Ammonium Sensitivity of Biological Nitrogen Fixation by Anaerobic Diazotrophs in Cultures and Benthic Marine Sediments

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AbstractNew 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 have observed BNF in benthic marine sediments linked to anaerobic sulfate‐reducing bacteria and fermenting firmicutes despite high porewater NH4+ concentrations (10–1,500 μM). To better understand the regulating controls and importance of benthic marine BNF, we evaluate BNF sensitivity to NH4+ in benthic diazotrophs using incubations of increasing biogeochemical complexity. BNF by cultures of model anaerobic diazotrophs (sulfate‐reducer Desulfovibrio vulgaris var. Hildenborough, fermenter Clostridium pasteurianum strain W5), sulfate‐reducing sediment enrichment cultures, and sediments from three Northeastern salt marshes (USA) is highly sensitive to external NH4+. BNF is inhibited by NH4+ beyond an apparent threshold [NH4+] of 2 μM in liquid cultures, most closely reflecting the true cellular sensitivity of BNF to NH4+. Sediment slurries exhibited an apparent threshold [NH4+] of 9 μM. Consistent with other studies, we find SRB‐like nitrogenase (nifH) gene and transcripts are prevalent in sediments. Our survey of porewater NH4+ data from diverse sediments suggests the broad applicability of inhibition thresholds measured here and confinement of benthic BNF to surficial sediments. Variations in BNF inhibition timing, NH4+ uptake rate, sediment composition, and biophysics could affect measurements of the apparent sensitivity of benthic BNF to NH4+. We propose NH4+ transporter affinity as a fundamental mechanistic constraint on NH4+ control of cellular BNF to improve biogeochemical models of N cycling.