Nitrification in acidic and alkaline environments

Abstract

Aerobic nitrification is a key process in the global nitrogen cycle mediated by microorganisms. While nitrification has primarily been studied in near-neutral environments, this process occurs at a wide range of pH values, spanning ecosystems from acidic soils to soda lakes. Aerobic nitrification primarily occurs through the activities of ammonia-oxidising bacteria and archaea, nitrite-oxidising bacteria, and complete ammonia-oxidising (comammox) bacteria adapted to these environments. Here, we review the literature and identify knowledge gaps on the metabolic diversity, ecological distribution, and physiological adaptations of nitrifying microorganisms in acidic and alkaline environments. We emphasise that nitrifying microorganisms depend on a suite of physiological adaptations to maintain pH homeostasis, acquire energy and carbon sources, detoxify reactive nitrogen species, and generate a membrane potential at pH extremes. We also recognize the broader implications of their activities primarily in acidic environments, with a focus on agricultural productivity and nitrous oxide emissions, as well as promising applications in treating municipal wastewater.

Keywords: archaea; metabolism; nitrification.

Figure 1. Differences in proton motive force composition under acidic, neutral and alkaline conditions.

ΔpH contributes to proton motive force (PMF) generation under acidic and neutral conditions, and detracts from proton motive force under alkaline conditions at 25°C. This is illustrated with examples from the obligate acidophile Acidithiobacillus ferrooxidans, the neutralophile Escherichia coli, and facultative alkaliphile Bacillus pseudofirmus OF4; adapted from Krulwich et al., 2011 [5].

Figure 2. Comparisons of concentrations of nitrogen and carbon sources for nitrifying microorganisms from pH 1 to 14.

These comparisons are based on pK_a values (NH₄⁺/NH₃ = 9.25, HNO₂/NO₂⁻ = 3.39, CO₂/HCO₃⁻ = 6.37, HCO₃⁻/CO₃²⁻ = 10.32), calculated using 1 mM total concentration for ammonia (orange, solid) and ammonium (orange, dashed); nitrite (blue, solid) and nitrous acid (blue, dashed); and 10 mM total concentration for bicarbonate (green, solid), carbon dioxide (green, dashed) and carbonate (green, dash dot).

Figure 3. Conceptual diagrams of substrate acquisition and pH homeostasis systems encoded in the genomes of nitrifiers.

(A) AOA Ca. Nitrosotalea devaniterrae based on illustrations in Lehtovira-Morley et al., 2016 [44]. (B) The intracytoplasmic membrane stacks based on illustration and electron micrographs of Ca. Nitrosacidococcus tergens RJ19 in Picone et al., 2020 [23]. The cation transporters and Na⁺/H⁺ antiporters provide pH homeostasis capabilities. (C) Proposed allocations of AMO and HAO on the intracytoplasmic membrane stacks according to electron microgram of Nitrosomonas halophila Ans1 [84]. The presence of respiratory complexes is inferred from the model pathway of N. halophila Nm1 at Biocyc.org [88]. Respiratory complexes I to V are indicated by roman numerals in panels (B and C); HP/HB, the hydroxypropionate/hydroxybutyrate cycle; TCA, the tricarboxylic acid cycle; CBB, Calvin–Benson–Bassham cycle; CA, carbonic anhydrase.