Cooperation and spatial self-organization determine ecosystem function for polysaccharide-degrading bacteria

Abstract

AbstractThe recycling of particulate organic matter (POM) by microbes is a key part of the global carbon cycle, one which is mediated by the extracellular hydrolysis of polysaccharides and the production of public goods that can trigger social behaviors in bacteria. Despite the potential importance of these microbial interactions, their role in regulating of ecosystem function remains unclear. In this study, we developed a computational and experimental model system to address this challenge and studied how POM depolymerization rate and its uptake efficiency –two main ecosystem function parameters– depended on social interactions and spatial self-organization on particle surfaces. We found an emergent trade-off between rate and efficiency resulting from the competition between oligosaccharide diffusion and cellular uptake, with low rate and high efficiency being achieved through cell-to-cell cooperation between degraders. Bacteria cooperated by aggregating in cell-clusters of ~10-20μm, where cells were able to share public goods. This phenomenon, which was independent of any explicit group-level regulation, led to the emergence of critical cell concentrations below which degradation did not occur, despite all resources being available in excess. By contrast, when particles were labile and turnover rates were high, aggregation promoted competition and decreased the efficiency of carbon utilization. Our study shows how social interactions and cell aggregation determine the rate and efficiency of particulate carbon turnover in environmentally relevant scenarios.Significance StatementMicroorganisms can cooperate by secreting public goods that benefit local neighbors, however, the impact of cooperation on ecosystem functions remains poorly constrained. We here pair computation and experiment to show that bacterial cooperation mediates the degradation of polysaccharide particles recalcitrant to hydrolysis in aquatic environments. On particle surfaces, cooperation emerges through the self-organization of cells into ~10-20μm clusters that promote cooperative uptake of hydrolysis products. The transition between cooperation and competition in aggregates is mitigated by individual cell behaviors such as motility and chemotaxis, that promote reorganization on the particle surface. When cooperation is required, the degradation of recalcitrant biopolymers can only take place when degraders exceed a critical cell concentration, underscoring the importance of microbial interactions for ecosystem function.