Polymorphic metabolism and the eco-evolutionary influence of social feeding strategies

Microbes live in complex environments where competitive and cooperative interactions occur that dictate their success and the status of their environment. By furthering our understanding of the interactions between microbes, questions into the evolution of cooperation, disease virulence and biodiversity can be addressed. This will help develop strategies to overcome problems concerning disease, socioeconomics and conservation. We use an approach that combines evolutionary ecology theory with genetics and molecular biology to establish and develop model microbial ecological systems to examine feeding strategies, in what has been termed synthetic ecology. Using the model fungal plant pathogen system of rice blast disease, we generated less virulent gene deletion mutants to examine the sociality of feeding strategies during infection and test a nascent virulence reduction strategy based on competitive exclusion. We revealed that the success of the pathogen is unexpectedly enhanced in mixed strain infections containing the virulent wild-type strain with a less virulent gene deletion mutant of the metabolic enzyme invertase. Our finding is explained by interference between different social traits that occur during sucrose feeding. To test the generality of our result, gene deletion mutants of putative proteases were generated and characterised. We found that if virulence related genes acted ‘privately’, as predicted by social theory, the associated mutants would not make viable strains to use for this virulence reduction strategy by competitive exclusion. Our study then went on to study the fitness of digesting resources extracellularly, as many microbes do, given that this strategy is exposed to social exploitation by individuals who do not pay the metabolic costs. This was investigated by developing an experimental system with Saccharomyces cerevisiae. Though internalising digestion could suppress cheats, the relative fitness of opposing strategies was dependent upon the environmental and demographic conditions. Using this polymorphic system, the influence of competitors on the stability of cooperation, and the influence of cheats on the maintenance of diversity were assessed. To test the fitness of internal versus external digestion in a more natural setting, we generated an internally digesting strain of the rice blast fungus. In addition to suppressing cheats, the strain had enhanced fitness and virulence over the wild-type. We propose that this is caused by a shift in a trade-off between yield and rate. We show how a synthetic ecology approach can capture details of the biology underlying complex ecological processes, while having control over the factors that drive them, so that the underlying mechanisms can be teased apart.NER