Abstract
Methane oxidation is an important process to mitigate the emission of the greenhouse gas methane and further exacerbating of climate forcing. Both aerobic and anaerobic microorganisms have been reported to catalyze methane oxidation with only a few possible electron acceptors. Recently, new microorganisms were identified that could couple the oxidation of methane to nitrate or nitrite reduction. Here we investigated such an enrichment culture at the (meta) genomic level to establish a metabolic model of nitrate-driven anaerobic oxidation of methane (nitrate-AOM). Nitrate-AOM is catalyzed by an archaeon closely related to (reverse) methanogens that belongs to the ANME-2d clade, tentatively named Methanoperedens nitroreducens. Methane may be activated by methyl-CoM reductase and subsequently undergo full oxidation to carbon dioxide via reverse methanogenesis. All enzymes of this pathway were present and expressed in the investigated culture. The genome of the archaeal enrichment culture encoded a variety of enzymes involved in an electron transport chain similar to those found in Methanosarcina species with additional features not previously found in methane-converting archaea. Nitrate reduction to nitrite seems to be located in the pseudoperiplasm and may be catalyzed by an unusual Nar-like protein complex. A small part of the resulting nitrite is reduced to ammonium which may be catalyzed by a Nrf-type nitrite reductase. One of the key questions is how electrons from cytoplasmically located reverse methanogenesis reach the nitrate reductase in the pseudoperiplasm. Electron transport in M. nitroreducens probably involves cofactor F420 in the cytoplasm, quinones in the cytoplasmic membrane and cytochrome c in the pseudoperiplasm. The membrane-bound electron transport chain includes F420H2 dehydrogenase and an unusual Rieske/cytochrome b complex. Based on genome and transcriptome studies a tentative model of how central energy metabolism of nitrate-AOM could work is presented and discussed.
Highlights
Methane is an important greenhouse gas that is produced by microbiological processes, mainly methanogenesis in freshwater and marine ecosystems (Thauer et al, 2008) and the demethylation of methylphosphonates in the ocean (Metcalf et al, 2012)
The here presented genome was reconstructed from a metagenome dataset of a bioreactor enrichment culture that coupled the anaerobic oxidation of methane to nitrate reduction to nitrite and ammonium (Zhu, 2014)
When we searched the Methanoperedens protein complement for enzymes potentially responsible for nitrite-dependent ammonium production, we found proteins that were homologous to the NrfAH type cytochrome c nitrite reductase (Figure 2), an enzyme complex that is well characterized in δand ε-proteobacteria (Simon et al, 2000; Simon, 2002; Rodrigues et al, 2008)
Summary
Methane is an important greenhouse gas that is produced by microbiological processes, mainly methanogenesis in freshwater and marine ecosystems (Thauer et al, 2008) and the demethylation of methylphosphonates in the ocean (Metcalf et al, 2012). The coverage of two contigs that encoded the nitrate reductases is higher than that of the contigs containing the core proteins, the sequence composition and gene content of these contigs support their inclusion in the M. nitroreducens MPEBLZ draft genome sequence.
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