Nitric oxide-dependent anaerobic ammonium oxidation

Nitric oxide (NO) is a central molecule in atmospheric chemistry as it is involved in ozone depletion and greenhouse gas emissions. Its high reactivity renders NO a potent toxin, and microorganisms usually detoxify it to less reactive nitrous oxide (N2O). Even though NO is a very potent oxidant, and was available in the history of earth earlier than oxygen, no microorganisms that use NO as the terminal electron acceptor have been discovered. Here we show that anaerobic ammonium-oxidizing bacteria that oxidize ammonium and nitrite to N2, are able to use NO as their terminal electron acceptor and gain energy for growth. Using highly enriched (>95%) free-living cell cultures of anammox bacterium Kuenenia stuttgartiensis, we could demonstrate that these microorganisms convert NO and ammonium to N2. Metatranscriptomic and metaproteomic analyses of this culture indicated that pathways necessary for NO generation were significantly downregulated at the transcription level, and suggested that a hydroxylamine oxidoreductase-like protein could be functioning as nitrite reductase in Kuenenia stuttgartiensis. Our results show that anammox bacteria do not produce N2O from NO, and therefore, are central in preventing N2O emissions from natural and manmade ecosystems, where they contribute significantly to N2 release to the atmosphere.