Dataset Information

Survival, Virulent Characteristics, and Transcriptomic Analyses of the Pathogenic Vibrio anguillarum Under Starvation Stress.

ABSTRACT: Many bacteria have developed strategies for metamorphosis into sophisticated survival forms to survive extended periods of environmental stress. As a global causative agent of vibriosis in marine fish farming, Vibrio anguillarum (V. anguillarum) can efficiently grow and proliferate under environmental stress, but the specific mechanism is not clear. In the present study, survival, virulent characteristics, and transcriptomic analysis of the V. anguillarum BH1 were performed under starvation stress. The results demonstrated that V. anguillarum was still culturable and showed rippled surface after 6 months of starvation. Starved cells maintained their infectivity in half-smooth tongue sole (Cynoglossus semilaevi). Detection of virulence factors and virulence-associated genes in starved cells showed that the starved strain still produced ?-hemolysis on rabbit blood agar, caseinase, dnase, and gelatinase, and possessed empA, vah1, vah2, vah3, vah4, vah5, rtxA, flaA, flaD, flaE, virC, tonB, mreB, toxR, rpoS, and ftsZ virulence-related genes. In addition, we first reported the RNA-seq study for V. anguillarum with and without starvation treatment for a period of 6 months and emphasized the regulation of gene expression at the whole transcriptional level. It indicated that V. anguillarum expressed 3,089 and 3,072 genes in the control group and starvation stress group, respectively. The differently expressed genes (DEGs) of the starved strain were thereby identified, including 251 up-regulated genes and 272 down-regulated genes in comparison with the non-starved strain. Gene Ontology (GO) analysis and Kyto Encyclopedia Genes and Genomes (KEGG) enrichment analysis of DEGs were also analyzed. GO functional classification revealed that among the significantly regulated genes with known function categories, more genes affiliated with signal transducer activity, molecular transducer activity, and cell communication were significantly up-regulated, and more genes affiliated with cellular macromolecule, cellular component, and structural molecule activity were significantly down-regulated. In addition, the DEGs involved in the pathway of two-component system was significantly up-regulated, and the pathways of ribosome and flagellar assembly were significantly down-regulated. This study provides valuable insight into the survival strategies of V. anguillarum and suggests that a portion of the bacterial populations may remain pathogenic while persisting under starvation stress by up-regulating or down-regulating a series of genes.

SUBMITTER: Gao X

PROVIDER: S-EPMC6250815 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Survival, Virulent Characteristics, and Transcriptomic Analyses of the Pathogenic Vibrio anguillarum Under Starvation Stress.

Gao Xiaojian X Pi Daming D Chen Nan N Li Xixi X Liu Xiaodan X Yang Hui H Wei Wanhong W Zhang Xiaojun X

Frontiers in cellular and infection microbiology 20181116

Many bacteria have developed strategies for metamorphosis into sophisticated survival forms to survive extended periods of environmental stress. As a global causative agent of vibriosis in marine fish farming, Vibrio anguillarum (V. anguillarum) can efficiently grow and proliferate under environmental stress, but the specific mechanism is not clear. In the present study, survival, virulent characteristics, and transcriptomic analysis of the V. anguillarum BH1 were performed ...[more]

PMID: 30505805

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Project description:Non-O1/O139 Vibrio cholerae is a pathogen of various aquatic organisms but requires major self-regulation to overcome environmental stress in the aquatic environment. However, its survival strategies under environmental stress are not well understood. The objective of this study was to describe the survival characteristics and changes in expression of stress resistance-related genes of non-O1/O139 V. cholerae after 6 months of starvation at room temperature. The results demonstrated that starved cells were still viable, exhibited shortened rods and shrinking surface, and maintained virulence to Macrobrachium rosenbergii. To investigate the changes in gene expression in non-O1/O139 V. cholerae under starvation stress, especially those involved in stress resistance, transcriptome profiles of starved and wild-type cells were determined. The differentially expressed genes (DEGs) in starved cells were identified, including 191 upregulated genes and 180 downregulated genes. Among these DEGs, the well-known stress resistance-related genes were upregulated significantly, including rpoS, rpoD, rpoN, rpoE, uspA, uspC, cspD, hslJ, etc. Gene Ontology (GO) analysis of the DEGs demonstrated that environmental adaptation-related categories, such as response to stimulus and signal transduction, were upregulated significantly in the starved cells, while cell motility was downregulated significantly. These DEGs were also enriched into 54 KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways, including biofilm formation, two-component system, quorum sensing, flagellar assembly, bacterial chemotaxis stress resistance-related pathways, etc. The potential existence of long-starved non-O1/O139 V. cholerae bacteria in the aquatic environment may raise new concerns about this devastating pathogen in aquaculture. IMPORTANCE Non-O1/O139 V. cholerae is a causal agent of vibriosis that can be subject to nutrient insufficiency and cause high rates of mortality in aquatic animals. However, its molecular mechanisms of survival in response to starvation stress have been investigated only partially. Here, we demonstrate that under starvation stress, non-O1/O139 V. cholerae can survive over the long term and cause disease by dwarfing of the cell structure, upregulation of a series of stress resistance-related genes, and downregulation of flagellum assembly-related genes. This knowledge can help the development of intervention strategies to control non-O1/O139 V. cholerae infection in aquaculture.

