PqsR-independent quorum-sensing response of Pseudomonas aeruginosa ATCC 9027 outlier-strain reveals new insights on the PqsE effect on RhlR activity

Mol Microbiol. 2021 Oct;116(4):1113-1123. doi: 10.1111/mmi.14797. Epub 2021 Aug 30.

Abstract

Pseudomonas aeruginosa is a ubiquitous environmental bacterium and an opportunistic pathogen that represents an important health hazard. The quorum-sensing response regulates the expression of several virulence factors and involves three regulons: Las, Rhl, and Pqs. The P. aeruginosa ATCC 9027 strain, which belongs to the genetically diverse PA7 clade, contains a frame-shift mutation in the pqsR gene that encodes a transcriptional activator necessary for pyocyanin (PYO) synthesis in type strains PAO1 and PA14. Here we characterize the PqsE-dependent production of PYO in strain ATCC 9027. We show that this strain expresses pqsE independently of PqsR and in the absence of quinolone production, and that PqsE promotes the RhlR-dependent production of PYO, yet this production is not strictly dependent on PqsE. In addition, we show that in both strains ATCC 9027 and PAO1, PqsE overexpression causes an increased concentration of RhlR and enhances PYO production but does not affect rhamnolipids (RL) production in the same way. These results suggest that PqsE interaction with RhlR preferentially modifies its ability to activate transcription of genes involved in PYO production and provide new evidence about PqsE-dependent RhlR activation, highlighting the variability of the QS response among different P. aeruginosa clades and strains. HIGHLIGHTS: Pseudomonas aeruginosa ATCC 9027 is able to produce pyocyanin in phosphate limiting conditions, even in the absence of a functional PqsR. This strain does not produce alkyl quinolones like PQS and HHQ, but expresses pqsE. Synthesis of pyocyanin by ATCC 9027 is only partially dependent on pqsE. The overexpression of pqsE in the ATCC 9027 and PAO1 strains causes pyocyanin overproduction. The overexpression of pqsE in these strains causes an increased RhlR concentration without affecting rhlR transcription or translation. Rhamnolipids production is not affected to the same extent as pyocyanin by overexpression of pqsE in these strains.

Keywords: Pseudomonas aeruginosa; PqsE; RhlR; pyocyanin; quorum sensing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Frameshift Mutation
  • Gene Expression Regulation, Bacterial
  • Glycolipids / metabolism
  • Humans
  • Mutation
  • Operon
  • Pseudomonas Infections / microbiology
  • Pseudomonas aeruginosa / genetics*
  • Pseudomonas aeruginosa / metabolism*
  • Pyocyanine / biosynthesis*
  • Quinolones / metabolism
  • Quorum Sensing*
  • Regulon
  • Thiolester Hydrolases / genetics*
  • Thiolester Hydrolases / metabolism*
  • Trans-Activators
  • Virulence Factors / genetics
  • Virulence Factors / metabolism

Substances

  • Bacterial Proteins
  • Glycolipids
  • Quinolones
  • RhlR protein, Pseudomonas aeruginosa
  • Trans-Activators
  • Virulence Factors
  • rhamnolipid
  • Pyocyanine
  • Thiolester Hydrolases