Abstract
The Favara Grande is a geothermal area located on Pantelleria Island, Italy. The area is characterized high temperatures in the top layer of the soil (60°C), low pH (3–5) and hydrothermal gas emissions mainly composed of carbon dioxide (CO2), methane (CH4), and hydrogen (H2). These geothermal features may provide a suitable niche for the growth of chemolithotrophic thermoacidophiles, including the lanthanide-dependent methanotrophs of the phylum Verrucomicrobia. In this study, we started enrichment cultures inoculated with soil of the Favara Grande at 50 and 60°C with CH4 as energy source and medium containing sufficient lanthanides at pH 3 and 5. From these cultures, a verrucomicrobial methanotroph could be isolated via serial dilution and floating filters techniques. The genome of strain AP8 was sequenced and based on phylogenetic analysis we propose to name this new species Methylacidimicrobium thermophilum AP8. The transcriptome data at μmax (0.051 ± 0.001 h−1, doubling time ~14 h) of the new strain showed a high expression of the pmoCAB2 operon encoding the membrane-bound methane monooxygenase and of the gene xoxF1, encoding the lanthanide-dependent methanol dehydrogenase. A second pmoCAB operon and xoxF2 gene were not expressed. The physiology of strain AP8 was further investigated and revealed an optimal growth in a pH range of 3–5 at 50°C, representing the first thermophilic strain of the genus Methylacidimicrobium. Moreover, strain AP8 had a KS(app) for methane of 8 ± 1 μM. Beside methane, a type 1b [NiFe] hydrogenase enabled hydrogen oxidation at oxygen concentrations up to 1%. Taken together, our results expand the knowledge on the characteristics and adaptations of verrucomicrobial methanotrophs in hydrothermal environments and add a new thermophilic strain to the genus Methylacidimicrobium.
Highlights
Methanotrophs are a diverse group of microorganisms that utilize methane (CH4) as energy source
In an attempt to enrich methanotrophic key players, volcanic soil from Pantelleria was used as inoculum in batch cultures with CH4 as energy source
Active cultures were diluted into fresh medium and one of them, grown at 50°C and pH 3, retained activity after dilution. 16S rRNA gene analysis performed on gDNA extracted from this enrichment showed the presence of a bacterial species having 97.2% identity to Methylacidimicrobium cyclopopanthes 3C, a methanotrophic species from the phylum Verrucomicrobia
Summary
Methanotrophs are a diverse group of microorganisms that utilize methane (CH4) as energy source. A new group of aerobic methanotrophs, belonging to the phylum Verrucomicrobia, has been discovered (Op den Camp et al, 2009) These verrucomicrobial methanotrophs are acidophiles so far only isolated from volcanic environments (Dunfield et al, 2007; Pol et al, 2007; Islam et al, 2008; Sharp et al, 2014; van Teeseling et al, 2014; Erikstad et al, 2019). They belong to the genera Methylacidiphilum, characterized by thermophilic strains and Methylacidimicrobium, represented by mesophilic bacteria. The CH3OH in turn is oxidized to formaldehyde (CH2O) and formate (HCOOH), and to CO2 (Picone and Op den Camp, 2019)
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