Many host-associated bacteria use pheromone-signaling (PS) systems to coordinate group behaviors. Such signaling requires high cell density, and is often referred to as “quorum sensing”. However, a high cell density “quorum” may be necessary but not sufficient to induce a behavior. Our understanding of the light-organ symbiosis between the bioluminescent bacterium Vibrio fischeri and the Hawaiian bobtail squid Euprymna scolopes suggests that the bacteria could use PS as a way to communicate information about host microenvironments. We have shown that environmental regulation combined with positive feedback could enable a subpopulation of bacteria experiencing a specific cue to elicit a response from the entire population, even though all the cells may not experience the cue. Using fluorescent reporters to probe gene regulation in symbionts, we have found that at least one cue regulating the V. fischeri PS system appears heterogeneous across different microenvironments of the host light organ. Our research suggests how bacterial PS may be used to communicate information about transient or heterogeneous environmental cues across a bacterial population.