Lifestyle Differentiation Among Marine Denitrifying Microorganisms

Microorganisms carrying out denitrification in marine anoxic zones drive bioavailable nitrogen loss. Sequencing datasets have demonstrated the modularity of denitrification, with most populations having the genetic capability for only a subset of the pathway (NO3-➔NO2-➔NO➔N2O➔N2). Although previous work provided ecological explanations for this diversity among the functional modules, large trait variations exist within each functional module, and this within-module diversity and its biogeochemical implications remain unexplored. Here, we combine genomic data and modeling to explore how metabolic "lifestyle" strategies influence denitrifier community structure. We build a comprehensive genomic database of marine denitrifiers, and identify lifestyle differentiation among denitrifier functional groups. We then extend a mathematical ecosystem model by resolving two microbial functional types for each module representing a metabolic trade-off: a copiotroph, optimized for fast growth, and an oligotroph, optimized for high nutrient affinity. In the model, as the supply of organic matter relative to nitrate increases, the degree of copiotrophy among the community increases and then decreases. This suggests that oligotrophs are associated with either organic-matter- or nitrate-limiting conditions, whereas copiotrophic lifestyles are associated with an intermediate regime. Our model further associates NO2- reducers with oligotrophy and NO3- reducers with copiotrophy, particularly those producing greenhouse gas nitrous oxide (N2O), linking N2O production to substrate-replete conditions, which is consistent with our genome-based lifestyle estimates. Results provide insight into denitrifier ecological niches and thus the biogeochemical conditions that are associated with the production of intermediates, such as N2O, improving our understanding of how nitrogen cycling will change in a warming ocean.