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Pseudomonas plecoglossicida is a Gram-negative bacterium that causes chronic granulomatous diseases in fish. However, the molecular mechanisms underlying its pathogenicity are poorly understood. Here, we identified a novel two-component system (TCS) named PvgAS in P. plecoglossicida , which regulates the expression of genes including the type VI secretion system-1 (T6SS-1), a key virulence factor, as well as the type III secretion system (T3SS) gene cluster and several genes associated with metabolic pathways. We showed that PvgAS is essential for bacterial virulence in large yellow croaker (LYC), an important aquaculture species, by controlling T6SS-1 expression, which is crucial for tissue colonization and intracellular survival. In contrast, T3SS was dispensable for P. plecoglossicida virulence in this model. We also confirmed T6SS-1 gene regulation by PvgAS at the transcriptional and translational levels using RNA-seq, RT-qPCR, lacZ reporter, and western blot assays. Our study reveals a regulatory and functional role of PvgAS in P. plecoglossicida pathogenicity and suggests that PvgAS may be a potential target for new therapeutic interventions against this bacterium. • Identified a novel two-component system PvgAS in Pseudomonas plecoglossicida. • PvgAS regulates type III and type VI secretion systems and bacterial virulence. • T3SS is dispensable but T6SS-1 is essential for P. plecoglossicida pathogenicity. • PvgAS is a potential target for developing new therapeutic interventions. [ABSTRACT FROM AUTHOR]

Pseudomonas plecoglossicida is a temperature-dependent opportunistic pathogen mediating visceral granulomas in many piscine species including the large yellow croaker (Larimichthys crocea) but the underlying mechanisms are unclear. RpoE is an alternative sigma (σ) factor involved in regulated intramembrane proteolytic (RIP) cascade, enabling bacterial pathogens to coordinate the expression of genetic traits associated with stress adaptation and virulence determinants in response to diverse stimuli in vitro and in vivo of the hosts. In this study, genes associated to RIP cascade in P. plecoglossicida were identified and characterized to show various sequence similarities to their counterparts in Escherichia coli and P. aeruginosa. The expression of P. plecoglossicida RIP locus was induced by higher temperatures. Moreover, RNA sequencing approach revealed that RpoE regulated the expression of ∼297 and ∼261 genes at virulent (18 °C) and non-virulent (28 °C) temperatures, respectively. RpoE regulon genes are involved in various processes associated with bacterial signal transduction, membrane homeostasis, energy metabolism and virulence. In particular, RpoE positively controlled expression of csrA encoding an RNA binding protein essential for central carbon metabolism. In addition, P. plecoglossicida RpoE was validated to regulate type VI secretion system (T6SS) expression, bacteria competition, biofilm formation and reproduction in macrophages. Collectively, RpoE-centered RIP cascade appeared to play important roles in control of the expression of genes involved in adaptation in vivo and in vitro niches by thermal sensing in P. plecoglossicida. These results facilitates to reveal the pathogenic mechanisms of P. plecoglossicida causing fish diseases and provides new perspectives to control bacterial infection. [ABSTRACT FROM AUTHOR]