Methane oxidation at 55°C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum

Abstract

Methanotrophic bacteria constitute a ubiquitous group of microorganisms playing an important role in the biogeochemical carbon cycle and in control of global warming through natural reduction of methane emission. These bacteria share the unique ability of using methane as a sole carbon and energy source and have been found in a great variety of habitats. Phylogenetically, known methanotrophs constitute a rather limited group and have so far only been affiliated with the Proteobacteria. Here, we report the isolation and initial characterization of a nonproteobacterial obligately methanotrophic bacterium. The isolate, designated Kam1, was recovered from an acidic hot spring in Kamchatka, Russia, and is more thermoacidophilic than any other known methanotroph, with optimal growth at Ϸ55°C and pH 3.5. Kam1 is only distantly related to all previously known methanotrophs and belongs to the Verrucomicrobia lineage of evolution. Genes for methane monooxygenases, essential for initiation of methane oxidation, could not be detected by using standard primers in PCR amplification and Southern blot analysis, suggesting the presence of a different methane oxidation enzyme. Kam1 also lacks the well developed intracellular membrane systems typical for other methanotrophs. The isolate represents a previously unrecognized biological methane sink, and, due to its unusual phylogenetic affiliation, it will shed important light on the origin, evolution, and diversity of biological methane oxidation and on the adaptation of this process to extreme habitats. Furthermore, Kam1 will add to our knowledge of the metabolic traits and biogeochemical roles of the widespread but poorly understood Verrucomicrobia phylum.extremophile ͉ methanotroph

Real-time detection of actively metabolizing microbes by redox sensing as applied to methylotroph populations in Lake Washington

“…These results suggest that these organisms may be involved in metabolism of methane in the site, either directly or indirectly. Indeed, methanotrophic Verrucomicrobiales have been described recently from acidic environments (Dunfield et al 2007;Pol et al, 2007;Islam et al, 2008) and our data suggest the existence of methanotrophic Verrucomicrobiales in freshwater lakes.…”

Active methylotrophs in the sediments of Lonar Lake, a saline and alkaline ecosystem formed by meteor impact

“…One of them showed maximum identity to the 16S rRNA gene of an uncultured Verrucomicrobium clone obtained from alkaline Mono Lake (Humayoun et al, unpublished). This sequence did not, however, cluster with that of thermo-acidophilic Verrucomicrobia methanotrophs (Dunfield et al, 2007;Pol et al, 2007;Islam et al, 2008) (Figure 3).…”

“…Methanotrophs are a specialized group of methylotrophs that use methane as the sole carbon and energy source. These are distributed among Gammaproteobacteria (type I methanotrophs), Alphaproteobacteria (type II methanotrophs) (reviewed in Trotsenko and Murrell, 2008), filamentous methane oxidizers (Stoecker et al, 2006;Vigliotta et al, 2007) and Verrucomicrobia (Dunfield et al, 2007;Pol et al, 2007;Islam et al, 2008). Methanotrophs oxidize methane to methanol by the enzyme methane monooxygenase (MMO), present either as the particulate form (pMMO) in all characterized methanotrophs (except in the genus Methylocella (Dedysh et al, 2000)) or as the soluble form (sMMO) in some methanotrophs (Trotsenko and Murrell, 2008).…”

One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic–anoxic interface in a flooded paddy soil

“…RNA samples were reverse transcribed with random hexamer primers and SuperScript III reverse transcriptase (Invitrogen, Darmstadt, Germany). Amplification of mmoX gene and transcript sequences was done using (i) primer set mmoX206f/886r (Hutchens et al, 2004), (ii) primer set mmoXf92/r1430 (Islam et al, 2008), and (iii) primer set mmoXLF/LR (Rahman et al, 2011). Primer set mmoX206f/886r covers a fairly wide range of mmoX diversity, whereas mmoXf92/r1430 includes verrrucomicrobial sequences.…”