Methane oxidation coupled to nitrate reduction under hypoxia by the Gammaproteobacterium Methylomonas denitrificans, sp. nov. type strain FJG1

Summary Obligate methanotrophs belonging to the Phyla Proteobacteria and Verrucomicrobia require oxygen for respiration and methane oxidation; nevertheless, aerobic methanotrophs are abundant and active in low oxygen environments. While genomes of some aerobic methanotrophs encode putative nitrogen...

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Bibliographic Details
Published in:Environmental microbiology 2015-09, Vol.17 (9), p.3219-3232
Main Authors: Kits, K. Dimitri, Klotz, Martin G., Stein, Lisa Y.
Format: Article
Language:English
Subjects:
Anaerobiosis
Denitrification - genetics
Hypoxia
Inventory
Metabolism
Methane
Methane - metabolism
Methylomonas - classification
Methylomonas - genetics
Methylomonas - metabolism
Nitrate Reductase - genetics
Nitrates - metabolism
Nitrous Oxide - metabolism
Oxidation
Oxidation-Reduction
Oxidoreductases - genetics
Oxygen - metabolism
Phylogeny
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Summary:Summary Obligate methanotrophs belonging to the Phyla Proteobacteria and Verrucomicrobia require oxygen for respiration and methane oxidation; nevertheless, aerobic methanotrophs are abundant and active in low oxygen environments. While genomes of some aerobic methanotrophs encode putative nitrogen oxide reductases, it is not understood whether these metabolic modules are used for NOx detoxification, denitrification or other purposes. Here we demonstrate using microsensor measurements that a gammaproteobacterial methanotroph Methylomonas denitrificans sp. nov. strain FJG1T couples methane oxidation to nitrate reduction under oxygen limitation, releasing nitrous oxide as a terminal product. Illumina RNA‐Seq data revealed differential expression of genes encoding a denitrification pathway previously unknown to methanotrophs as well as the pxmABC operon in M. denitrificans sp. nov. strain FJG1T in response to hypoxia. Physiological and transcriptome data indicate that genetic inventory encoding the denitrification pathway is upregulated only upon availability of nitrate under oxygen limitation. In addition, quantitation of ATP levels demonstrates that the denitrification pathway employs inventory such as nitrate reductase NarGH serving M. denitrificans sp. nov. strain FJG1T to conserve energy during oxygen limitation. This study unravelled an unexpected metabolic flexibility of aerobic methanotrophs, thereby assigning these bacteria a new role at the metabolic intersection of the carbon and nitrogen cycles.
ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.12772