Individual and Combined Roles of the Master Regulators AphA and LuxR in Control of the Vibrio harveyi Quorum-Sensing Regulon

Abstract

bBacteria use a chemical communication process called quorum sensing to control transitions between individual and group behaviors. In the Vibrio harveyi quorum-sensing circuit, two master transcription factors, AphA and LuxR, coordinate the quorum-sensing response. Here we show that AphA regulates 167 genes, LuxR regulates 625 genes, and they coregulate 77 genes. LuxR strongly controls genes at both low cell density and high cell density, suggesting that it is the major quorum-sensing regulator. In contrast, AphA is absent at high cell density and acts to fine-tune quorum-sensing gene expression at low cell density. We examined two loci as case studies of coregulation by AphA and LuxR. First, AphA and LuxR directly regulate expression of the genes encoding the quorum-regulatory small RNAs Qrr2, Qrr3, and Qrr4, the consequence of which is a specifically timed transition between the individual and the group life-styles. Second, AphA and LuxR repress type III secretion system genes but at different times and to different extents. The consequence of this regulation is that type III secretion is restricted to a peak at midcell density. Thus, the asymmetric production of AphA and LuxR coupled with differences in their strengths and timing of target gene regulation generate a precise temporal pattern of gene expression.

Quorum Sensing Regulates the Osmotic Stress Response in Vibrio harveyi

“…The Qrr sRNAs repress translation of the master quorum-sensing transcription factor LuxR, and they activate translation of the master LCD quorum-sensing transcription factor AphA (5,6). Thus, at LCD, high AphA and low LuxR levels produce a gene expression pattern that yields individual behaviors (7). At HCD, the quorum-sensing receptors bind accumulated autoinducers, and in the bound state, the receptors act as phosphatases.…”

“…Thus, at HCD, AphA is not made, while LuxR is maximally produced. LuxR, in turn, controls the gene expression pattern underpinning group behaviors (7). Several regulatory feedback loops exist to properly maintain the levels of the Qrr sRNAs and to facilitate transitions between LCD and HCD: the Qrr sRNAs repress translation of LuxO (10,11), AphA represses luxR and represses qrr expression, and LuxR represses aphA and activates qrr expression ( Fig.…”

“…Several regulatory feedback loops exist to properly maintain the levels of the Qrr sRNAs and to facilitate transitions between LCD and HCD: the Qrr sRNAs repress translation of LuxO (10,11), AphA represses luxR and represses qrr expression, and LuxR represses aphA and activates qrr expression ( Fig. 1) (6,7,11,12).…”

Comprehensive analysis reveals how single nucleotides contribute to noncoding RNA function in bacterial quorum sensing

“…The Qrr sRNAs, in conjunction with the chaperone Hfq, activate translation of the LCD master regulator called AphA and destabilize the mRNA encoding LuxR, the high-cell density (HCD) master regulator (16,17). AphA controls genes that underpin individual behaviors (17,18). At HCD, AI binding converts the receptors to phosphatases, resulting in dephosphorylation and inactivation of LuxO, and cessation of qrr expression (13,15).…”

“…This event terminates Qrr activation of AphA translation, and luxR mRNA is stabilized, leading to LuxR production. LuxR controls the expression of genes that underlie collective processes (17)(18)(19)(20). The Qrr sRNAs feed back to repress luxO, and they repress or activate 17 additional mRNA targets (21).…”