Dataset Information

Distribution and Genetic Characteristics of SXT/R391 Integrative Conjugative Elements in Shewanella spp. From China.

ABSTRACT: The genus Shewanella consists of facultatively anaerobic Gram-negative bacteria, which are regarded as potential agents of food contamination and opportunistic human pathogens. Information about the distribution and genetic characteristics of SXT/R391 integrative conjugative elements (ICEs) in Shewanella species is limited. Here, 91 Shewanella strains collected from diverse samples in China were studied for the presence of SXT/R391 ICEs. Three positive strains, classified as Shewanella upenei, were obtained from patients and water from a local mill. In light of their close clonal relationships and high sequence similarity, a representative ICE was selected and designated ICESupCHN110003. The BLASTn searches against GenBank showed that ICEVchBan5 was most closely related to ICESupCHN110003, with the coverage of 76% and identity of 99%. The phylogenetic tree of concatenated core genes demonstrated that ICESupCHN110003 formed a distinct branch outside the cluster comprising ICEValA056-1, ICEPmiCHN2410, and ICEPmiChn1. Comparison of the genetic structures revealed that ICESupCHN110003 encoded uncommon genes in hotspots, such as specific type III restriction-modification system, conferring adaptive functions to the host. Based on the low coverage in the sequence analysis, independent clade in the phylogenetic tree, and unique inserted fragments in hotspots, ICESupCHN110003 represented a novel SXT/R391 element, which widened the list of ICEs. Furthermore, the antibiotic resistance genes floR, strA, strB, and sul2 in ICESupCHN110003 and resistance to multiple drugs of the positive isolates were detected. A cross-species transfer capability of the SXT/R391 ICEs was also discovered. In summary, it is necessary to reinforce continuous surveillance of SXT/R391 ICEs in the genus Shewanella.

SUBMITTER: Fang Y

PROVIDER: S-EPMC5958206 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Distribution and Genetic Characteristics of SXT/R391 Integrative Conjugative Elements in Shewanella spp. From China.

Fang Yujie Y Wang Yonglu Y Li Zhenpeng Z Liu Zongdong Z Li Xinyue X Diao Baowei B Kan Biao B Wang Duochun D

Frontiers in microbiology 20180511

The genus Shewanella consists of facultatively anaerobic Gram-negative bacteria, which are regarded as potential agents of food contamination and opportunistic human pathogens. Information about the distribution and genetic characteristics of SXT/R391 integrative conjugative elements (ICEs) in Shewanella species is limited. Here, 91 Shewanella strains collected from diverse samples in China were studied for the presence of SXT/R391 ICEs. Three positive strains, classified as ...[more]

PMID: 29867831

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Project description:Integrative and conjugative elements (ICEs) of the SXT/R391 family are key drivers of the spread of antibiotic resistance in Vibrio cholerae, the infectious agent of cholera, and other pathogenic bacteria. The SXT/R391 family of ICEs was defined based on the conservation of a core set of 52 genes and site-specific integration into the 5' end of the chromosomal gene prfC Hence, the integrase gene int has been intensively used as a marker to detect SXT/R391 ICEs in clinical isolates. ICEs sharing most core genes but differing by their integration site and integrase gene have been recently reported and excluded from the SXT/R391 family. Here we explored the prevalence and diversity of atypical ICEs in GenBank databases and their relationship with typical SXT/R391 ICEs. We found atypical ICEs in V. cholerae isolates that predate the emergence and expansion of typical SXT/R391 ICEs in the mid-1980s in seventh-pandemic toxigenic V. cholerae strains O1 and O139. Our analyses revealed that while atypical ICEs are not associated with antibiotic resistance genes, they often carry cation efflux pumps, suggesting heavy metal resistance. Atypical ICEs constitute a polyphyletic group likely because of occasional recombination events with typical ICEs. Furthermore, we show that the alternative integration and excision genes of atypical ICEs remain under the control of SetCD, the main activator of the conjugative functions of SXT/R391 ICEs. Together, these observations indicate that substitution of the integration/excision module and change of specificity of integration do not preclude atypical ICEs from inclusion into the SXT/R391 family.IMPORTANCEVibrio cholerae is the causative agent of cholera, an acute intestinal infection that remains to this day a world public health threat. Integrative and conjugative elements (ICEs) of the SXT/R391 family have played a major role in spreading antimicrobial resistance in seventh-pandemic V. cholerae but also in several species of Enterobacteriaceae Most epidemiological surveys use the integrase gene as a marker to screen for SXT/R391 ICEs in clinical or environmental strains. With the recent reports of closely related elements that carry an alternative integrase gene, it became urgent to investigate whether ICEs that have been left out of the family are a liability for the accuracy of such screenings. In this study, based on comparative genomics, we broaden the SXT/R391 family of ICEs to include atypical ICEs that are often associated with heavy metal resistance.

