Abstract
Methanotrophic verrucomicrobia of the order Methylacidiphilales are known as extremely acidophilic, thermophilic or mesophilic bacteria that inhabit acidic geothermal ecosystems. The occurrence of verrucomicrobial methanotrophs in other types of acidic environments remains an open question. Notably, Methylacidiphilales-affiliated 16S rRNA gene sequences are commonly retrieved from acidic (pH 3.5–5.5) peatlands. In this study, we compared the patterns of verrucomicrobial diversity in four acidic raised bogs and six neutral fens located in European North Russia. Methylacidiphilales-like 16S rRNA gene reads displaying 83–86% similarity to 16S rRNA gene sequences of currently described verrucomicrobial methanotrophs were recovered exclusively from raised bogs. Laboratory incubation of peat samples with 10% methane for 3 weeks resulted in the pronounced increase of a relative abundance of alphaproteobacterial methanotrophs, while no response was detected for Methylacidiphilales-affiliated bacteria. Three metagenome-assembled genomes (MAGs) of peat-inhabiting Methylacidiphilales bacteria were reconstructed and examined for the presence of genes encoding methane monooxygenase enzymes and autotrophic carbon fixation pathways. None of these genomic determinants were detected in assembled MAGs. Metabolic reconstructions predicted a heterotrophic metabolism, with a potential to hydrolyze several plant-derived polysaccharides. As suggested by our analysis, peat-inhabiting representatives of the Methylacidiphilales are acidophilic aerobic heterotrophs, which comprise a sister family of the methanotrophic Methylacidiphilaceae.
Highlights
The occurrence of methanotrophic capabilities in members of the bacterial phylum Verrucomicrobia was discovered fifteen years ago in three independent studies that focused on exploring methanotrophic microbial communities of three geographically remote acidic geothermal sites located in New Zealand, Italy and Kamchatka [1,2,3]
The three originally obtained isolates of methanotrophic verrucomicrobia, strains V4, SolV and Kam1, were represented by thermophilic and extremely acidophilic bacteria, which grew at 37–65 ◦ C in the pH range between 0.8 and 5.0
A total of 2,174,164 partial 16S rRNA gene sequences were retrieved from the examined peat samples
Summary
The occurrence of methanotrophic capabilities in members of the bacterial phylum Verrucomicrobia was discovered fifteen years ago in three independent studies that focused on exploring methanotrophic microbial communities of three geographically remote acidic geothermal sites located in New Zealand, Italy and Kamchatka [1,2,3]. Extensive studies of verrucomicrobial methanotrophs over the past years revealed their high metabolic versatility (reviewed by Schmitz et al [9]) These bacteria seem to be key players in multiple volcanic nutrient cycles and can utilize several gases and other compounds present in acidic geothermal ecosystems, such as methane, H2 , CO2 , N2 , ammonium and perhaps hydrogen sulfide [8,9]. A number of other cultivation-independent studies reported the retrieval of Methylacidophilales-affiliated 16S rRNA gene sequences from acidic peatlands, mainly raised bogs [12,13,14]. These sequences, displayed only a low similarity (83–87%) to 16S rRNA gene sequences of currently described verrucomicrobial methanotrophs. Peat-inhabiting Methylacidophilales are aerobic chemoorganotrophic bacteria with some hydrolytic capabilities, which comprise a sister family of the methanotrophic Methylacidiphilaceae
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