CAREER: The impact of spatial-positioning mechanisms on the metabolic interactions and emergent properties of synthetic bacterial communities

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Microbes constitute a large portion of the Earth's biomass. In the majority of environments, microbes live as interacting communities. However, not much is known regarding how microbial worlds communicate, evolve, share resources, and interact with other organisms. This project will address how bacteria position themselves within microbial communities to cooperatively trade nutrients with neighboring cells or alternatively steal nutrients from neighbors. Such cross-feeding interactions influence important processes, including human health and element cycling. Cross-feeding communities can also be harnessed to degrade pollutants and convert renewable resources into useful products, such as biofuels. The results from this project will thus have broad benefits by informing on natural microbial interactions of environmental and medical relevance and by generating principles for the engineering of bacterial communities as a technology to benefit society. This research will involve direct participation of regional high school students, including underrepresented minorities. Additional high school students will gain research experiences through a collaboration between the research team and high school teachers, which will bring experiments to classrooms. This project will also generate an innovative storytelling platform that will provide an intuitive framework upon which to communicate detail-intensive and traditionally unpopular topics in metabolism and biochemistry to learners of all ages. This project will examine how bacteria optimize their location within cross-feeding communities that pit cooperative cells against exploitive (cheater) cells. Current theory indicates that clustering of cooperative cells can keep cheaters at bay. However, this theory does not take into account mechanisms that bacteria use to sense and swim towards nutrients and to adhere to surfaces and other cells. A lack of knowledge on how motility and adhesion influence metabolic interactions and community structure hampers not only our general understanding of microbial community behavior but also our ability to design useful synthetic communities. The objective of this project is to determine the impact of motility and adhesion on subpopulation dynamics in cross-feeding communities and on emergent properties, such as hydrogen biofuel production. The objective will be achieved using both experimental and computationally-simulated communities. One community will pair ammonium-excreting cooperators and ammonium-consuming cheaters of a single species, Rhodopseudomonas palustris. A second community will pair R. palustris with Escherichia coli in an obligate cross-feeding relationship wherein ammonium from R. palustris is exchanged for carbon nutrients from E. coli. This mutualism will also be challenged with an R. palustris cheater. In each case, the effects of motility and adhesion on cooperator and cheater fitness and community structure will be determined using environmental and genetic conditions that either permit or restrict motility and adhesion. This project will thus provide a much-needed molecular understanding of spatial bacterial community behaviors of environmental, medical, and industrial relevance.