Verrucomicrobial methanotrophs: ecophysiology of metabolically versatile acidophiles

Abstract

Methanotrophs are an important group of microorganisms that counteract methane emissions to the atmosphere. Methane-oxidising bacteria of the Alpha- and Gammaproteobacteria have been studied for over a century, while methanotrophs of the phylum Verrucomicrobia are a more recent discovery. Verrucomicrobial methanotrophs are extremophiles that live in very acidic geothermal ecosystems. Currently, more than a dozen strains have been isolated, belonging to the genera Methylacidiphilum and Methylacidimicrobium. Initially, these methanotrophs were thought to be metabolically confined. However, genomic analyses and physiological and biochemical experiments over the past years revealed that verrucomicrobial methanotrophs, as well as proteobacterial methanotrophs, are much more metabolically versatile than previously assumed. Several inorganic gases and other molecules present in acidic geothermal ecosystems can be utilised, such as methane, hydrogen gas, carbon dioxide, ammonium, nitrogen gas and perhaps also hydrogen sulfide. Verrucomicrobial methanotrophs could therefore represent key players in multiple volcanic nutrient cycles and in the mitigation of greenhouse gas emissions from geothermal ecosystems. Here, we summarise the current knowledge on verrucomicrobial methanotrophs with respect to their metabolic versatility and discuss the factors that determine their diversity in their natural environment. In addition, key metabolic, morphological and ecological characteristics of verrucomicrobial and proteobacterial methanotrophs are reviewed.

Metagenome Assembled Genome of a Novel Verrucomicrobial Methanotroph From Pantelleria Island

“…One single pmoCAB operon and a pmoD subunit, encoding a copper-binding protein ( Fisher et al, 2018 ), were found in MAG9, whereas no other mmo genes were identified ( Table 3 ). This is in line with previously described verrucomicrobial methanotrophs, although the number of pmo operons seems to be variable ( Op den Camp et al, 2009 ; van Teeseling et al, 2014 ; Erikstad et al, 2019 ; Picone et al, 2020 ; Schmitz et al, 2021 ). The PmoA phylogenetic tree including strain PQ17 ( Supplementary Figure 3 ) supports the phylogeny derived from 16S rRNA gene analysis.…”

“…Phylogenetic analysis showed that the 16S rRNA gene of MAG9 clustered in between Methylacidimicrobium and Methylacidiphilum species ( Figure 1 ; Dunfield et al, 2007 ; Pol et al, 2007 ; Op den Camp et al, 2009 ; van Teeseling et al, 2014 ; Schmitz et al, 2021 ). The 16S rRNA and AAI values ( Table 1 and Supplementary Table 1 ) fell below the threshold for species delimitation (95% for AAI and 98.7–99% for 16S rRNA) ( Stackebrandt and Ebers, 2006 ; Thompson et al, 2013 ).…”

“…This “ Ca. Methylacidithermus” genus is the third genus of methanotrophic Verrucomicrobia within the family Methylacidiphilaceae, that adds to the previously described Methylacidiphilum and Methylacidimicrobium genera ( Op den Camp et al, 2009 ; van Teeseling et al, 2014 ; Schmitz et al, 2021 ).…”

“…Subunits for a canonical complex III could not be retrieved. The verrucomicrobial methanotrophs, including strain PQ17, possess genes encoding an Alternative Complex III, a structurally different protein complex with similar function (MPNT_10279-10285) ( Refojo et al, 2012 ; Schmitz et al, 2021 ). Finally, the electrons are transferred to complex IV and the F 0 F 1 ATP synthase (complex V) generating ATP using the proton motive force ( Supplementary Table 3 ).…”

“…Cyanate can act as energy and nitrogen source for nitrifiers (Palatinszky et al, 2015) and its presence has been detected in other verrucomicrobial methanotrophs (Picone et al, 2021). Unlike other verrucomicrobial methanotrophs, genes encoding a nitrogenase enzyme could not be found (Op den Camp et al, 2009;Khadem et al, 2010;Schmitz et al, 2021). Fixed ammonium is mostly used for biosynthetic purposes, but some ammonium is also converted into hydroxylamine by pmoA, which is a structural homolog of ammonium monooxygenase amoA (Sirajuddin and Rosenzweig, 2015).…”