Nitrifier adaptation to low energy flux controls inventory of reduced nitrogen in the dark ocean

Abstract

Ammonia oxidation to nitrite and its subsequent oxidation to nitrate provides energy to the two populations of nitrifying chemoautotrophs in the energy-starved dark ocean, driving a coupling between reduced inorganic nitrogen (N) pools and production of new organic carbon (C) in the dark ocean. However, the relationship between the flux of new C production and the fluxes of N of the two steps of oxidation remains unclear. Here, we show that, despite orders-of-magnitude difference in cell abundances between ammonia oxidizers and nitrite oxidizers, the two populations sustain similar bulk N-oxidation rates throughout the deep waters with similarly high affinities for ammonia and nitrite under increasing substrate limitation, thus maintaining overall homeostasis in the oceanic nitrification pathway. Our observations confirm the theoretical predictions of a redox-informed ecosystem model. Using balances from this model, we suggest that consistently low ammonia and nitrite concentrations are maintained when the two populations have similarly high substrate affinities and their loss rates are proportional to their maximum growth rates. The stoichiometric relations between the fluxes of C and N indicate a threefold to fourfold higher C-fixation efficiency per mole of N oxidized by ammonia oxidizers compared to nitrite oxidizers due to nearly identical apparent energetic requirements for C fixation of the two populations. We estimate that the rate of chemoautotrophic C fixation amounts to ∼1 × 1013to ∼2 × 1013mol of C per year globally through the flux of ∼1 × 1014to ∼2 × 1014mol of N per year of the two steps of oxidation throughout the dark ocean.

Simulation of Enhanced Growth of Marine Group II Euryarchaeota From the Deep Chlorophyll Maximum of the Western Pacific Ocean: Implication for Upwelling Impact on Microbial Functions in the Photic Zone

“…The radiocarbon signatures of thaumarchaeal DNA demonstrated that MGI members derive the majority of their carbon from inorganic carbon fixation from the same site (Hansman et al, 2009). A recent quantitative study of the amoA and accA genes in the western Pacific revealed similar distributional trends at depths greater than or equal to 100 m as those documented in our study (Zhang et al, 2020). Our sequencing data showed that in 400 m, the distribution trend of 16S rRNA, amoA, and accA genes was highly consistent, confirming that the ammonia oxidation process of AOA and the fixation of carbon dioxide were mutually coupled in our culture experiments (Supplementary Figure S1).…”

Genomic and kinetic analysis of novel Nitrospinae enriched by cell sorting

“…N. vancouverensis" is also most closely related to the Nitrospinae clades 1 and 2 that are abundant in oligotrophic waters [20] (see above). However, its K m(app) is still 1-2 342 orders of magnitude higher than the K m(app) values of nitrite oxidation reported for environmental 343 samples from an OMZ (0.254±0.161 μM NO 2 -) and South China Sea waters (0.03 to 0.5 µM) 344 [22,57]. The very high nitrite affinity observed with these samples might be explained by the 345 presence of uncharacterized nitrite oxidizers, whose nitrite affinity exceeds that of all cultured 346 NOB.…”

“…In addition to their importance in the nitrogen cycle, the Nitrospinae have been suggested to play a major role in dark ocean carbon fixation by contributing up to 15-45% of the fixed inorganic carbon in some environments [20]. The contribution of Nitrospinae to CO 2 63 fixation is, however, still under debate [21,22], partially due to a lack of cultured representative 64 organisms.…”

Genomic and Physiological Characteristics of a Novel Nitrite-Oxidizing Nitrospira Strain Isolated From a Drinking Water Treatment Plant

“…Strain KM1 had the lowest value among cultured NOB from non-marine habitats. According to a recent study, in situ kinetic values for nitrite oxidation in the dark ocean were at nanomolar levels and orders of magnitude lower than the K m(app) values of cultured NOB (Zhang et al, 2020). This would suggest uncultured NOB are well-adapted to oligotrophic environments in nature.…”