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. However, most of this interest has focused on developing coarse ecosystem-level maximisation principles, providing little insight into underlying mechanisms that lead to such emergent constraints. 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.
Highlights
The constraints thermodynamics place upon on individual organisms inevitably impact ecosystem dynamics
We show that when the free-energy availability is low, species with reactions close to thermodynamic equilibrium are favoured, leading to more diverse and efficient communities
In addition to the conventional interaction types, our model reveals the existence of two novel interaction types mediated by products rather than substrates
Summary
The constraints thermodynamics place upon on individual organisms inevitably impact ecosystem dynamics. These attempts have generally involved the development of coarse, whole-ecosystem level extremal (maximisation or minimisation) principles, such as flux [1] and power maximisation [2] Most notable of these is the maximum entropy production principle, that ecosystems tend towards states that produce entropy at the maximum achievable rate [3]. In biophysics, non-equilibrium thermodynamics at the cellular level have been considered in much greater detail [7], in the areas of kinetic proofreading [8] and sensing accuracy [9, 10] This opens the possibility of detailed consideration of the impact of thermodynamic constraints on ecosystem dynamics
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