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Abstract:
Only three biological pathways are known to produce oxygen: photosynthesis, chlorate respiration and the detoxification of
reactive oxygen species.Herewepresent evidence for a fourth pathway, possibly of considerable geochemical and evolutionary
importance. The pathway was discovered after metagenomic sequencing of an enrichment culture that couples anaerobic
oxidation of methane with the reduction of nitrite to dinitrogen. The complete genome of the dominant bacterium, named
‘CandidatusMethylomirabilis oxyfera’, was assembled. This apparently anaerobic, denitrifying bacterium encoded, transcribed
and expressed the well-established aerobic pathway for methane oxidation, whereas it lacked known genes for dinitrogen
production. Subsequent isotopic labelling indicated that ‘M. oxyfera’ bypassed the denitrification intermediate nitrous oxide by
the conversion of two nitric oxidemolecules to dinitrogen and oxygen,whichwas used to oxidizemethane.These results extend
our understanding of hydrocarbon degradation under anoxic conditions and explain the biochemical mechanism of a poorly
understood freshwater methane sink. Because nitrogen oxides were already present on early Earth, our finding opens up the
possibility that oxygen was available to microbial metabolism before the evolution of oxygenic photosynthesis.
