Environmental sensing in dynamic quorum responses

Cell communication and coordinated cell behavior are hallmarks of multicellular behavior of living systems. However, in many cases, including the ancient and archetypal example of bacterial quorum sensing, the meaning of the communicated information remains a subject of debate. It is commonly assumed that quorum sensing encodes the information on the current state of the colony, including cell density and physical colony confinement. Here, we show that quorum sensing can also be exquisitely sensitive to dynamic changes in the environment, including fluctuations of the prevailing nutrient source. We propose a new signaling mechanism accounting for this sensory capability. This mechanism combines regulation by the commonly studied lux operon-encoded network with the environmentally determined balance of protein synthesis and dilution rates, dependent on the rate of cell proliferation. This regulatory mechanism accounts for observed complex spatial distribution of quorum responses, and emergence of sophisticated processing of dynamic inputs, including temporal thresholds and persistent partial induction following a transient change in the environmental conditions. We further show that, in this context, cell communication in quorum sensing acquires a new meaning: education of cells within a population about the past history of transient exposure to adverse conditions by a subset of induced cells. In combination, these signaling and communication features may endow a cell population with increased fitness in diverse fluctuating environments.