BBSRC-NSF/BIO - The impact of public versus private metabolism on the stability of microbial communities within natural hosts

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Why do microorganisms engage in cooperative nutrient consumption that is open to exploitation when an exploitation-free alternative is available? Our proposal will answer this fundamental yet unanswered question through a combination of synthetic biology, mathematical modelling and in vivo microbial community experiments. Microorganisms play crucial roles in ecosystem functioning and the health of macro organisms. They form beneficial relationships with multicellular organisms, in environments ranging from animal guts to soil, and can be exploited to degrade industrial waste or produce useful chemicals. But they can also cause devastating damage by destroying our food sources and eliminating key plant species, thus preventing the absorption of hundreds of megatonnes of CO2. Microorganisms do not exist in isolation, instead they form intricate communities of diverse strains and species where individuals participate in complex cooperative and competitive interactions. However, we lack a comprehensive understanding of how these interactions alter the function and stability of the community. This is crucial for predicting the evolution of microbial strategies that promote survival and growth in natural environments.To survive and thrive, microorganisms must obtain nutrients from their environment and cooperative and competitive actions are key to the way that microbes feed. A common strategy to obtain nutrients involves secreting metabolic products into the external, "public" environment to break down or capture resources, before they are taken up into the cell. The metabolic products are considered to be cooperative public goods as they are generated externally and so benefit other cells in the shared environment. This seemingly successful strategy, termed "public metabolism", is used by a wide range of microbial species that inhabit diverse habitats, yet it has two obvious drawbacks. First, the public goods can easily be lost into the environment before they are successfully taken up by the cell that generated them. Second, the public-goods can be exploited by microbes that "cheat" by not contributing to their production but still reap the rewards. These shortcomings can threaten the success of public metabolism and the stability and functioning of microbial communities. Curiously, an exploitation-free strategy exists whereby microbes can secure nutrients by taking them directly into the cell, with digestion taking place "privately" inside the cell, instead of "publicly" in the environment. Yet despite this failsafe alternative, many microbes still feed by public metabolism. Our project will determine why this is the case and what benefits public metabolism provides.Based on preliminary data we hypothesise that microbial feeding strategies involving either public or private metabolism represent two opposing approaches to survival, the success of which is environment-dependent. In particular, we hypothesise that sufficiently spatially structured environments will limit exploitation of public-metabolisers thus favouring them over private-metabolisers.To test this, we have generated two well-defined and tractable synthetic systems involving the environmental yeast Saccharomyces cerevisiae and the plant pathogen Magnaporthe oryzae. These communities will be used to experimentally probe the fitness of different metabolic strategies in their natural environments and assess community stability and function. In parallel, we will develop dynamic, spatially explicit, genome-scale mathematical models to generate mechanistic understanding of how metabolic interactions and the degree of spatial structure support community stability. This will enable us to extrapolate general principles from the system-specific observation and to develop a classification of different types of biotic (e.g. host-pathogen and microbe-microbe) and abiotic (e.g. spatial structure) conditions that favour cooperative metabolism.