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Discovery of novel Vibrio cholerae VSP-II genomic islands using comparative genomic analysis.

ABSTRACT: This report describes Vibrio seventh pandemic island II (VSP-II) and three novel variants revealed by comparative genomics of 23 Vibrio cholerae strains and their presence among a large and diverse collection of V. cholerae isolates. Three VSP-II variants were reported previously and our results demonstrate the presence of three novel VSP-II in clinical and environmental V. cholerae marked by major deletions and genetic rearrangements. A new VSP-II cluster was found in the seventh pandemic V. cholerae O1 El Tor strain CIRS101, which is dominant (95%) among the recent (2004-2007) seven pandemic V. cholerae O1 El Tor isolates from two endemic sites, but was not found in older strains from the same region. Two other variants were found in V. cholerae TMA21 and RC385, two environmental strains from coastal Brazil and the Chesapeake Bay, respectively, the latter being prevalent among environmental V. cholerae non-O1/non-O139 and Vibrio mimicus. The results of this study indicate that the VSP-II island has undergone significant rearrangement through a complex evolutionary pathway in V. cholerae. Interestingly, one of the new VSP-II revealed the presence of 'old' and 'new' V. cholerae O1 El Tor pandemic clones circulating in some of the areas where cholera is endemic.

SUBMITTER: Taviani E

PROVIDER: S-EPMC2925232 | biostudies-literature | 2010 Jul

REPOSITORIES: biostudies-literature

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Discovery of novel Vibrio cholerae VSP-II genomic islands using comparative genomic analysis.

Taviani Elisa E Grim Christopher J CJ Choi Jinna J Chun Jongsik J Haley Bradd B Hasan Nur A NA Huq Anwar A Colwell Rita R RR

FEMS microbiology letters 20100506 2

This report describes Vibrio seventh pandemic island II (VSP-II) and three novel variants revealed by comparative genomics of 23 Vibrio cholerae strains and their presence among a large and diverse collection of V. cholerae isolates. Three VSP-II variants were reported previously and our results demonstrate the presence of three novel VSP-II in clinical and environmental V. cholerae marked by major deletions and genetic rearrangements. A new VSP-II cluster was found in the seventh pandemic V. ch ...[more]

PMID: 20528940

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Project description:In recent years genome sequencing has been used to characterize new bacterial species, a method of analysis available as a result of improved methodology and reduced cost. Included in a constantly expanding list of Vibrio species are several that have been reclassified as novel members of the Vibrionaceae. The description of two putative new Vibrio species, Vibrio sp. RC341 and Vibrio sp. RC586 for which we propose the names V. metecus and V. parilis, respectively, previously characterized as non-toxigenic environmental variants of V. cholerae is presented in this study.Based on results of whole-genome average nucleotide identity (ANI), average amino acid identity (AAI), rpoB similarity, MLSA, and phylogenetic analysis, the new species are concluded to be phylogenetically closely related to V. cholerae and V. mimicus. Vibrio sp. RC341 and Vibrio sp. RC586 demonstrate features characteristic of V. cholerae and V. mimicus, respectively, on differential and selective media, but their genomes show a 12 to 15% divergence (88 to 85% ANI and 92 to 91% AAI) compared to the sequences of V. cholerae and V. mimicus genomes (ANI <95% and AAI <96% indicative of separate species). Vibrio sp. RC341 and Vibrio sp. RC586 share 2104 ORFs (59%) and 2058 ORFs (56%) with the published core genome of V. cholerae and 2956 (82%) and 3048 ORFs (84%) with V. mimicus MB-451, respectively. The novel species share 2926 ORFs with each other (81% Vibrio sp. RC341 and 81% Vibrio sp. RC586). Virulence-associated factors and genomic islands of V. cholerae and V. mimicus, including VSP-I and II, were found in these environmental Vibrio spp.Results of this analysis demonstrate these two environmental vibrios, previously characterized as variant V. cholerae strains, are new species which have evolved from ancestral lineages of the V. cholerae and V. mimicus clade. The presence of conserved integration loci for genomic islands as well as evidence of horizontal gene transfer between these two new species, V. cholerae, and V. mimicus suggests genomic islands and virulence factors are transferred between these species.

