The microbial ecological dynamics of nitrogen loss versus retention

ABSTRACT Microorganisms drive complex biogeochemical cycling. Therefore, examining environmental change through the lens of microbial ecology is particularly useful for developing a mechanistic understanding of the consequences and potential feedbacks of changes and perturbations. For example, when aquatic systems undergo eutrophication, the resulting productivity impacts the microbial community function of the unventilated, dark waters below the euphotic zone, where, if anoxic, metabolisms are predominantly anaerobic. In anoxic waters, the increase in organic carbon sinking from the productive surface can shift the anaerobic community function from one in which the dominant metabolisms result in inorganic nitrogen (N) loss (such as denitrification), to one on in which metabolisms which lead to N retention dominate (such as the dissimilatory reduction of nitrate to ammonia, DNRA). This may amplify eutrophication as a positive feedback. However, we lack a mechanistic model of the controls on this transition from N loss to retention in diverse aquatic environments and in natural community consortia. Here, we provide a first-principles, quantitative understanding of this critical transition by linking ecological dynamics to the energetics underlying microbial metabolisms. We develop and analyze an ecosystem model where traits of key anaerobic N-cycling microbial functional types are constrained by redox chemistry. The model simulates the transition from N loss to N retention with increasing organic carbon supply, consistent with previous observations and theory 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. Results demonstrate that microbial ecological dynamics can be linked to environmental chemical potential, providing a predictive framework as well as testable hypotheses for sequencing data and other observations.