Maintenance and evolution of cooperation in synthetic microbial ecosystems

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The emergence of cooperative traits (like production of public goods) in microbial populations and their maintenance in the presence of free-riders is a central problem in evolutionary biology. In the first funding period, our focus was on the effect of demographic noise on growth dynamics and composition of cooperative bacterial populations under non-selective and selective conditions, combining experiments and theory. We showed that under non-selective conditions, growing populations never fixate to a trait, but adjust to a random steady state composition. In selective conditions, we experimentally validated our theoretical prediction that demographic noise leads to a transient increase in the fraction of public good producers in an ensemble of populations. To this end, we established a synthetic ecosystem and identified experimental conditions for cooperative behavior in Pseudomonas populations. Moreover, we showed that the expression of pyoverdine synthesis genes is phenotypically heterogeneous in a Pseudomonas population, and is modulated by iron availability. In the upcoming funding period, we intend to broaden the scope of the project and proceed along two main lines of research. (1) First, we will develop a more mechanistic molecular understanding of gene regulatory mechanisms underlying pyoverdine production and consumption, as well as its effect on the growth rate of producer and non-producer strains. Previous theoretical models partially neglected the effects of accumulated pyoverdine and growth phase on siderophore production. We will extend these models to account for this feature and perform a quantitative analysis of the impact of external pyoverdine on growth dynamics of producer and non-producer strains. Moreover, we plan to unravel the molecular mechanisms of pyoverdine production and regulation in P. putida. Specifically, we will analyze the presumed individual regulatory circuits and relate their activity to the metabolic state and pyoverdine production under various conditions of iron availability. These analyses will provide a comprehensive picture of the regulatory network and information on cell behavior in different environments. (2) Second, we will consider spatially extended systems to understand whether and how spatial structuring impacts cooperative behavior. We will investigate how the additional effects of dynamics and regulation of the public goods, and heterogeneity in bacterial mobility affect the emergence of cooperative behavior. Our theoretical studies will rely on lattice gas models, which we will analyze employing stochastic simulations and analytic approaches. Experiments will be performed with producer/non-producer co-cultures in two distinct settings: a fixed spatial environment with discontinuous expansion to new sites, and a structured environment allowing continuous spreading of public good and cells. The development of the co-culture in space and time will be analyzed in various ecological conditions.