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.

Highlights

  • Methane (CH4) is a powerful greenhouse gas, which is released to the atmosphere from both natural and anthropogenic sources

  • We show that M. fumariolicum SolV is able to co-metabolize ethane and propane with methane or methanol, but not butane

  • The ability to use other gaseous hydrocarbons for growth is unprecedented in a particulate methane monooxygenase (pMMO)-encoding methanotroph

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Summary

Introduction

Methane (CH4) is a powerful greenhouse gas, which is released to the atmosphere from both natural and anthropogenic sources. About 70–80% of CH4 is generated biologically and a large part of it is removed in the stratosphere and troposphere through reactions with chlorine and ·OH radicals (Le Mer and Roger, 2001). Microbial methane oxidation is an important terrestrial methane sink (Conrad, 2020). Bacteria can convert CH4 to methanol aerobically using the enzyme methane monooxygenase (MMO; Conrad, 2009). Mostly methanotrophic archaea remove methane via reverse methanogenesis (Welte et al, 2016).

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