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

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 have observ...

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Bibliographic Details
Published in:Journal of geophysical research. Biogeosciences 2022-07, Vol.127 (7), p.n/a
Main Authors: Darnajoux, Romain, Reji, Linta, Zhang, Xin Rei, Luxem, Katja E., Zhang, Xinning
Format: Article
Language:English
Subjects:
Ammonium
Ammonium compounds
Bacteria
Benthic environment
benthic microbial ecology
benthic nitrogen fixation
Benthos
Bioavailability
Biogeochemistry
Biophysics
Cultures
Deactivation
Drawdown
Energy sources
Fermentation
Heterogeneity
heterotrophic diazotrophy
Limiting factors
Marine ecosystems
marine nitrogen cycling
Marine sediments
Microorganisms
NifH gene
Nitrogen
Nitrogen fixation
Nitrogenase
Nitrogenation
Organic carbon
Photosynthesis
Pore water
Productivity
Salt marshes
Saltmarshes
Sediment
Sediment composition
Sediments
Sensitivity analysis
Slurries
Sulfates
Surveying
Uptake
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Summary: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 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. Plain Language Summary Biological nitrogen fixation (BNF) is the main source of the bioavailable nitrogen (N) that serves as a source of energy and limiting nutrient for productivity in the ocean. Nitrogen‐fixing microorganisms typically inactivate BNF when less metabolically costly N sources, like ammonium, are available. However, recent field studies that report BNF under ammonium‐rich conditions suggest that non‐photosynthetic, organic carbon‐consuming “heterotrophic” microbes in benthic environments play a bigger role in oceanic BNF than previously thought. Here, we show that BNF by cultured and sediment‐dwelling heterotrophic N‐fixers is highly sensitive to ammonium, with a
ISSN:2169-8953
2169-8961
DOI:10.1029/2021JG006596