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. 2022 Apr;68(2):267-287.
doi: 10.1007/s00294-022-01229-z. Epub 2022 Jan 22.

Prophage-encoded gene VpaChn25_0734 amplifies ecological persistence of Vibrio parahaemolyticus CHN25

Yingwei Xu  1 , Lianzhi Yang  1 , Yaping Wang  1   2 , Zhuoying Zhu  1 , Jizhou Yan  3 , Si Qin  4 , Lanming Chen  5
Affiliations

Prophage-encoded gene VpaChn25_0734 amplifies ecological persistence of Vibrio parahaemolyticus CHN25

Yingwei Xu et al. Curr Genet. 2022 Apr.

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.

Keywords: Foodborne pathogen; Gene deletion and reversion; Prophage; Secretome; Transcriptome; Vibrio parahaemolyticus.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1
Fig. 1
Survival of V. parahaemolyticus CHN25 (WT), ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains at different temperatures. a–c 37 °C (a), 25 °C (b), and 15 °C (c), respectively
Fig. 2
Fig. 2
Survival of the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains in different pH conditions. a–f pH 5.5 (a), pH 6.0 (b), pH 6.5 (c), pH 7.0 (d), pH 7.5 (e), and pH 8.0 (f), respectively
Fig. 3
Fig. 3
Swimming mobility of the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains at different temperatures. a–c 37 °C (a-1–c-1), 25 °C (a-2–c-2), and 15 °C (a-3–c-3), respectively
Fig. 4
Fig. 4
Biofilm formation of the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains in the TSB medium at 37 °C. *p < 0.05; ***p < 0.001 compared with the WT strain
Fig. 5
Fig. 5
Cell membrane permeability and fluidity, and surface hydrophobicity of the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains. a–d Outer and internal membrane permeability (a, b), fluidity (c), and hydrophobicity (d). DPH: 1,6-diphenyl-1,3,5-hexatriene. **p < 0.01 compared with the WT strain
Fig. 6
Fig. 6
The 2D-GE analysis of extracellular proteins of the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains. a–c WT (a); ΔVpaChn25_0734 (543-bp) (b); and ΔVpaChn25_0734-com (543-bp) (c), respectively
Fig. 7
Fig. 7
The viability and apoptosis of Caco-2 cells infected by the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains. (a) Cell viability; and (b) cell apoptosis. **p < 0.01 compared with the WT
Fig. 8
Fig. 8
Thirteen metabolic pathways significantly altered in the ΔVpaChn25_0734 (543-bp) mutant
Fig. 9
Fig. 9
The SEM observation of cell structure of the WT, ΔVpaChn25_0734 (543-bp), and ΔVpaChn25_0734-com (543-bp) strains. a, d WT; b, e ΔVpaChn25_0734; and c, f ΔVpaChn25_0734-com
Fig. 10
Fig. 10
Phylogenetic relationships between the VpaChn25_0734 (543-bp) gene and its homologues
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