Dataset Information

Molecular Characterization, Phylogenetic, Expression, and Protective Immunity Analysis of OmpF, a Promising Candidate Immunogen Against Yersinia ruckeri Infection in Channel Catfish.

ABSTRACT: Outer membrane porins, as the major components of Gram-negative bacterial membrane proteins, have been proven to be involved in interactions with the host immune system and potent protective antigen candidates against bacterial infection in fish. Outer membrane porin F (OmpF) is one of the major porins of Yersinia ruckeri (Y. ruckeri), the causative agent of enteric red mouth disease of salmonid and non-salmonid fish. In the present study, the molecular characterization and phylogenetic analysis of OmpF gene was studied, heterogenous expression, immunogenicity and protective immunity of OmpF were systemically evaluated as a subunit vaccine for channel catfish against Y. ruckeri infection. The results showed that OmpF gene was highly conserved among 15 known Yersinia species based on the analysis of conserved motifs, sequences alignment and phylogenetic tree, and was subjected to negative/purifying selection with global dN/dS ratios value of 0.649 throughout the evolution. Besides, OmpF was also identified to have immunogenicity by western blotting and was verified to be located on the surface of Y. ruckeri using cell surface staining and indirect immunofluorescence assays. Moreover, recombinant OmpF (rtOmpF) as a subunit vaccine was injected with commercial adjuvant ISA763, significantly enhanced the immune response by increasing serum antibody levels, lysozyme activity, complement C3 activity, total protein content, SOD activity, immune-related genes expression in the head kidney and spleen, and survival percent of channel catfish against Y. ruckeri infection. Thus, our present results not only enriched the information of molecular characterization and phylogenetics of OmpF, but also demonstrated that OmpF holds promise to be used as a potential antigen against Y. ruckeri infection in fish.

SUBMITTER: Wang E

PROVIDER: S-EPMC6146100 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Molecular Characterization, Phylogenetic, Expression, and Protective Immunity Analysis of OmpF, a Promising Candidate Immunogen Against Yersinia ruckeri Infection in Channel Catfish.

Wang Erlong E Qin Zhenyang Z Yu Zehui Z Ai Xiaohui X Wang Kaiyu K Yang Qian Q Liu Tao T Chen Defang D Geng Yi Y Huang Xiaoli X Ouyang Ping P Lai Weimin W

Frontiers in immunology 20180913

Outer membrane porins, as the major components of Gram-negative bacterial membrane proteins, have been proven to be involved in interactions with the host immune system and potent protective antigen candidates against bacterial infection in fish. Outer membrane porin F (OmpF) is one of the major porins of Yersinia ruckeri (Y. ruckeri), the causative agent of enteric red mouth disease of salmonid and non-salmonid fish. In the present study, the molecular characterization and phyloge ...[more]

PMID: 30271401

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Project description:Yersinia ruckeri is the causative agent of enteric redmouth disease (ERM) which causes economically significant losses in farmed salmonids, especially Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss, Walbaum). However, very little is known about the genetic relationships of disease-causing isolates in these two host species or about factors responsible for disease. Phylogenetic analyses of 16 representative isolates based on the nucleotide sequences of 19 housekeeping genes suggests that pathogenic Atlantic salmon and rainbow trout isolates represent distinct host-specific lineages. However, the apparent phylogenies of certain isolates has been influenced by horizontal gene transfer and recombinational exchange. Splits decomposition analysis demonstrated a net-like phylogeny based on the housekeeping genes, characteristic of recombination. Comparative analysis of the distribution of individual housekeeping gene alleles across the isolates demonstrated evidence of genomic mosaicism and recombinational exchange involving certain Atlantic salmon and rainbow trout isolates. Comparative nucleotide sequence analysis of the key outer membrane protein genes ompA and ompF revealed that the corresponding gene trees were both non-congruent with respect to the housekeeping gene phylogenies providing evidence that horizontal gene transfer has influenced the evolution of both these surface protein-encoding genes. Analysis of inferred amino acid sequence variation in OmpA identified a single variant, OmpA.1, that was present in serotype O1 and O8 isolates representing typical pathogenic strains in rainbow trout and Atlantic salmon, respectively. In particular, the sequence of surface-exposed loop 3 differed by seven amino acids to that of other Y. ruckeri isolates. These findings suggest that positive selection has likely influenced the presence of OmpA.1 in these isolates and that loop 3 may play an important role in virulence. Amino acid sequence variation of OmpF was greater than that of OmpA and was similarly restricted mainly to the surface-exposed loops. Two OmpF variants, OmpF.1 and OmpF.2, were associated with pathogenic rainbow trout and Atlantic salmon isolates, respectively. These OmpF proteins had very similar amino acid sequences suggesting that positive evolutionary pressure has also favoured the selection of these variants in pathogenic strains infecting both species.

Project description:Yersinia ruckeri is the causative agent of enteric redmouth disease (ERM), a serious infection that affects global aquaculture with high economic impact. The present study used whole genome sequences to perform a comparative analysis on 10 Y. ruckeri strains and to explore their genetic relatedness to other members of the genus. Y. ruckeri, Yersinia entomophaga, and Yersinia nurmii formed a species complex that constitutes the most basal lineage of the genus. The results showed that the taxonomy of Y. ruckeri strains is better defined by using a core genome alignment and phylogenetic analysis. The distribution of accessory genes in all Yersinia species revealed the presence of 303 distinctive genes in Y. ruckeri. Of these, 169 genes were distributed in 17 genomic islands potentially involved in the pathogenesis of ERM via (1) encoding virulence factors such as Afp18, Yrp1, phage proteins and (2) improving the metabolic capabilities by enhancing utilization and metabolism of iron, amino acids (specifically, arginine and histidine), and carbohydrates. The genome of Y. ruckeri is highly conserved regarding gene structure, gene layout and functional categorization of genes. It contains various components of mobile genetic elements but lacks the CRISPR-Cas system and possesses a stable set of virulence genes possibly playing a critical role in pathogenicity. Distinct virulence plasmids were exclusively restricted to a specific clonal group of Y. ruckeri (CG4), possibly indicating a selective advantage. Phylogenetic analysis of Y. ruckeri genomes revealed the co-presence of multiple genetically distant lineages of Y. ruckeri strains circulating in Germany. Our results also suggest a possible dissemination of a specific group of strains in the United States, Peru, Germany, and Denmark. In conclusion, this study provides new insights into the taxonomy and evolution of Y. ruckeri and contributes to a better understanding of the pathogenicity of ERM in aquaculture. The genomic analysis presented here offers a framework for the development of more efficient control strategies for this pathogen.

Dataset Information

Molecular Characterization, Phylogenetic, Expression, and Protective Immunity Analysis of OmpF, a Promising Candidate Immunogen Against Yersinia ruckeri Infection in Channel Catfish.

Publications

Molecular Characterization, Phylogenetic, Expression, and Protective Immunity Analysis of OmpF, a Promising Candidate Immunogen Against <i>Yersinia ruckeri</i> Infection in Channel Catfish.

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