Functional convergence in slow-growing microbial communities arises from thermodynamic constraints

Abstract

The dynamics of microbial communities is complex, determined by competition for metabolic substrates and cross-feeding of byproducts. Species in the community grow by harvesting energy from chemical reactions that transform substrates to products. In many anoxic environments, these reactions are close to thermodynamic equilibrium and growth is slow. To understand the community structure in these energy-limited environments, we developed a microbial community consumer-resource model incorporating energetic and thermodynamic constraints on an interconnected metabolic network. The central element of the model is product inhibition, meaning that microbial growth may be limited not only by depletion of metabolic substrates but also by accumulation of products. We demonstrate that these additional constraints on microbial growth cause a convergence in the structure and function of the community metabolic network-independent of species composition and biochemical details-providing a possible explanation for convergence of community function despite taxonomic variation observed in many natural and industrial environments. Furthermore, we discovered that the structure of community metabolic network is governed by the thermodynamic principle of maximum free energy dissipation. Our results predict the decrease of functional convergence in faster growing communities, which we validate by analyzing experimental data from anaerobic digesters. Overall, the work demonstrates how universal thermodynamic principles may constrain community metabolism and explain observed functional convergence in microbial communities.