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HutZ is required for biofilm formation and contributes to the pathogenicity of Edwardsiella piscicida.

ABSTRACT: Edwardsiella piscicida is a severe fish pathogen. Haem utilization systems play an important role in bacterial adversity adaptation and pathogenicity. In this study, a speculative haem utilization protein, HutZEp, was characterized in E. piscicida. hutZEp is encoded with two other genes, hutW and hutX, in an operon that is similar to the haem utilization operon hutWXZ identified in V. cholerae. However, protein activity analysis showed that HutZEp is probably not related to hemin utilization. To explore the biological role of HutZEp, a markerless hutZEp in-frame mutant strain, TX01?hutZ, was constructed. Deletion of hutZEp did not significantly affect bacterial growth in normal medium, in iron-deficient conditions, or in the presence of haem but significantly retarded bacterial biofilm growth. The expression of known genes related to biofilm growth was not affected by hutZEp deletion, which indicated that HutZEp was probably a novel factor promoting biofilm formation in E. piscicida. Compared to the wild-type TX01, TX01?hutZ exhibited markedly compromised tolerance to acid stress and host serum stress. Pathogenicity analysis showed that inactivation of hutZEp significantly impaired the ability of E. piscicida to invade and reproduce in host cells and to infect host tissue. In contrast to TX01, TX01?hutZ was defective in blocking host macrophage activation. The expression of hutZEp was directly regulated by the ferric uptake regulator Fur. This study is the first functional characterization of HutZ in a fish pathogen, and these findings suggested that HutZEp is essential for E. piscicida biofilm formation and contributes to host infection.

SUBMITTER: Shi YJ

PROVIDER: S-EPMC6775658 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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HutZ is required for biofilm formation and contributes to the pathogenicity of Edwardsiella piscicida.

Shi Yan-Jie YJ Fang Qing-Jian QJ Huang Hui-Qin HQ Gong Chun-Guang CG Hu Yong-Hua YH

Veterinary research 20191002 1

Edwardsiella piscicida is a severe fish pathogen. Haem utilization systems play an important role in bacterial adversity adaptation and pathogenicity. In this study, a speculative haem utilization protein, HutZEp, was characterized in E. piscicida. hutZEp is encoded with two other genes, hutW and hutX, in an operon that is similar to the haem utilization operon hutWXZ identified in V. cholerae. However, protein activity analysis showed that HutZEp is probably not ...[more]

PMID: 31578154

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Project description:Edwardsiella piscicida is found to be an important facultative intracellular pathogen with a broad host range. These organisms can replicate and survive within host macrophages to escape from the subversion of the immune defense. E. piscicida-macrophage interaction is very important in determining the outcome of edwardsiellasis. As an effector protein of E. piscicida T6SS, EvpP has been determined to be a very important virulence factor for E. piscicida, although its precise role in E. piscicida-macrophage interactions is not yet clear. In this study, the roles of EvpP in E. piscicida-macrophage interactions were characterized. Here, we constructed the deletion mutants of evpP (?evpP) and complementation (?evpP-C) by the allelic exchange method. Compared to wild type strain (WT), ?evpP was found to be attenuated for growth within macrophages. In line with this observation, we found its survival capacity was lower than WT under oxidative and acid stress in vitro, which simulate conditions encountered in host macrophages. Attenuation of ?evpP also correlated with enhanced activation of macrophages, as reflected by augmented NO production in ?evpP-treated macrophages. Moreover, compared to WT, ?evpP induced markedly increased apoptosis of macrophages, characterized by increased Annexin V binding and the activation of cleaved caspase-3. These findings provided strong evidence that EvpP is involved in the process of E. piscicida-macrophage interactions and is required for its survival and replication in macrophages. Thus, we propose that EvpP might be an important factor that controlling the fate of E. piscicida inside macrophages. To further exploring the underlying mechanism of EvpP action, the cDNA library was constructed from E. piscicida-infected macrophages and a yeast two-hybrid screen was performed to search for cellular proteins interacting with EvpP. Ribosomal protein S5 (RPS5) was identified as a target of EvpP. Furthermore, the interaction was validated with co-immunoprecipitation assay. This result implies that the observed effect of EvpP on macrophages might be related to RPS5-mediated regulation, contributing to a better understanding of the mechanisms of EvpP involved in E. piscicida-macrophage interactions.

Project description:Edwardsiella ictaluri and Edwardsiella piscicida are important fish pathogens affecting cultured and wild fish worldwide. To investigate the genome-level differences and similarities between catfish-adapted strains in these two species, the complete E. ictaluri 93-146 and E. piscicida C07-087 genomes were evaluated by applying comparative genomics analysis. All available complete (10) and non-complete (19) genomes from five Edwardsiella species were also included in a systematic analysis. Average nucleotide identity and core-genome phylogenetic tree analyses indicated that the five Edwardsiella species were separated from each other. Pan-/core-genome analyses for the 29 strains from the five species showed that genus Edwardsiella members have 9474 genes in their pan genome, while the core genome consists of 1421 genes. Orthology cluster analysis showed that E. ictaluri and E. piscicida genomes have the greatest number of shared clusters. However, E. ictaluri and E. piscicida also have unique features; for example, the E. ictaluri genome encodes urease enzymes and cytochrome o ubiquinol oxidase subunits, whereas E. piscicida genomes encode tetrathionate reductase operons, capsular polysaccharide synthesis enzymes and vibrioferrin-related genes. Additionally, we report for what is believed to be the first time that E. ictaluri 93-146 and three other E. ictaluri genomes encode a type IV secretion system (T4SS), whereas none of the E. piscicida genomes encode this system. Additionally, the E. piscicida C07-087 genome encodes two different type VI secretion systems. E. ictaluri genomes tend to encode more insertion elements, phage regions and genomic islands than E. piscicida. We speculate that the T4SS could contribute to the increased number of mobilome elements in E. ictaluri compared to E. piscicida. Two of the E. piscicida genomes encode full CRISPR-Cas regions, whereas none of the E. ictaluri genomes encode Cas proteins. Overall, comparison of the E. ictaluri and E. piscicida genomes reveals unique features and provides new insights on pathogenicity that may reflect the host adaptation of the two species.

Dataset Information

HutZ is required for biofilm formation and contributes to the pathogenicity of Edwardsiella piscicida.

Publications

HutZ is required for biofilm formation and contributes to the pathogenicity of Edwardsiella piscicida.

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