Abstract
Nitric oxide (NO) has important functions in biology and atmospheric chemistry as a toxin, signaling molecule, ozone depleting agent and the precursor of the greenhouse gas nitrous oxide (N2O). Although NO is a potent oxidant, and was available on Earth earlier than oxygen, it is unclear whether NO can be used by microorganisms for growth. Anaerobic ammonium-oxidizing (anammox) bacteria couple nitrite reduction to ammonium oxidation with NO and hydrazine as intermediates, and produce N2 and nitrate. Here, we show that the anammox bacterium Kuenenia stuttgartiensis is able to grow in the absence of nitrite by coupling ammonium oxidation to NO reduction, and produce only N2. Under these growth conditions, the transcription of proteins necessary for NO generation is downregulated. Our work has potential implications in the control of N2O and NO emissions from natural and manmade ecosystems, where anammox bacteria contribute significantly to N2 release to the atmosphere. We hypothesize that microbial NO-dependent ammonium oxidation may have existed on early Earth.
Highlights
In microbial processes, Nitric oxide (NO) is either generated via nitrite reduction catalyzed by Cu-containing (Cu-NIR) or cytochrome cd1-containing nitrite reductases[7,9], or alternatively by hydroxylamine oxidation catalyzed by octaheme hydroxylamine oxidoreductases (HAO)[6,10]
All continuous bioreactors were operated with free-living planktonic K. stuttgartiensis cell cultures for more than 50 days (~5 generations)
In reactor II, where NO was supplied as an additional substrate next to ammonium and nitrite, NO consumption was accompanied with an increase in ammonium oxidation, in line with an earlier study that used flocculent biomass[24]
Summary
NO is either generated via nitrite reduction catalyzed by Cu-containing (Cu-NIR) or cytochrome cd1-containing (cd1-NIR) nitrite reductases[7,9], or alternatively by hydroxylamine oxidation catalyzed by octaheme hydroxylamine oxidoreductases (HAO)[6,10]. Anaerobic ammonium-oxidizing (anammox) bacteria use the oxidative power of NO to activate ammonium in the absence of oxygen These microorganisms normally use nitrite as their terminal electron acceptor, producing nitrate and N215. Reactions (2) and (3) would be sufficient both to conserve energy and supply necessary electrons for cell carbon fixation (CO2) for biomass In this scenario, three of the four electrons released from hydrazine oxidation would be used for hydrazine synthesis, and the remaining electron could be used for biomass production, without the need for nitrite oxidation to nitrate. We show that K. stuttgartiensis is able to use NO as its terminal electron acceptor, and conserve energy and grow by coupling NO reduction to ammonium oxidation in the absence of nitrite Under these conditions, nitrate is not produced and the sole end product is N2. Using comparative transcriptomics and proteomics, we demonstrate that when growing on NOdependent ammonium oxidation, K. stuttgartiensis down regulates the transcription of proteins responsible for NO generation as well as nitrite oxidation
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