Abstract

Vibrio parahaemolyticus is a waterborne pathogen that can cause acute gastroenteritis, wound infection, and septicemia in humans. The molecular basis of its pathogenicity is not yet fully understood. Phages are found most abundantly in aquatic environments and play a critical role in horizontal gene transfer. Nevertheless, current literature on biological roles of prophage-encoded genes remaining in V. parahaemolyticus is rare. In this study, we characterized one such gene VpaChn25_0734 (543-bp) in V. parahaemolyticus CHN25 genome. A deletion mutant ΔVpaChn25_0734 (543-bp) was obtained by homologous recombination, and a revertant ΔVpaChn25_0734-com (543-bp) was also constructed. The ΔVpaChn25_0734 (543-bp) mutant was defective in growth and swimming mobility particularly at lower temperatures and/or pH 7.0–8.5. Cell surface hydrophobicity and biofilm formation were significantly decreased in the ΔVpaChn25_0734 (543-bp) mutant (p < 0.05). Based on the in vitro Caco-2 cell model, the deletion of VpaChn25_0734 (543-bp) gene significantly reduced the cytotoxicity of V. parahaemolyticus CHN25 to human intestinal epithelial cells (p < 0.05). Comparative secretomic and transcriptomic analyses revealed a slightly increased extracellular proteins, and thirteen significantly changed metabolic pathways in the ΔVpaChn25_0734 (543-bp) mutant, showing down-regulated carbon source transport and utilization, biofilm formation, and type II secretion system (p < 0.05), consistent with the observed defective phenotypes. Taken, the prophage-encoded gene VpaChn25_0734 (543-bp) enhanced V. parahaemolyticus CHN25 fitness for survival in the environment and the host. The results in this study facilitate better understanding of pathogenesis and genome evolution of V. parahaemolyticus, the leading sea foodborne pathogen worldwide.

Highlights

  • Vibrio parahaemolyticus is a Gram-negative bacterium that resides in aquatic environments worldwide (Letchumanan et al 2014; Su and Chen 2020)

  • These results indicated that the prophage-encoded VpaChn25_0734 (543bp) gene amplified the environmental persistence of V. parahaemolyticus CHN25

  • We characterized for the first time the prophage-encoded gene VpaChn25_0734 (543-bp) in V. parahaemolyticus CHN25 genome

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Summary

Introduction

Vibrio parahaemolyticus is a Gram-negative bacterium that resides in aquatic environments worldwide (Letchumanan et al 2014; Su and Chen 2020). Outbreaks of human gastroenteritis caused by V. parahaemolyticus occurred in many Asian nations and around the world (Elmahdi et al 2016; Meparambu Prabhakaran et al 2020). A national surveillance of 152,792 patients of all ages with acute diarrhea was administered in 217 hospitals and 93 reference laboratories in 31 provinces of China by the Chinese Center for Diseases Control and Prevention in 2009‒2018 (Wang et al 2021a). Some clinical V. parahaemolyticus strains do not produce the two major toxins but display virulence, indicating that putative toxic determinants exist. Their pathogenicity might be achieved with different strategies employed by different strains (Li et al 2020). It is imperative to identify such risk factors in V. parahaemolyticus to assure food safety and human health

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