The Evolution of Cell-to-Cell Communication in a Sporulating Bacterium

Traditionally microorganisms were considered to be autonomous organisms that could be studied in isolation. However, over the last decades cell-to-cell communication has been found to be ubiquitous. By secreting molecular signals in the extracellular environment microorganisms can indirectly assess the cell density and respond in accordance. In one of the best-studied microorganisms, Bacillus subtilis, the differentiation processes into a number of distinct cell types have been shown to depend on cell-to-cell communication. One of these cell types is the spore. Spores are metabolically inactive cells that are highly resistant against environmental stress. The onset of sporulation is dependent on cell-to-cell communication, as well as on a number of other environmental cues. By using individual-based simulations we examine when cell-to-cell communication that is involved in the onset of sporulation can evolve. We show that it evolves when three basic premises are satisfied. First, the population of cells has to affect the nutrient conditions. Second, there should be a time-lag between the moment that a cell decides to sporulate and the moment that it turns into a mature spore. Third, there has to be environmental variation. Cell-to-cell communication is a strategy to cope with environmental variation, by allowing cells to predict future environmental conditions. As a consequence, cells can anticipate environmental stress by initiating sporulation. Furthermore, signal production could be considered a cooperative trait and therefore evolves when it is not too costly to produce signal and when there are recurrent colony bottlenecks, which facilitate assortment. Finally, we also show that cell-to-cell communication can drive ecological diversification. Different ecotypes can evolve and be maintained due to frequency-dependent selection. Biological systems are characterized by communication; humans talk, insects produce pheromones and birds sing. Over the last decades it has been shown that even the simplest organisms on earth, the bacteria, communicate. Despite the prevalence of communication, it is often hard to explain how communicative systems evolve. In bacteria, communication results from the secretion of molecular signals that accumulate in the environment. Cells can assess the concentration of these signals, which indicate cell density, and respond in accordance. This form of cell-to-cell communication is responsible for the regulation of numerous bacterial behaviors, such as sporulation. Spores are metabolically inactive cells that are highly resistant against environmental stress. It is adaptive for a cell to sporulate when it struggles to survive. We show, via individual-based simulations, that cell-to-cell communication evolves because it allows cells to predict future environmental conditions. As a consequence, cells are capable of anticipating environmental stress by initiating sporulation before conditions are actually harmful. Furthermore, our model shows that cell-to-cell communication can even drive ecological diversification, since it facilitates the evolution of individuals that specialize on distinct ecological conditions.