Thermodynamic constraints on the assembly and diversity of microbial ecosystems are different near to and far from equilibrium

Abstract

Non-equilibrium thermodynamics has long been an area of substantial interest to ecologists because most fundamental biological processes, such as protein synthesis and respiration, are inherently energy-consuming. Microbial communities are a natural system to decipher this mechanistic basis because their interactions in the form of substrate consumption, metabolite production, and cross-feeding can be described explicitly in thermodynamic terms. Previous work has considered how thermodynamic constraints impact competition between pairs of species, but restrained from analysing how this manifests in complex dynamical systems. To address this gap, we develop a thermodynamic microbial community model with fully reversible reaction kinetics, which allows direct consideration of free-energy dissipation. This also allows species to interact via products rather than just substrates, increasing the dynamical complexity, and allowing a more nuanced classification of interaction types to emerge. Using this model, we find that community diversity increases with substrate lability, because greater free-energy availability allows for faster generation of niches. Thus, more niches are generated in the time frame of community establishment, leading to higher final species diversity. We also find that allowing species to make use of near-to-equilibrium reactions increases diversity in a low free-energy regime. In such a regime, two new thermodynamic interaction types that we identify here reach comparable strengths to the conventional (competition and facilitation) types, emphasising the key role that thermodynamics plays in community dynamics. Our results suggest that accounting for realistic thermodynamic constraints is vital for understanding the dynamics of real-world microbial communities.

arXiv comment23 pages, 5 figures

References in corpus (8)

• Information theory explanation of the fluctuation theorem, maximum entropy production and self-organized criticality in non-equilibrium stationary states
• The protein cost of metabolic fluxes: prediction from enzymatic rate laws and cost minimization
• Available energy fluxes drive a transition in the diversity, stability, and functional structure of microbial communities
• A minimal model for microbial biodiversity can reproduce experimentally observed ecological patterns
• Thermodynamics of statistical inference by cells
• Effect of resource dynamics on species packing in diverse ecosystems
• Modeling microbial cross-feeding at intermediate scale portrays community dynamics and species coexistence
• Kinetic Proofreading and the Limits of Thermodynamic Uncertainty