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Response of the anaerobic methanotroph ' Candidatus Methanoperedens nitroreducens' to oxygen stress.

' Candidatus Methanoperedens nitroreducens' is an archaeon that couples the anaerobic oxidation of methane to nitrate reduction. In natural and man-made ecosystems, this archaeon is often found at oxic-anoxic interfaces where nitrate, the product of aerobic nitrification, co-occurs with methane produced by methanogens. As such, populations of ' Ca M. nitroreducens' could be prone to regular oxygen exposure. Here, we investigated the effect of 5% (v/v) oxygen exposure on a ' Ca M. nitroreducens' culture enriched from an Italian paddy field, in batch activity assays. Metagenome sequencing of the DNA extracted from the enrichment culture revealed that 83% of 16S rRNA gene reads were assigned to a novel strain of ' Ca. M. nitroreducens Verserenetto'. RNA was extracted and metatranscriptome sequencing upon oxygen exposure, revealed that the active community changed, most notably in the appearance of aerobic methanotrophs. The gene expression of ' Ca M. nitroreducens' revealed that the key genes encoding enzymes of the methane oxidation and nitrate reduction pathways were down regulated. In contrast to this, we identified upregulation of glutaredoxin, thioredoxin family/like proteins, rubrerythrins, peroxiredoxins, peroxidase, alkyl hydroperoxidase, type A flavoproteins, FeS cluster assembly protein and cysteine desulfurases, indicating the genomic potential of ' Ca. M. nitroreducens Verserenetto' to counteract the oxidative damage and adapt in environments where they might be exposed to regular oxygen intrusion. Importance 'Candidatus Methanoperedens nitroreducens' are anaerobic archaea which couple the reduction of nitrate to the oxidation of methane. These microorganisms are present in a wide range of aquatic environments and man-made ecosystems such as paddy fields and wastewater treatments. In such environments they may experience regular oxygen exposure.Yet ' Ca M. nitroreducens' are able to thrive under such conditions and could be applied for the simultaneous removal of dissolved methane and nitrogenous pollutants in oxygen-limited systems. To understand what machinery ' Ca M. nitroreducens' possesses to counteract the oxidative stress and survive, we characterized the response to oxygen exposure using a multi-omics approach.

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