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A Regulatory Network Controls cabABC Expression Leading to Biofilm and Rugose Colony Development in Vibrio vulnificus.

ABSTRACT: Biofilms provide bacteria with protection from environmental stresses and host immune defenses. The pathogenic marine bacterium Vibrio vulnificus forms biofilms and colonizes environmental niches such as oysters. The cabABC operon encodes an extracellular matrix protein CabA and the corresponding type I secretion system, which are essential for biofilm and rugose colony development of V. vulnificus. In this study, molecular biological analyses revealed the roles of three transcriptional regulators BrpR, BrpT, and BrpS in the regulatory pathway for the cabABC operon. BrpR induces brpT and BrpT in turn activates the cabABC operon in a sequential cascade, contributing to development of robust biofilm structures. BrpT also activates brpS, but BrpS represses brpT, constituting a negative feedback loop that stabilizes brpT expression. BrpT and BrpS directly bind to specific sequences upstream of cabA, and they constitute a feedforward loop in which BrpT induces brpS and together with BrpS activates cabABC, leading to precise regulation of cabABC expression. Accordingly, BrpS as well as BrpT plays a crucial role in complete development of rugose colonies. This elaborate network of three transcriptional regulators BrpR, BrpT, and BrpS thus tightly controls cabABC regulation, and contributes to successful development of robust biofilms and rugose colonies in V. vulnificus.

SUBMITTER: Hwang S

PROVIDER: S-EPMC6978666 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Project description:Vibrio vulnificus is a potent opportunistic human pathogen that contaminates the human food chain by asymptomatically colonizing seafood. The expression of the 9-gene brp exopolysaccharide locus mediates surface adherence and is controlled by the secondary signaling molecule c-di-GMP and the regulator BrpT. Here, we show that c-di-GMP and BrpT also regulate the expression of an adjacent 5-gene cluster that includes the cabABC operon, brpT, and another VpsT-like transcriptional regulator gene, brpS The expression of the 14 genes spanning the region increased with elevated intracellular c-di-GMP levels in a BrpT-dependent manner, save for brpS, which was positively regulated by c-di-GMP and repressed by BrpT. BrpS repressed brpA expression and was required for rugose colony development. The mutation of its consensus WFSA c-di-GMP binding motif blocked these activities, suggesting that BrpS function is dependent on binding c-di-GMP. BrpT specifically bound the cabA, brpT, and brpS promoters, and binding sites homologous to the Vibrio cholerae VpsT binding site were identified upstream of brpA and brpT Transcription was initiated distal to brpA, and a conserved RfaH-recruiting ops element and a potential Rho utilization (rut) terminator site were identified within the 100-bp leader region, suggesting the integration of early termination and operon polarity suppression into the regulation of brp transcription. The GC content and codon usage of the 16-kb brp region was 5.5% lower relative to that of the flanking DNA, suggesting its recent assimilation via horizontal transfer. Thus, architecturally, the brp region can be considered an acquired biofilm and rugosity island that is subject to complex regulation.IMPORTANCE Biofilm and rugose colony formation are developmental programs that underpin the evolution of Vibrio vulnificus as a potent opportunistic human pathogen and successful environmental organism. A better understanding of the regulatory pathways governing theses phenotypes promotes the development and implementation of strategies to mitigate food chain contamination by this pathogen. c-di-GMP signaling is central to both pathways. We show that the molecule orchestrates the expression of 14 genes clustered in a 16-kb segment of the genome that governs biofilm and rugose colony development. This region exhibits the hallmarks of horizontal transfer, suggesting complex regulatory control of a recently assimilated genetic island governing the colonization response of V. vulnificus.

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A Regulatory Network Controls cabABC Expression Leading to Biofilm and Rugose Colony Development in Vibrio vulnificus.

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