Project description:Cholera remains a formidable disease, and reports of multidrug-resistant strains of the causative agent Vibrio cholerae have become common during the last 3 decades. The pervasiveness of resistance determinants has largely been ascribed to mobile genetic elements, including SXT/R391 integrative conjugative elements, IncC plasmids, and genomic islands (GIs). Conjugative transfer of IncC plasmids is activated by the master activator AcaCD whose regulatory network extends to chromosomally integrated GIs. MGIVchHai6 is a multidrug resistance GI integrated at the 3' end of trmE (mnmE or thdF) in chromosome 1 of non-O1/non-O139 V. cholerae clinical isolates from the 2010 Haitian cholera outbreak. In the presence of an IncC plasmid expressing AcaCD, MGIVchHai6 excises from the chromosome and transfers at high frequency. Herein, the mechanism of mobilization of MGIVchHai6 GIs by IncC plasmids was dissected. Our results show that AcaCD drives expression of GI-borne genes, including xis and mobIM , involved in excision and mobilization. A 49-bp fragment upstream of mobIM was found to serve as the minimal origin of transfer (oriT) of MGIVchHai6. The direction of transfer initiated at oriT was determined using IncC plasmid-driven mobilization of chromosomal markers via MGIVchHai6. In addition, IncC plasmid-encoded factors, including the relaxase TraI, were found to be required for GI transfer. Finally, in silico exploration of Gammaproteobacteria genomes identified 47 novel related and potentially AcaCD-responsive GIs in 13 different genera. Despite sharing conserved features, these GIs integrate at trmE, yicC, or dusA and carry a diverse cargo of genes involved in phage resistance.IMPORTANCE The increasing association of the etiological agent of cholera, Vibrio cholerae serogroup O1 and O139, with multiple antibiotic resistance threatens to deprive health practitioners of this effective tool. Drug resistance in cholera results mainly from acquisition of mobile genetic elements. Genomic islands conferring multidrug resistance and mobilizable by IncC conjugative plasmids were reported to circulate in non-O1/non-O139 V. cholerae clinical strains isolated from the 2010 Haitian cholera outbreak. As these genomic islands can be transmitted to pandemic V. cholerae serogroups, their mechanism of transmission needed to be investigated. Our research revealed plasmid- and genomic island-encoded factors required for the resistance island excision, mobilization, and integration, as well as regulation of these functions. The discovery of related genomic islands carrying diverse phage resistance genes but lacking antibiotic resistance-conferring genes in a wide range of marine dwelling bacteria suggests that these elements are ancient and recently acquired drug resistance genes.

Project description:The PFGRC has developed a cost effective alternative to complete genome sequencing in order to study the genetic differences between closely related species and/or strains. The comparative genomics approach combines Gene Discovery (GD) and Comparative Genomic Hybridization (CGH) techniques, resulting in the design and production of species microarrays that represent the diversity of a species beyond just the sequenced reference strain(s) used in the initial microarray design. These species arrays may then be used to interrogate hundreds of closely related strains in order to further unravel their evolutionary relationships. Many infectious agents that cause emerging and re-emerging diseases appear to evolve from non-virulent forms. We still lack a clear understanding about the natural history of various microbial agents that cause human infectious diseases and the events leading to acquisition of their pathogenic potential. There have been seven pandemics of V. cholerae throughout the history of the mankind. To date, the world population is still experiencing the seventh one which started in the early 1960s. From almost 200 recognized V. cholerae serotypes, the majority of these epidemics are associated with primarily O1 serotype. However there is evidence that this species is undergoing some phenotypic changes during the last decades. Such examples include shifts in some metabolic pathways used for biotyping, phage sensitivity profiling and the acquisition of plasmids that carry multiple genes conferring antimicrobial resistance. Furthermore, the recent emergence of a non-O1 serotype (‘Bengal strain’, classified serologically as O139) has prompted the experts to think that perhaps this genotype will be the predominant one in the upcoming (eighth) pandemic. Besides the O1 and O139, the non-O1 and non-O139 V. cholerae stains are occasionally associated with other severe forms of gastrointestinal disease in humans. Interestingly, many of these non-canonical strains lack the genes encoding the typical virulence factors for this species such as the Cholera-toxin (ctx) and toxin co-regulated pilus (tcpA). Therefore it has been hypothesized that this group of non-canonical V. cholerae pathogens consist of several sub-clones that elicit disease via unknown virulence determinants and underlying mechanisms. The flow of genetic information within this group motivated us to identify novel genes for the purpose of creating a "species" DNA microarray to better understand the ancestral relationships among its members. Based on preliminary genotyping (MLST, and CGH using a single-genome-based array), 10 diverse V. cholerae and one V. mimicus were selected for sequencing. Sequence information obtained from this project, and from other publicly available sources, led to the development of a comprehensive species microarray for V. cholerae group members. The availability of the V. cholerae species DNA microarray has allowed us to carry out a collaborative CGH genotyping project to validate this microarray as well as understand the phylogenomic relationships among members of V. cholerae group.

Dataset Information

Discovery of novel Vibrio cholerae VSP-II genomic islands using comparative genomic analysis.

Publications

Discovery of novel Vibrio cholerae VSP-II genomic islands using comparative genomic analysis.

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