Project description:Vibrio anguillarum is a marine bacterium that can cause vibriosis in many fish and shellfish species, leading to high mortalities and economic losses in aquaculture. Although putative virulence factors have been identified, the mechanism of pathogenesis of V. anguillarum is not fully understood. Here, we analyzed whole-genome sequences of a collection of V. anguillarum strains and compared them to virulence of the strains as determined in larval challenge assays. Previously identified virulence factors were globally distributed among the strains, with some genetic diversity. However, the pan-genome revealed that six out of nine high-virulence strains possessed a unique accessory genome that was attributed to pathogenic genomic islands, prophage-like elements, virulence factors, and a new set of gene clusters involved in biosynthesis, modification, and transport of polysaccharides. In contrast, V. anguillarum strains that were medium to nonvirulent had a high degree of genomic homogeneity. Finally, we found that a phylogeny based on the core genomes clustered the strains with moderate to no virulence, while six out of nine high-virulence strains represented phylogenetically separate clusters. Hence, we suggest a link between genotype and virulence characteristics of Vibrio anguillarum, which can be used to unravel the molecular evolution of V. anguillarum and can also be important from survey and diagnostic perspectives. IMPORTANCE Comparative genome analysis of strains of a pathogenic bacterial species can be a powerful tool to discover acquisition of mobile genetic elements related to virulence. Here, we compared 28 V. anguillarum strains that differed in virulence in fish larval models. By pan-genome analyses, we found that six of nine highly virulent strains had a unique core and accessory genome. In contrast, V. anguillarum strains that were medium to nonvirulent had low genomic diversity. Integration of genomic and phenotypic features provides insights into the evolution of V. anguillarum and can also be important for survey and diagnostic purposes.

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Project description:UnlabelledThe genetic heterogeneity of the close relatives Vibrio anguillarum and Vibrio ordalii, both serious pathogens of fish causing extensive losses in aquaculture, was studied. Eight housekeeping genes, i.e., atpA, ftsZ, gapA, gyrB, mreB, rpoA, topA, and pyrH, were partially sequenced in 116 isolates from diverse fish species and geographical areas. The eight genes appear to be under purifying selection, and the genetic diversity in the total data set was estimated to be 0.767 ± 0.026. Our multilocus sequence analysis (MLSA) scheme identified several widespread clonal complexes and resolved the isolates, for the most part, according to serotype. Serotype O2b isolates from diseased cod in Norway, Ireland, and Scotland were found to be extremely homogeneous. Horizontal gene transfer appears to be fairly common within and between clonal complexes. Taken together, MLSA and in silico DNA-DNA hybridization (DDH) calculations suggest that some isolates previously characterized as V ordalii, i.e., 12B09, FF93, FS144, and FS238, are in fact V. anguillarum isolates. The precise taxonomic situation for two isolates from Atlantic cod that display several traits consistent with V. ordalii, i.e., NVI 5286 and NVI 5918, and a single environmental strain that was previously considered to represent V. ordalii, i.e., FF167, is less clear.ImportanceIt is still being debated whether V. anguillarum and V ordalii represent separate bacterial species. Our study addresses this issue and elucidates the degree of genetic variability within this group of closely related bacteria, based on a substantial number of isolates. Our results clearly illustrate the existence of different populations among putative V ordalii isolates. On the basis of additional full-length genomic analysis, we conclude that most environmental isolates previously identified as V ordalii lie firmly within the species V. anguillarum While bona fide fish-pathogenic V ordalii isolates display a very close genetic relationship with V. anguillarum, they combine a clearly divergent evolutionary pattern with clear phenotypic differences. The study also highlights the need for further characterization of fish-pathogenic isolates from the northern Atlantic region that share phenotypic characteristics with V. ordalii but are genetically closer to V. anguillarum The retention of taxonomic distinctions between the phenotypically different groups of bacteria is of practical advantage to microbial ecologists and veterinarians.

Dataset Information

Survival, Virulent Characteristics, and Transcriptomic Analyses of the Pathogenic Vibrio anguillarum Under Starvation Stress.

Publications

Survival, Virulent Characteristics, and Transcriptomic Analyses of the Pathogenic <i>Vibrio anguillarum</i> Under Starvation Stress.

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