Thermodynamics Underpinning the Microbial Community-Level Nitrogen Networks

Abstract

Nitrogen species often serve as crucial electron donors or acceptors in microbial catabolism, enabling the synthesis of adenosine triphosphate (ATP). Although theoretically any nitrogen redox reactions could be an energy source, it remains unclear why specific reactions are predominantly utilized. This study evaluates energetically superior reactions from 988 theoretically plausible combinations involving 11 nitrogen species, oxygen gas, hydrogen ion, and water. Our analysis of the similarity between this model-based energetically superior network and the actual microbial community-level nitrogen network, reconstructed as a combination of enzymatic reactions, showed increased link overlap rates with thermodynamic weighting on reaction rates. In particular, existing microbial reactions involving solely nitrogen species and additionally oxygen, such as anaerobic ammonia oxidation (ANAMMOX) and complete and partial nitrification, were frequently identified as energetically superior among the examined reactions. The alignment of these reactions with thermodynamically favorable outcomes underscores the critical role of thermodynamics not only in individual metabolic processes but also in shaping the broader network interactions within ecosystems, consequently affecting biodiversity and ecological functions. Significance StatementThis study advances our understanding of how thermodynamics governs energy metabolism at the community level within microbial ecosystems by systematically analyzing 988 potential redox reactions involving inorganic nitrogen species, oxygen gas, hydrogen ion, and water. We uncover that existing microbial reactions, such as anaerobic ammonia oxidation (ANAMMOX) and nitrification, stand out as energetically superior over other examined reactions. The robust alignment between model-predicted energetically favorable reactions and actual microbial nitrogen reactions underscores the predictive power of thermodynamic principles, even in ecological networks. Our findings extend the traditional applications of thermodynamics in biology, highlighting how thermodynamic constraints shape ecological networks and influence biodiversity and ecosystem functions in natural ecosystems.