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AphA and LuxR/HapR reciprocally control quorum sensing in vibrios
Steven T. Rutherford1,
Julia C. van Kessel1,
Yi Shao1,, and
Bonnie L. Bassler1,2,3
1 Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544, USA; 2 Howard Hughes Medical Institute, Princeton University, Princeton, New Jersey 08544, USA
Bacteria cycle between periods when they perform individualbehaviors and periods when they perform group behaviors. Thesetransitions are controlled by a cell–cell communicationprocess called quorum sensing, in which extracellular signalmolecules, called autoinducers (AIs), are released, accumulate,and are synchronously detected by a group of bacteria. AI detectionresults in community-wide changes in gene expression, enablingbacteria to collectively execute behaviors such as bioluminescence,biofilm formation, and virulence factor production. In thisstudy, we show that the transcription factor AphA is a masterregulator of quorum sensing that operates at low cell density(LCD) in Vibrio harveyi and Vibrio cholerae. In contrast, LuxR(V. harveyi)/HapR (V. cholerae) is the master regulator thatoperates at high cell density (HCD). At LCD, redundant smallnoncoding RNAs (sRNAs) activate production of AphA, and AphAand the sRNAs repress production of LuxR/HapR. Conversely, atHCD, LuxR/HapR represses aphA. This network architecture ensuresmaximal AphA production at LCD and maximal LuxR/HapR productionat HCD. Microarray analyses reveal that 300 genes are regulatedby AphA at LCD in V. harveyi, a subset of which is also controlledby LuxR. We propose that reciprocal gradients of AphA and LuxR/HapRestablish the quorum-sensing LCD and HCD gene expression patterns,respectively.