Insights into the role of the two-component system pfeS/pfeR in Vibrio harveyi adaptation to host fish blood.

Abstract

Host environments are complex and highly dynamic for bacterial pathogens, requiring rapid and precise response and adaptation for successful systemic infection. In this study, RNA-Seq was used to investigate the transcriptional response of Vibrio harveyi TS-628 during adaptation to yellow grouper (Epinephelus awoara) blood. A total of 1,273 genes were differentially expressed, accounting for 28.35% of the total gene complement, indicating a highly significant metabolic reprogramming of V. harveyi during host adaptation. Genes encoding two-component systems (TCSs) were prominently enriched among the differentially expressed genes (DEGs). Notably, the pfeS/pfeR TCS was consistently up-regulated during adaptation to host blood, mucus, and muscle, suggesting its core role in the host adaptation. Subsequent knockdown of pfeS or pfeR did not affect bacterial growth but altered the expression of iron uptake-related genes, implying a regulatory role of the TCS in maintaining iron homeostasis. Furthermore, both pfeS-RNAi and pfeR-RNAi strains displayed significantly reduced motility, chemotaxis, and biofilm formation, indicating that the pfeS/pfeR system coordinates multiple adaptive traits essential for host colonization. Blood exposure significantly induced chemotaxis and biofilm formation in the wild-type strain, but this inducibility was lost in the knockdown strains, suggesting that the pfeS/pfeR system may function in environmental signal sensing. In conclusion, we hypothesize that during the early stages of infection, pfeS/pfeR mediates metabolic reprogramming in response to environmental cues, thereby regulating iron homeostasis and virulence-related behaviors to promote bacterial adaptation to the host environment and preparing for further dissemination.