Nitrite-driven anaerobic methane oxidation by oxygenic bacteria

Abstract

Only three biological pathways are known to produce oxygen: photosynthesis, chlorate respiration and the detoxification of reactive oxygen species. Here we present 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 'Candidatus Methylomirabilis 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 oxide molecules to dinitrogen and oxygen, which was used to oxidize methane. 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.

High rates of anaerobic methane oxidation in freshwater wetlands reduce potential atmospheric methane emissions

“…Their lower d 13 C values compared with the other fatty acids in these FWW suggest a methanotrophic influence. 10-Methylhexadecanoic acid, a characteristic lipid for 'Methylomirabilis oxyfera', a freshwater bacterium capable of oxidizing methane with nitrite 33 , was either not detected at these sites or found in rather low abundance (o1.5% of all fatty acids; data not shown). This proposed biomarker for n-damo 48 was not sufficiently depleted in 13 C to unambiguously support a relationship with AOM (Supplementary Table 3); a conclusive relationship of this biomarker to AOM is complicated by the evidence for chemoorganoautotrophy of M. oxyfera 49 , in analogy to some ANME archaea 47 , and additional sources of this biomarker such as sulphate-reducing 50 and anammox bacteria 51 .…”

“…In contrast, a dominant electron acceptor for freshwater AOM has not been identified. Experimental evidence suggest sulphate is not the sole electron acceptor for AOM in freshwater sediments and peat 2,9,15,20 , and AOM in low-sulphate environments has been linked to the reduction of nitrate, nitrite, iron and manganese 4,5,12,13,16,33 . The geochemical and rate profiles in the wetlands studied here support a linkage between SR and AOM.…”

Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology ofNitrospiraspp.

“…Unraveling the microbial composition and processes occurring in these systems will not only help optimize the technical processes but can also lead to the discovery of novel pathways and organisms. In the era of next-generation sequencing techniques, metagenomics-based approaches have enabled the discovery of a suite of novel microbial pathways (Schleper et al, 2005;Bryant et al, 2007;Ettwig et al, 2010;Carrión et al, 2015) and the expansion of the tree of life (Brown et al, 2015). Some of these discoveries have been made in technical systems; for example, novel candidate phyla and expanded metabolic versatility have been identified in aerobic and anaerobic bioreactors (Wexler et al, 2005;Rinke et al, 2013;Nobu et al, 2015).…”

Microbiotes et métagénomique

“…Ceux-ci concernent, par exemple, le traitement des eaux où se produisent des étapes majeures de la minéralisation de substrats organiques dans le déroulement des cycles du carbone, de l'azote et du phosphore. De nouvelles étapes de ces cycles, comme le processus anammox (anaerobic ammonium oxidation) [28], ou l'oxydation anaérobie du méthane [29] [25]. Pour le moment ces signes espérés de raréfac-tion s'observent surtout au niveau de biomes très étudiés (Figure 2).…”