A collaboration between the Radboud University Nijmegen, Wageningen University & Research and the Ludwig Maximilian University Munich.
When thinking of biological hydrogen oxidation we often consider microorganisms in animal guts and leguminous soils. Indeed, hydrogen gas is used as an energy source by many microorganisms and could even be one of the first available substrates on early Earth. In the atmosphere, only one out of two million molecules is a hydrogen gas molecule. Specialized microorganisms in soil that possess group 1h [NiFe] hydrogenases can scavenge hydrogen gas from the atmosphere to persist during dormancy. Remarkably, this enzyme is also encoded in the genome of the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV. This bacterium was isolated from a hot and acidic mud pot inside the Solfatara crater near Naples (Italy) more than a decade ago (Image 1). Surprisingly, this extremophile is able to grow below pH 1 and belongs to a phylum formerly unknown to comprise methanotrophs: the Verrucomicrobia. Moreover, this microorganism needs rare earth elements for growth and its genome suggests that many alternative substrates found in volcanic ecosystems can be used as alternative energy sources.
Image 1: Sampling by dr. Arjan Pol in the natural environment of strain SolV: a mud pool at the Solfatara near Naples (Italy).
M. fumariolicum SolV was isolated on methane, but can also make a living as a “Knallgas” bacterium, oxidizing hydrogen gas. Unlike other atmospheric hydrogen-oxidizing microbes, this bacterium uses the group 1h [NiFe] hydrogenase to rapidly grow on this substrate. Furthermore, this hydrogenase type seems to be much more oxygen-tolerant than other hydrogenases found in nature. In our new study, we show that M. fumariolicum SolV cannot only grow on hydrogen gas with this enzyme, but also use it to oxidize subatmospheric hydrogen gas (Image 2). We purified and characterized the hydrogenase and found it to be an extremely thermostable membrane-associated protein with high affinity for hydrogen gas. The ability of a methanotroph to consume such a broad range of hydrogen gas concentrations as additional energy source provides a major advantage in ecosystems where methane availability fluctuates. Consequently, we propose that the group 1h [NiFe] hydrogenase provides M. fumariolicum SolV a survival benefit that could therefore enhance mitigation of methane emissions from methanotrophic ecosystems.
Image 2: Subatmospheric H2 oxidation by Hyd-1h in cells of Methylacidiphilum fumariolicum SolV. The dashed line indicates the atmospheric H2 concentration (0.53 ppmv). The arrows indicate when hydrogen gas was added. 120 mL capped serum bottles were inoculated with 10 mL (OD600 = 0.12) heat-killed cells (HK) or viable cells (VC). At 29 h, H2 was again supplemented to VC. Error bars indicate standard deviations (n=3).
Studying microorganisms from ecosystems with harsh conditions is interesting for many reasons. Most importantly, many greenhouse gases and gases with a detrimental effect on the environment are emitted from such systems. Most notably, these gases are methane, carbon dioxide, carbon monoxide, sulfur dioxide and hydrogen sulfide. Understanding what microorganisms do with these compounds and to what extend, is pivotal to understanding a changing climate. Microorganisms control the Earth and should therefore always be taken into account when constructing models to predict the future of our planet. With our new paper, we hope to encourage the research community to continue investigating alternative substrates for methanotrophs, to feed the models to predict and assess the future climate of our planet.