Project description:UNLABELLED:SXT-R391 Integrative conjugative elements (ICEs) are self-transmissible mobile genetic elements able to confer multidrug resistance and other adaptive features to bacterial hosts, including Vibrio cholerae, the causative agent of cholera. ICEs are arranged in a mosaic genetic structure composed of a conserved backbone interspersed with variable DNA clusters located in conserved hot spots. In this study, we investigated ICE acquisition and subsequent microevolution in pandemic V. cholerae. Ninety-six ICEs were retrieved from publicly available sequence databases from V. cholerae clinical strains and were compared to a set of reference ICEs. Comparative genomics highlighted the existence of five main ICE groups with a distinct genetic makeup, exemplified by ICEVchInd5, ICEVchMoz10, SXT, ICEVchInd6, and ICEVchBan11. ICEVchInd5 (the most frequent element, represented by 70 of 96 elements analyzed) displayed no sequence rearrangements and was characterized by 46 single nucleotide polymorphisms (SNPs). SNP analysis revealed that recent inter-ICE homologous recombination between ICEVchInd5 and other ICEs circulating in gammaproteobacteria generated ICEVchMoz10, ICEVchInd6, and ICEVchBan11. Bayesian phylogenetic analyses indicated that ICEVchInd5 and SXT were independently acquired by the current pandemic V. cholerae O1 and O139 lineages, respectively, within a period of only a few years. IMPORTANCE:SXT-R391 ICEs have been recognized as key vectors of antibiotic resistance in the seventh-pandemic lineage of V. cholerae, which remains a major cause of mortality and morbidity on a global scale. ICEs were acquired only recently in this clade and are acknowledged to be major contributors to horizontal gene transfer and the acquisition of new traits in bacterial species. We have reconstructed the temporal dynamics of SXT-R391 ICE acquisition and spread and have identified subsequent recombination events generating significant diversity in ICEs currently circulating among V. cholerae clinical strains. Our results showed that acquisition of SXT-R391 ICEs provided the V. cholerae seventh-pandemic lineage not only with a multidrug resistance phenotype but also with a powerful molecular tool for rapidly accessing the pan-genome of a large number of gammaproteobacteria.

Project description:BackgroundThe emergence, resurgence and spread of human food-borne pathogenic Vibrios are one of the major contributors to disease burden and mortality particularly in developing countries with disputable sanitary conditions. Previous research on pathogenic Vibrio cholerae and Vibrio parahaemolitycus derived from clinical samples has proposed links between acquisition of virulence and multiple drug resistance traits and intercellular transmissibility of mobile genetic elements in the environment. To date, very few information is available on environmental Vibrio isolates. In this study, we characterized eleven Vibrio strains bearing the SXT/R391-like integrative and conjugative elements (ICEs) derived from aquatic products and environment in the Yangtze River Estuary, China.ResultsThe eleven Vibrio strains were isolated in 2010 to 2011, and taxonomically identified, which included six Vibrio cholerae, three Vibrio parahaemolyticus, one Vibrio alginolyticus and one Vibrio natriegens. Most of the strains displayed strong resistance phenotypes to ampicillin, mercury and chromium. The majority of their ICEs, which belong to S and R exclusion system groups, contain ICEs-chromosome junction sequences and highly conserved core-genes required for ICE transfer. However, comparative sequence analysis uncovered interesting diversity in their mosaic accessory gene structures, which carry many novel genes that have not been described in any known ICEs to date. In addition, antibiotic resistance was transmitted by ICEVchChn6 and ICEVpaChn1 from V. cholerae, V. parahaemolyticus to E. coli MG1655 via conjugation, respectively. Our data also revealed that the ICEs characterized in this study are phylogenetically distant from most of the SXT/R391 ICEs reported previously, which may represent a novel cluster likely shaped by the ecological environment in the Yangtze River Estuary, China.ConclusionsThis study constitutes the first investigation of ICEs-positive Vibrio spp. in the Yangze River Estuary, China. The newly identified ICEs were characterized with mosaic accessory gene structures and many novel genes. The results demonstrated self-transmissibility of antibiotic resistance mediated by two of the ICEs from V. cholerae, V. parahaemolyticus to E. coli via conjugation, respectively. Our results also revealed that the ICEs examined in this study may represent a novel cluster in the SXT/R391 family.

Dataset Information

Distribution and Genetic Characteristics of SXT/R391 Integrative Conjugative Elements in Shewanella spp. From China.

Publications

Distribution and Genetic Characteristics of SXT/R391 Integrative Conjugative Elements in <i>Shewanella</i> spp. From China.

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