Modelling the effects of microbial spatial heterogeneity on soil metabolic networks

Abstract. Bacteria and archaea with a wide variety of metabolisms are found in huge numbers in soil and are engaged in both intra- and inter-specific interactions. The exchange and transformation of resources within the metabolic networks formed by microbes are affected by the heterogeneity of soil, as well as by the diversity and abundance of microorganisms. Therefore, depending on environmental conditions and the relative abundance of species and resources present, not all theoretically possible interactions are likely to be realized in practice. Most studies that aim to reconstruct metabolic networks in soil do not account for the potential spatial separation between organisms, caused by the heterogeneous physical structure of the soil environment, and thus only represent some kind of "average network" that may not reflect reality. Here, we further developed a simple geometric model to study how bacterial spatial distributions can alter the functioning of metabolic networks and the emerging behaviours that can arise from them. We show that the spatial distribution of bacteria impacts the transformation of resources depending on the distance to which cells can alter their environment, and that it can lead to behaviours that blur the line between cooperation and competition between bacterial species when both interact with a third partner species. We found that when bacterial density is low, have short interaction ranges and are distributed independently of one another, the use of available resources is less efficient and more variable. On the other hand, when population densities are high and interactions occur over longer distances, more complex interactions emerge. For example, apparent competitors can enter into mutualistic interactions merely due to their spatial configuration around a common partner. Overall, we show that the spatial distribution of organisms may be an important regulatory factor of the functioning of microbial communities and may determine the rates at which resources are transformed in soils.