Ammonium sensitivity of biological nitrogen fixation in anaerobic
diazotrophs and coastal salt marsh sediments
Abstract
New bioavailable nitrogen (N) from biological nitrogen fixation (BNF) is
critical for the N budget and productivity of marine ecosystems.
Nitrogen-fixing organisms typically inactivate BNF when less
metabolically costly N sources, like ammonium (NH4+), are available.
Yet, several studies observed BNF in benthic marine sediments linked to
anaerobic sulfate-reducing bacteria (SRB) and fermenting firmicutes
despite high porewater NH4+;concentrations (10-1,500 μM), making the
importance of and regulating controls on benthic BNF unclear. Here, we
evaluate BNF sensitivity to NH4+ in model anaerobic diazotrophs, the
sulfate-reducer Desulfovibrio vulgaris var. Hildenborough and fermenter
Clostridium pasteurianum strain W5; in sulfate-reducing sediment
enrichment cultures, and in sediment slurry incubations from three
Northeastern salt marshes (USA). BNF in sulfate-reducing cultures and
sediments is highly sensitive to external NH4+, with a threshold for BNF
inhibition of [NH4+] < 2 μM in cultures and < 9
μM in sediment slurries. The prevalence of SRB-like sequences in
sediment-derived nitrogenase (nifH) genes and transcripts in this and
other studies of benthic BNF along with an analysis of benthic NH4+
porewater data suggests a broad applicability of the inhibition
thresholds measured here and the confinement of benthic BNF to surficial
sediments. The timing of inhibition, fast NH4+ drawdown, and sediment
heterogeneity are factors that can complicate studies of benthic BNF
sensitivity to NH4+. We propose a simple theoretical framework based on
the affinity of the NH4+ transporter to explain NH4+ control of BNF and
improve biogeochemical models of N cycling.