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

Abstract

Biological nitrogen fixation (BNF) is the dominant source of new bioavailable nitrogen (N) in the ocean (Gruber & Galloway, 2008;Zhang et al., 2020). By replenishing fixed N lost by denitrification and anammox, BNF promotes N availability and marine productivity. Present in a subset of diverse prokaryotes termed diazotrophs, all BNF is catalyzed by the enzyme nitrogenase in a complex, energy-intensive reaction that reduces dinitrogen (N 2 ) into ammonia (NH 3 ), which is subsequently incorporated into cell material. Diazotrophs thus function as natural gatekeepers for ecosystem N input and are critically important in oligotrophic systems, such as tropical and subtropical marine surface waters (

A diazotrophy-ammoniotrophy dual growth model for the sulfate reducing bacterium Desulfovibrio vulgaris var. Hildenborough

“…Yet, several studies in benthic environments have reported the presence of nif genes, coding for the canonical Mo-nitrogenase, in areas with relatively high bulk levels of ammonium, which have raised questions on the possible contributions of BNF to N input in the presence of NH 4 + and on the spatio-temporal complexity of benthic N cycling [36] . In support of the traditional conceptualization of BNF as a less-preferred N source, recent findings showed clear downregulation of benthic BNF activity in the presence of ammonium [11] , [13] . However, measured NH 4 + thresholds for BNF inhibition in naturally heterogeneous benthic sediments were relatively high (<30 µM NH 4 + , [13] , 0–20 µM NH 4 + , [11] ) as compared to cellular thresholds in liquid culture (<2 µM, [11] ).…”

“…In support of the traditional conceptualization of BNF as a less-preferred N source, recent findings showed clear downregulation of benthic BNF activity in the presence of ammonium [11] , [13] . However, measured NH 4 + thresholds for BNF inhibition in naturally heterogeneous benthic sediments were relatively high (<30 µM NH 4 + , [13] , 0–20 µM NH 4 + , [11] ) as compared to cellular thresholds in liquid culture (<2 µM, [11] ). This difference suggests that sediment bio-physical complexity (e.g., nutrient diffusion, remineralization, flow heterogeneity) could significantly obscure our ability to observe “true” sensitivities in various sediment types.…”

“…

Fig. 1 Summary growth dynamics of Dv H (modified from [11] ) and conceptual view of the Diazotrophic-Ammoniotrophic Dual growth model (DAD-GM) . Panel (A) illustrates the classical characteristics of DvH growth in batch culture under sub-replete initial [NH 4 + ].

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“…The main features of batch culture experiments with Dv H under sub-replete initial ammonium concentrations ([NH 4 + ] initial ) (<2300 µM, 30 mM of Pyruvate, 10 mM Sulfate, [11] ) are summarized in Fig. 1 A. Cultures exhibited a clear bi-phasic growth, with the initial growth phase supported by ammonium uptake (first ∼ 75 h.) followed by a second, diazotrophic growth phase.…”

“…Hence, during ARA experiments, diazotrophic cells acquire nitrogen to support the increase of the Cell BNF pool at only (1-Sat) % of the measured nitrogenase activity (see Table 1 ). According to measured delays in ammonium inhibition [11] , we incorporated in the model a 30 min delay between NH 4 + addition and the occurrence of the transition between diazotrophy and ammoniotrophy.…”