Emergent spatial structure in a community of extracellular enzyme-producing microbes

Background/Question/Methods

Extracellular enzymes represent a public good for microbial communities, as these enzymes break down complex molecules into products that can be taken up by microbes other than the enzyme producer. These communities are vulnerable to cheating by microbes that do not produce enzymes, but benefit from those produced by others. However, enzymes are ubiquitous in nature, indicating that production is a viable strategy that is robust to cheating. In this study, we develop an individual-based, spatially explicit model in order to investigate the role of spatial structure in maintaining cooperation among microbes. This model includes three resources (C, N, and P), three enzymes, and eight types of microbes that produce zero to three enzymes. The community is characterized by facilitative (+/+), competitive (-/-), and parasitic (+/-) interactions. First, we characterize the spatial structures that emerge from each of these types of interactions. Second, we investigate the formation and stability of coalitions between complementary types, by which we mean any types that together produce all three enzymes, but which cannot produce all three alone, for example, a C/N producer and a P producer.

Results/Conclusions

The spatial structure of the community emerges spontaneously as a result of facilitative, competitive, and parasitic interactions. Facilitative interactions lead to dense aggregations of microbes in roughly circular shapes, maximizing the ratio of internal area to periphery. In contrast, competitive interactions cause microbes to be spread more evenly and thinly. Parasitic interactions lead to clouds of cheaters that cling to the peripheries of producer aggregations. Coalitions involve both facilitative and competitive interactions over asymmetrically valued resources, leading to complex and varied spatial structures of interpenetrating aggregations. Coalitions often succumb to infiltration by cheaters, especially when the cheaters are able to create a wedge in the space between the coalitional colonies. In other cases, coalitions are able to grow sufficiently large to be stable even in the presence of cheaters.

Spatially-structured social interactions allow the microbial community to evolve in surprising ways and influence total density, diversity, and community composition. These community properties lead to different concentrations of the enzymes that determine the rates of mineralization of carbon, nitrogen, and phosphorus, which are important factors to the cycling of nutrients through the ecosystem.