More Than a Methanotroph: A Broader Substrate Spectrum for Methylacidiphilum fumariolicum SolV

Abstract

Volcanic areas emit a number of gases including methane and other short chain alkanes, that may serve as energy source for the prevailing microorganisms. The verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV was isolated from a volcanic mud pot, and is able to grow under thermoacidophilic conditions on different gaseous substrates. Its genome contains three operons encoding a particulate methane monooxygenase (pMMO), the enzyme that converts methane to methanol. The expression of two of these pmo operons is subjected to oxygen-dependent regulation, whereas the expression of the third copy (pmoCAB3) has, so far, never been reported. In this study we investigated the ability of strain SolV to utilize short-chain alkanes and monitored the expression of the pmo operons under different conditions. In batch cultures and in carbon-limited continuous cultures, strain SolV was able to oxidize and grow on C1–C3 compounds. Oxidation of ethane did occur simultaneously with methane, while propane consumption only started once methane and ethane became limited. Butane oxidation was not observed. Transcriptome data showed that pmoCAB1 and pmoCAB3 were induced in the absence of methane and the expression of pmoCAB3 increased upon propane addition. Together the results of our study unprecedently show that a pMMO-containing methanotroph is able to co-metabolize other gaseous hydrocarbons, beside methane. Moreover, it expands the substrate spectrum of verrucomicrobial methanotrophs, supporting their high metabolic flexibility and adaptation to the harsh and dynamic conditions in volcanic ecosystems.

Growth on Formic Acid Is Dependent on Intracellular pH Homeostasis for the Thermoacidophilic Methanotroph Methylacidiphilum sp. RTK17.1

“…Congruently, the closely related, and proximally located, pmoCAB1 operon (homologous to M. infernorum V4 loci Minf_1509-1511) that is highly expressed during oxygen-replete growth on methane was only weakly transcribed. As observed in M. fumariolicum SolV (Picone et al, 2020), methylotrophic growth of Methylacidiphilum sp. RTK17.1 was accompanied by very weak expression of the pmoCAB3 operon (average FPKM = 331; Supplementary Table S1).…”

“…RTK17.1 ( Carere et al, 2019 ) and M. fumariolicum SolV ( Khadem et al, 2012a ) has previously been demonstrated in response to oxygen availability. Recently, expression of the pmoCAB3 operon was reported during the growth of M. fumariolicum SolV on methanol/ethane and methanol/propane ( Picone et al, 2020 ). This led authors to suggest that pmoCAB3 expression was linked to the absence of methane or the presence of methanol and to note that expression levels increased when propane was supplied.…”

“…In the acidophilic verrucomicrobial methanotrophs, chemolithoautotrophic growth on H 2 has been reported ( Mohammadi et al, 2016 , 2019 ; Carere et al, 2017 ), with mixotrophic growth (H 2 and CH 4 ) proposed to provide a competitive advantage over obligate methanotrophy at the oxic/anoxic soil boundaries of acidic geothermally heated soils ( Carere et al, 2017 ). A recent report that Methylacidiphilum fumariolicum SolV can utilize ethane and propane gases has further expanded the suit of substrates that can support the survival of these methanotrophs in situ ( Picone et al, 2020 ).…”

Verrucomicrobial methanotrophs grow on diverse C3 compounds and use a homolog of particulate methane monooxygenase to oxidize acetone

“…Oxidation of gaseous hydrocarbons, including propane, is also performed by strictly anaerobic sulfate-reducing bacteria in marine hydrocarbon seep environments [ 6 , 7 ]. However, studies on aerobic microbial propane oxidation in geothermal environments are rare [ 8 ]. In contrast, aerobic methane oxidation mediated by verrucomicrobial methanotrophs has been widely investigated in acidic geothermal environments [ 9 – 13 ].…”

Key Targets for Improving Algal Biofuel Production

“…As commented upon earlier, pre-treatment of algal biomass to degrade cell walls enhances the fermentative H 2 productivity up to 50-70%. In addition, genetic manipulation of microalgae using genes from methanotrophs (methane utilising bacteria-such as Methylacidiphilum fumariolicum) to increase O 2 tolerance and enhance biohydrogen production could be an approach [98].…”