Redox-constrained microbial ecology dictates nitrogen loss versus retention

Abstract

Microorganisms drive biogeochemical cycling. Therefore, examining environmental change through the lens of microbial ecology is particularly useful for developing a mechanistic understanding of the biogeochemical consequences and feedbacks of perturbations to ecosystems. When aquatic systems with deep anoxic waters undergo eutrophication, the resulting surface productivity impacts the anaerobic microbial community below. The increase in sinking organic carbon can shift the anaerobic community function from inorganic nitrogen (N) loss to N retention, amplifying eutrophication as a positive feedback. However, we lack a mechanistic understanding of this transition, which is critical for anticipating these impacts in aquatic environments where microbial community composition is unknown. Here, we provide a first-principles, quantitative model of this transition from N loss to retention by linking ecological dynamics to the energetics underlying microbial metabolisms. We develop and analyze an ecosystem model in which redox chemistry constrains the traits of key anaerobic N-cycling microbial functional types: denitrification, dissimilatory nitrate reduction to ammonium (DNRA), and anaerobic ammonium oxidation (anammox). The model captures the transition from N loss to N retention with increasing organic carbon supply, consistent with previous observations for specific systems and species. Results identify characteristics of the microbial community composition at the net zero N loss point at which N loss balances N retention, providing testable hypotheses for sequencing data and other observations. By tying microbial ecological dynamics to environmental chemical potential, results provide a broadly applicable framework for improving predictions of the biogeochemical impacts of eutrophication alongside deoxygenation and other ecosystem perturbations.