A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator

Mol Microbiol. 2013 Jan;87(1):1-13. doi: 10.1111/mmi.12079. Epub 2012 Nov 19.

Abstract

ICEMlSym(R7A) of Mesorhizobium loti is an integrative and conjugative element (ICE) that confers the ability to form a nitrogen-fixing symbiosis with Lotus species. Horizontal transfer is activated by TraR and N-acyl-homoserine lactone (AHL), which can stimulate ICE excision in 100% of cells. However, in wild-type cultures, the ICE is excised at low frequency. Here we show that QseM, a widely conserved ICE-encoded protein, is an antiactivator of TraR. Mutation of qseM resulted in TraR-dependent activation of AHL production and excision, but did not affect transcription of traR. QseM and TraR directly interacted in a bacterial two-hybrid assay in the presence of AHL. qseM expression was repressed by a DNA-binding protein QseC, which also activated qseC expression from a leaderless transcript. QseC differentially bound two adjacent operator sites, the lower affinity of which overlapped the -35 regions of the divergent qseC-qseM promoters. QseC homologues were identified on ICEs, TraR/TraM-regulated plasmids and restriction-modification cassettes, suggesting a conserved mode of regulation. Six QseC variants with distinct operators were identified that showed evidence of reassortment between mobile elements. We propose that QseC and QseM comprise a bimodal switch that restricts quorum sensing and ICEMlSym(R7A) transfer to a small proportion of cells in the population.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Butyrolactone / analogs & derivatives
  • 4-Butyrolactone / pharmacology
  • Amino Acid Sequence
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Conjugation, Genetic
  • Gene Expression Regulation, Bacterial
  • Gene Transfer, Horizontal
  • Genomic Islands*
  • Homoserine / analogs & derivatives
  • Homoserine / pharmacology
  • Lotus / metabolism
  • Lotus / microbiology
  • Mesorhizobium / genetics
  • Mesorhizobium / metabolism
  • Mesorhizobium / physiology*
  • Nitrogen Fixation / genetics
  • Plasmids / genetics
  • Promoter Regions, Genetic
  • Quorum Sensing / genetics*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Symbiosis / genetics
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Transcription, Genetic / drug effects
  • Transcriptional Activation* / drug effects

Substances

  • Bacterial Proteins
  • N-(3-oxododecanoyl)homoserine lactone
  • RNA, Messenger
  • Transcription Factors
  • Homoserine
  • 4-Butyrolactone