Environmental cues in an ecological niche are often temporal in nature. For instance, in temperate climates, temperature is higher in daytime compared to during night. In response to these temporal cues, bacteria have been known to exhibit anticipatory regulation, whereby triggering response to a yet to appear cue. Such an anticipatory response in known to enhance Darwinian fitness, and hence, is likely an important feature of regulatory networks in microorganisms. However, the conditions under which an anticipatory response evolves as an adaptive response are not known. In this work, we develop a quantitative model to study response of a population to two temporal environmental cues, and predict variables which are likely important for evolution of anticipatory regulatory response. We follow this with experimental evolution of Escherichia coli in alternating environments of rhamnose and paraquat for ∼850 generations. We demonstrate that growth in this cyclical environment leads to evolution of anticipatory regulation. As a result, pre-exposure to rhamnose leads to a greater fitness in paraquat environment. Genome sequencing reveals that this anticipatory regulation is encoded via mutations in global regulators. Overall, our study contributes to understanding of how environment shapes the topology of regulatory networks in an organism.

One of the central goals of ecology is to explain and predict coexistence of species. In this context, microbial communities provide a model system where community structure can be studied in environmental niches and in laboratory conditions. A community of microbial population is stabilized by interactions between participating species. However, the nature of these stabilizing interactions has remained largely unknown. Theory and experiments have suggested that communities are stabilized by antagonistic interactions between member species, and destabilized by synergistic interactions. However, experiments have also revealed that a large fraction of all the interactions between species in a community are synergistic in nature. To understand the relative significance of the two types of interactions (synergistic vs. antagonistic) between species, we perform simulations of microbial communities with a small number of participating species using two frameworks—a replicator equation and a Lotka-Volterra framework. Our results demonstrate that synergistic interactions between species play a critical role in maintaining diversity in cultures. These interactions are critical for the ability of the communities to survive perturbations and maintain diversity. We follow up the simulations with quantification of the extent to which synergistic and antagonistic interactions are present in a bacterial community present in a soil sample. Overall, our results show that community stability is largely achieved with the help of synergistic interactions between participating species. However, we perform experiments to demonstrate that antagonistic interactions, in specific circumstances, can also contribute toward community stability.

Environmental cues in an ecological niche are temporal. In response to these temporal cues, bacteria have been known to exhibit learning or conditioning, whereby they trigger response to a yet to appear cue, anticipating its actual arrival in the near future. Such an anticipatory response in known to enhance Darwinian fitness, and hence, is likely an important feature in the regulatory networks in microorganisms. However, the conditions under which an anticipatory response optimizes cellular fitness are not known. Nor has evolution of anticipatory regulation in laboratory conditions been experimentally demonstrated. In this work, we develop a quantitative model to study response of a population to two temporal environmental cues, and present the key variables in cellular physiology associated with response to the cues whose modulation is likely to lead to evolution of anticipatory regulatory response. We predict experimental conditions, which are likely to lead to demonstration of rewiring of regulation, and evolution of anticipatory response in bacterial populations. Using inputs from the modeling results, we evolve E. coli in alternating environments of the pentose sugar rhamnose and paraquat, which induces oxidative stress. We demonstrate that growth in this cyclical environment leads to evolution of anticipatory regulation. Thus, we argue that in niches where environmental stimuli have a cyclical nature, conditioning evolves in a population as an adaptive response.