Peat-Inhabiting Verrucomicrobia of the Order Methylacidiphilales Do Not Possess Methanotrophic Capabilities

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.

Microbial sensitivity to temperature and sulfate deposition modulates greenhouse gas emissions from peat soils

“…Enhanced dissociation of Sphagnum ‐derived polysaccharides was partly inferred from increased unique (absent in control) phenolic constituent in the porewater DOM after sulfate addition at T1 (Figure S12) and increased Fe concentration (Figure S17) due to the pH fluctuation (Figure S10a) and acid‐catalyzed reactions (potentially abiotic decomposition, Figure S13) and partly due to the shifts within microbial functional guilds and taxonomic shifts to decompose plant‐derived material via cellulolysis and xylanolysis (Figure 4d; Figure S15). An increase in the relative abundance of Methylacidiphilales order from the Verrucomicrobia phylum and Solibacterales order from the Acidobacteria phylum, capable of anaerobic hydrolysis of several plant‐derived polysaccharides (Dedysh et al, 2021; Hester et al, 2018), coupled with an increase in the relative abundance of obligate anaerobes in Holophagales order capable of fermenting several aromatic compounds to acetate (Fukunaga & Ichikawa, 2014) further supports the prevalence of additional sources for the SRBs activity. Organisms in Desulfovibrionales order are further shown to oxidize organic substrates such as phenolic constituents and humic substances incompletely to acetate (Kuever, 2014); thus, the disappearances of the labile phenolic constituents at T4 and T6 in sulfate‐amended samples (Figure S12) could be attributed to the SRB capabilities to produce the substrates for sulfate reduction directly.…”

Genome analysis of the candidate phylum MBNT15 bacterium from a boreal peatland predicted its respiratory versatility and dissimilatory iron metabolism

“…Microbial diversity patterns in two types of boreal peatlands, raised bogs and eutrophic fens, analyzed using the 16S rRNA gene profiling, were described previously ( Dedysh et al, 2021 ) and deposited in sequence read archive (SRA) under the accession numbers SRR11280489 – SRR11280524 (BioProject PRJNA610704 ). The peat samples for 16S rRNA gene profiling were obtained from four raised bogs (Shichengskoe, Piyavochnoe, Barskoe, and Alekseevskoe) and six eutrophic fens (Shichengskoe, Piyavochnoe, Rodionskoe, Ileksa, Povreka, and Charozerskoe) located in the Vologda region of European North Russia, within the zone of middle taiga.…”

“…The peat samples for 16S rRNA gene profiling were obtained from four raised bogs (Shichengskoe, Piyavochnoe, Barskoe, and Alekseevskoe) and six eutrophic fens (Shichengskoe, Piyavochnoe, Rodionskoe, Ileksa, Povreka, and Charozerskoe) located in the Vologda region of European North Russia, within the zone of middle taiga. Detail description of the sampling sites was reported previously ( Ivanova et al, 2020 ; Dedysh et al, 2021 ), as well as their physicochemical characteristics ( Dedysh et al, 2021 ).…”

Biogeography of microbial communities in high‐latitude ecosystems: Contrasting drivers for methanogens, methanotrophs and global prokaryotes

“…The presence of Methylacidiphilaceae in very acid samples (pH <4,7) is also in line with the extremely acidophilic nature of their unique representant, Methylacidiphilum , with optimal growth below pH 3.5 (Op den Camp et al, 2009). It is also noteworthy that this family is adapted to CH 4 and O 2 limitation (Carere et al, 2017; Smith and Wrighton, 2019) and shows a large temperature tolerance, being found from thermophilic environments (Dunfield et al, 2007; van Teeseling et al, 2014) to high latitudes (Bashenkhaeva et al, 2020; Dedysh et al, 2021; Zakharova et al, 2021).…”