Trace gas oxidation sustains energy needs of a thermophilic archaeon at suboptimal temperatures.

Diverse aerobic bacteria use atmospheric hydrogen (H2) and carbon monoxide (CO) as energy sources to support growth and survival. Such trace gas oxidation is recognised as a globally significant process that serves as the main sink in the biogeochemical H2 cycle and sustains microbial biodiversity in oligotrophic ecosystems. However, it is unclear whether archaea can also use atmospheric H2. Here we show that a thermoacidophilic archaeon, Acidianus brierleyi (Thermoproteota), constitutively consumes H2 and CO to sub-atmospheric levels. Oxidation occurs across a wide range of temperatures (10 to 70 °C) and enhances ATP production during starvation-induced persistence under temperate conditions. The genome of A. brierleyi encodes a canonical CO dehydrogenase and four distinct [NiFe]-hydrogenases, which are differentially produced in response to electron donor and acceptor availability. Another archaeon, Metallosphaera sedula, can also oxidize atmospheric H2. Our results suggest that trace gas oxidation is a common trait of Sulfolobales archaea and may play a role in their survival and niche expansion, including during dispersal through temperate environments.

Interaction between ferruginous clay sediment and an iron-reducing hyperthermophilic Pyrobaculum sp. in a terrestrial hot spring.

Green-coloured sediments in low-temperature geothermal surface features are typically indicative of photosynthetic activity. A near-boiling (89-93°C), alkali-chloride spring in the Taupo Volcanic Zone, New Zealand, was observed to have dark green sediments despite being too hot to support any known photosynthetic organisms. Analysis of aqueous and sediment microbial communities via 16S rRNA amplicon sequencing revealed them to be dominated by Aquifex spp., a genus of known hyperthermophilic hydrogen-oxidisers (69%-91% of operational taxonomic units (OTUs)), followed by groups within the Crenarchaeota (3%-20%), including the known iron-reducing genus Pyrobaculum. Cultivation experiments suggest that the green colouration of clay sediments in this spring may be due in part to ferruginous clays and associated compounds serving as substrates for the iron-reducing activity of low-abundance Pyrobaculum spp. These findings demonstrate the dynamic nature of microbe-mineral interactions in geothermal environments, and the potential ability of the rarer biosphere (1%-2% of observed sequences, cell densities of 450-33 000 g-1 sediment) to influence mineral formation at a macro-scale.

Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging.

The majority of microbial cells in global soils exist in a spectrum of dormant states. However, the metabolic processes that enable them to survive environmental challenges, such as nutrient-limitation, remain to be elucidated. In this work, we demonstrate that energy-starved cultures of Pyrinomonas methylaliphatogenes, an aerobic heterotrophic acidobacterium isolated from New Zealand volcanic soils, persist by scavenging the picomolar concentrations of H2 distributed throughout the atmosphere. Following the transition from exponential to stationary phase due to glucose limitation, the bacterium up-regulates by fourfold the expression of an eight-gene operon encoding an actinobacteria-type H2-uptake [NiFe]-hydrogenase. Whole-cells of the organism consume atmospheric H2 in a first-order kinetic process. Hydrogen oxidation occurred most rapidly under oxic conditions and was weakly associated with the cell membrane. We propose that atmospheric H2 scavenging serves as a mechanism to sustain the respiratory chain of P. methylaliphatogenes when organic electron donors are scarce. As the first observation of H2 oxidation to our knowledge in the Acidobacteria, the second most dominant soil phylum, this work identifies new sinks in the biogeochemical H2 cycle and suggests that trace gas oxidation may be a general mechanism for microbial persistence.