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Bacterial pheromone signaling is often governed both by environmentally responsive regulators and by positive feedback. This regulatory combination has the potential to coordinate a group response among distinct subpopulations that perceive key environmental stimuli differently. We have explored the interplay between an environmentally responsive regulator and pheromone-mediated positive feedback in intercellular signaling by  Vibrio fischeri  ES114, a bioluminescent bacterium that colonizes the squid  Euprymna scolopes . Bioluminescence in ES114 is controlled in part by  N -(3-oxohexanoyl)-L-homoserine lactone (3OC6), a pheromone produced by LuxI that together with LuxR activates transcription of the  luxICDABEG  operon, initiating a positive feedback loop and inducing luminescence. The  lux  operon is also regulated by environmentally responsive regulators, including the redox-responsive ArcA/ArcB system, which directly represses  lux  in culture. Here we show that inactivating  arcA  leads to increased 3OC6 accumulation to initiate positive feedback. In the absence of positive feedback,  arcA -mediated control of luminescence was only ∼2-fold, but  luxI -dependent positive feedback contributed more than 100 fold to the net induction of luminescence in the  arcA  mutant. Consistent with this overriding importance of positive feedback, 3OC6 produced by the  arcA  mutant induced luminescence in nearby wild-type cells, overcoming their ArcA repression of  lux . Similarly, we found that artificially inducing ArcA could effectively repress luminescence before, but not after, positive feedback was initiated. Finally, we show that 3OC6 produced by a subpopulation of symbiotic cells can induce luminescence in other cells co-colonizing the host. Our results suggest that even transient loss of ArcA-mediated regulation in a sub-population of cells can induce luminescence in a wider community. Moreover, they indicate that 3OC6 can communicate information about both cell density and the state of ArcA/ArcB.

Coordination of the Arc Regulatory System and Pheromone-Mediated Positive Feedback in Controlling the Vibrio fischeri lux Operon