A nitrite-oxidising bacterium constitutively consumes atmospheric hydrogen

• Published in: The ISME Journal 2022-09, Vol.16 (9), p.2213-2219
• Main Authors: Leung, Pok Man, Daebeler, Anne, Chiri, Eleonora, Hanchapola, Iresha, Gillett, David L., Schittenhelm, Ralf B., Daims, Holger, Greening, Chris
• Format: Article
• Language: English
• Subjects: 631/158/855; 631/326/171; 631/443/319; 82/58; Affinity; Alternative energy; Alternative energy sources; Bacteria; Biomedical and Life Sciences; Depletion; Ecology; Energy expenditure; Evolutionary Biology; Hydrogen; Hydrogenase; Life Sciences; Microbial Ecology; Microbial Genetics and Genomics; Microbiology; Natural environment; Nickel; Nickel iron; Nitrification; Nitrites; Nitrospira; Oxidation; Proteomics; Substrates; Survival; Thermodynamic models
• ISSN: 1751-7362; 1751-7370
• DOI: 10.1038/s41396-022-01265-0

Chemolithoautotrophic nitrite-oxidising bacteria (NOB) of the genus Nitrospira contribute to nitrification in diverse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternative energy sources. Here, we demonstrate that the canonical nitrite oxidiser Nitrospira moscoviensis oxidises hydrogen (H 2 ) below atmospheric levels using a high-affinity group 2a nickel-iron hydrogenase [ K m(app) = 32 nM]. Atmospheric H 2 oxidation occurred under both nitrite-replete and nitrite-deplete conditions, suggesting low-potential electrons derived from H 2 oxidation promote nitrite-dependent growth and enable survival during nitrite limitation. Proteomic analyses confirmed the hydrogenase was abundant under both conditions and indicated extensive metabolic changes occur to reduce energy expenditure and growth under nitrite-deplete conditions. Thermodynamic modelling revealed that H 2 oxidation theoretically generates higher power yield than nitrite oxidation at low substrate concentrations and significantly contributes to growth at elevated nitrite concentrations. Collectively, this study suggests atmospheric H 2 oxidation enhances the growth and survival of NOB amid variability of nitrite supply, extends the phenomenon of atmospheric H 2 oxidation to an eighth phylum (Nitrospirota), and reveals unexpected new links between the global hydrogen and nitrogen cycles. Long classified as obligate nitrite oxidisers, our findings suggest H 2 may primarily support growth and survival of certain NOB in natural environments.