A σE-Mediated Temperature Gauge Controls a Switch from LuxR-Mediated Virulence Gene Expression to Thermal Stress Adaptation in Vibrio alginolyticus

PLoS Pathog. 2016 Jun 2;12(6):e1005645. doi: 10.1371/journal.ppat.1005645. eCollection 2016 Jun.

Abstract

In vibrios, the expression of virulence factors is often controlled by LuxR, the master quorum-sensing regulator. Here, we investigate the interplay between LuxR and σE, an alternative sigma factor, during the control of virulence-related gene expression and adaptations to temperature elevations in the zoonotic pathogen Vibrio alginolyticus. An rpoE null V. alginolyticus mutant was unable to adapt to various stresses and was survival-deficient in fish. In wild type V. alginolyticus, the expression of LuxR-regulated virulence factors increased as the temperature was increased from 22°C to 37°C, but mutants lacking σE did not respond to temperature, indicating that σE is critical for the temperature-dependent upregulation of virulence genes. Further analyses revealed that σE binds directly to -10 and -35 elements in the luxR promoter that drive its transcription. ChIP assays showed that σE binds to the promoter regions of luxR, rpoH and rpoE at high temperatures (e.g., 30°C and 37°C). However, at higher temperatures (42°C) that induce thermal stress, σE binding to the luxR promoter decreased, while its binding to the rpoH and rpoE promoters was unchanged. Thus, the temperature-dependent binding of σE to distinct promoters appears to underlie a σE-controlled switch between the expression of virulence genes and adaptation to thermal stress. This study illustrates how a conserved temperature response mechanism integrates into quorum-sensing circuits to regulate both virulence and stress adaptation.

MeSH terms

  • Adaptation, Physiological / physiology*
  • Animals
  • Chromatin Immunoprecipitation
  • Electrophoretic Mobility Shift Assay
  • Gene Expression Regulation, Bacterial / physiology*
  • Immunoblotting
  • Polymerase Chain Reaction
  • Repressor Proteins / biosynthesis*
  • Sigma Factor / metabolism*
  • Stress, Physiological / physiology
  • Temperature
  • Trans-Activators / biosynthesis*
  • Vibrio Infections / metabolism
  • Vibrio alginolyticus / physiology*
  • Virulence / physiology*
  • Virulence Factors / biosynthesis*
  • Zebrafish

Substances

  • Repressor Proteins
  • Sigma Factor
  • Trans-Activators
  • Virulence Factors
  • LuxR autoinducer binding proteins

Grants and funding

This work was supported by grants from the National Natural Science Foundation of China (www.nsfc.gov.cn) (Nos. 31372560 and 41376128) to QW and YZ, respectively, the Shanghai Youth Sailing Program (www.stcsm.gov.cn) (No. 14YF1413700) to MY, and the National Institute of Food and Agriculture, US Department of Agriculture Grant (CONS00935) to XZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.