IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti

ABSTRACT Mobile genetic elements play a pivotal role in the adaptation of bacterial populations, allowing them to rapidly cope with hostile conditions, including the presence of antimicrobial compounds. IncA/C conjugative plasmids (ACPs) are efficient vehicles for dissemination of multidrug resistan...

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Autores principales: Nicolas Carraro, Nicolas Rivard, Daniela Ceccarelli, Rita R. Colwell, Vincent Burrus
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:dfa1cd5071a54bffbc9abde942473c662021-11-15T15:50:18ZIncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti10.1128/mBio.00509-162150-7511https://doaj.org/article/dfa1cd5071a54bffbc9abde942473c662016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00509-16https://doaj.org/toc/2150-7511ABSTRACT Mobile genetic elements play a pivotal role in the adaptation of bacterial populations, allowing them to rapidly cope with hostile conditions, including the presence of antimicrobial compounds. IncA/C conjugative plasmids (ACPs) are efficient vehicles for dissemination of multidrug resistance genes in a broad range of pathogenic species of Enterobacteriaceae. ACPs have sporadically been reported in Vibrio cholerae, the infectious agent of the diarrheal disease cholera. The regulatory network that controls ACP mobility ultimately depends on the transcriptional activation of multiple ACP-borne operons by the master activator AcaCD. Beyond ACP conjugation, AcaCD has also recently been shown to activate the expression of genes located in the Salmonella genomic island 1 (SGI1). Here, we describe MGIVchHai6, a novel and unrelated mobilizable genomic island (MGI) integrated into the 3′ end of trmE in chromosome I of V. cholerae HC-36A1, a non-O1/non-O139 multidrug-resistant clinical isolate recovered from Haiti in 2010. MGIVchHai6 contains a mercury resistance transposon and an integron In104-like multidrug resistance element similar to the one of SGI1. We show that MGIVchHai6 excises from the chromosome in an AcaCD-dependent manner and is mobilized by ACPs. Acquisition of MGIVchHai6 confers resistance to β-lactams, sulfamethoxazole, tetracycline, chloramphenicol, trimethoprim, and streptomycin/spectinomycin. In silico analyses revealed that MGIVchHai6-like elements are carried by several environmental and clinical V. cholerae strains recovered from the Indian subcontinent, as well as from North and South America, including all non-O1/non-O139 clinical isolates from Haiti. IMPORTANCE Vibrio cholerae, the causative agent of cholera, remains a global public health threat. Seventh-pandemic V. cholerae acquired multidrug resistance genes primarily through circulation of SXT/R391 integrative and conjugative elements. IncA/C conjugative plasmids have sporadically been reported to mediate antimicrobial resistance in environmental and clinical V. cholerae isolates. Our results showed that while IncA/C plasmids are rare in V. cholerae populations, they play an important yet insidious role by specifically propagating a new family of genomic islands conferring resistance to multiple antibiotics. These results suggest that nonepidemic V. cholerae non-O1/non-O139 strains bearing these genomic islands constitute a reservoir of transmissible resistance genes that can be propagated by IncA/C plasmids to V. cholerae populations in epidemic geographical areas as well to pathogenic species of Enterobacteriaceae. We recommend future epidemiological surveys take into account the circulation of these genomic islands.Nicolas CarraroNicolas RivardDaniela CeccarelliRita R. ColwellVincent BurrusAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Nicolas Carraro
Nicolas Rivard
Daniela Ceccarelli
Rita R. Colwell
Vincent Burrus
IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti
description ABSTRACT Mobile genetic elements play a pivotal role in the adaptation of bacterial populations, allowing them to rapidly cope with hostile conditions, including the presence of antimicrobial compounds. IncA/C conjugative plasmids (ACPs) are efficient vehicles for dissemination of multidrug resistance genes in a broad range of pathogenic species of Enterobacteriaceae. ACPs have sporadically been reported in Vibrio cholerae, the infectious agent of the diarrheal disease cholera. The regulatory network that controls ACP mobility ultimately depends on the transcriptional activation of multiple ACP-borne operons by the master activator AcaCD. Beyond ACP conjugation, AcaCD has also recently been shown to activate the expression of genes located in the Salmonella genomic island 1 (SGI1). Here, we describe MGIVchHai6, a novel and unrelated mobilizable genomic island (MGI) integrated into the 3′ end of trmE in chromosome I of V. cholerae HC-36A1, a non-O1/non-O139 multidrug-resistant clinical isolate recovered from Haiti in 2010. MGIVchHai6 contains a mercury resistance transposon and an integron In104-like multidrug resistance element similar to the one of SGI1. We show that MGIVchHai6 excises from the chromosome in an AcaCD-dependent manner and is mobilized by ACPs. Acquisition of MGIVchHai6 confers resistance to β-lactams, sulfamethoxazole, tetracycline, chloramphenicol, trimethoprim, and streptomycin/spectinomycin. In silico analyses revealed that MGIVchHai6-like elements are carried by several environmental and clinical V. cholerae strains recovered from the Indian subcontinent, as well as from North and South America, including all non-O1/non-O139 clinical isolates from Haiti. IMPORTANCE Vibrio cholerae, the causative agent of cholera, remains a global public health threat. Seventh-pandemic V. cholerae acquired multidrug resistance genes primarily through circulation of SXT/R391 integrative and conjugative elements. IncA/C conjugative plasmids have sporadically been reported to mediate antimicrobial resistance in environmental and clinical V. cholerae isolates. Our results showed that while IncA/C plasmids are rare in V. cholerae populations, they play an important yet insidious role by specifically propagating a new family of genomic islands conferring resistance to multiple antibiotics. These results suggest that nonepidemic V. cholerae non-O1/non-O139 strains bearing these genomic islands constitute a reservoir of transmissible resistance genes that can be propagated by IncA/C plasmids to V. cholerae populations in epidemic geographical areas as well to pathogenic species of Enterobacteriaceae. We recommend future epidemiological surveys take into account the circulation of these genomic islands.
format article
author Nicolas Carraro
Nicolas Rivard
Daniela Ceccarelli
Rita R. Colwell
Vincent Burrus
author_facet Nicolas Carraro
Nicolas Rivard
Daniela Ceccarelli
Rita R. Colwell
Vincent Burrus
author_sort Nicolas Carraro
title IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti
title_short IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti
title_full IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti
title_fullStr IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti
title_full_unstemmed IncA/C Conjugative Plasmids Mobilize a New Family of Multidrug Resistance Islands in Clinical <named-content content-type="genus-species">Vibrio cholerae</named-content> Non-O1/Non-O139 Isolates from Haiti
title_sort inca/c conjugative plasmids mobilize a new family of multidrug resistance islands in clinical <named-content content-type="genus-species">vibrio cholerae</named-content> non-o1/non-o139 isolates from haiti
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/dfa1cd5071a54bffbc9abde942473c66
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