</stitle><addtitle>Antimicrob Agents Chemother</addtitle><date>2024-12-05</date><risdate>2024</risdate><volume>68</volume><issue>12</issue><spage>e0103824</spage><pages>e0103824-</pages><issn>0066-4804</issn><issn>1098-6596</issn><eissn>1098-6596</eissn><abstract>is globally recognized as a multi-drug-resistant pathogen of critical concern due to its capacity for horizontal gene transfer and resistance to antibiotics. Phylogenetically diverse
species mediate human infection, including many considered as important emerging pathogens. While globally recognized as a pathogen of concern, pathogenesis mechanisms are poorly understood. P-type type IV secretion systems (T4SSs) represent important drivers of pathogen evolution, responsible for horizontal gene transfer and secretion of proteins that mediate host-pathogen interactions, contributing to pathogen survival, antibiotic resistance, virulence, and biofilm formation. Genes encoding a P-type T4SS were previously identified on plasmids harboring the carbapenemase gene
in several clinically problematic
; however, their prevalence among the genus, geographical distribution, the conservation of T4SS proteins, and full capacity for resistance genes remain unclear. Using systematic analyses, we show that these plasmids belong to a group of 53 P-type T4SS-encoding plasmids in 20 established
species, the majority of clinical relevance, including diverse
sequence types and one strain of
. The strains were globally distributed in 14 countries spanning five continents, and the conjugative operon's T4SS proteins were highly conserved in most plasmids. A high proportion of plasmids harbored resistance genes, with 17 different genes spanning seven drug classes. Collectively, this demonstrates that P-type T4SS-encoding plasmids are more widespread among the
genus than previously anticipated, including strains of both clinical and environmental importance. This research provides insight into the spread of resistance genes among
and highlights a group of plasmids of importance for future surveillance.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>39494882</pmid><doi>10.1128/aac.01038-24</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0003-4340-7778</orcidid><oa>free_for_read</oa></addata></record> |
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source | American Society for Microbiology Journals |
subjects | Acinetobacter - drug effects Acinetobacter - genetics Acinetobacter baumannii - drug effects Acinetobacter baumannii - genetics Acinetobacter Infections - microbiology Anti-Bacterial Agents - pharmacology Antimicrobial Chemotherapy Bacterial Proteins - genetics beta-Lactamases - genetics Drug Resistance, Multiple, Bacterial - genetics Epidemiology and Surveillance Gene Transfer, Horizontal Humans Microbial Sensitivity Tests Phylogeny Plasmids - genetics Type IV Secretion Systems - genetics |
title | Analysis of Acinetobacter P-type type IV secretion system-encoding plasmid diversity uncovers extensive secretion system conservation and diverse antibiotic resistance determinants |
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