Potential competition between marine heterotrophic prokaryotes and autotrophic picoplankton for nitrogen substrates

Abstract

Heterotrophic prokaryotes have the capacity to uptake inorganic nitrogen (N) substrates. However, it remains unclear what the potential competition is between heterotrophic prokaryotes and autotrophic plankton for N in the ocean, which would shunt the flow of N supporting primary production. To date, it has been difficult to distinguish heterotrophic prokaryotic N uptake from that of autotrophic picoplankton, especially in oligotrophic oceans dominated by cyanobacteria. We carried out field-based DNA stable isotope probing incubation experiments in the South China Sea combining measurements of uptake rates of ammonium, nitrate, nitrite, and urea to estimate the taxon-specific potential N assimilation. The results indicate that phylogenetically diverse heterotrophic prokaryotes significantly incorporated multiple N sources, contributing approximately 17–41% and 19–55% of total N uptake potential in the euphotic zone of the South China Sea continental shelf and open ocean, respectively, potentially competing with cyanobacteria (mainly Prochlorococcus). Notably, heterotrophic prokaryotes made a higher contribution to bulk uptake of nitrate in the incubation systems of the open ocean relative to regenerated N, and thus there was a tendency to overestimate the f-ratio. Extrapolating our results to the oligotrophic, low-latitude ocean via a global model suggests the f-ratio would decrease ~ 18%. This suggests a more complicated biogeochemical role of heterotrophic prokaryotes in the biological carbon pump than hitherto assumed, with important implications for N and carbon cycling in the vast open ocean.