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

Pok Man Leung (), Rhys Grinter, Eve Tudor-Matthew, James P. Lingford, Luis Jimenez, Han-Chung Lee, Michael Milton, Iresha Hanchapola, Erwin Tanuwidjaya, Ashleigh Kropp, Hanna A. Peach, Carlo R. Carere, Matthew B. Stott, Ralf B. Schittenhelm and Chris Greening ()
Additional contact information
Pok Man Leung: Monash University
Rhys Grinter: Monash University
Eve Tudor-Matthew: Monash University
James P. Lingford: Monash University
Luis Jimenez: Monash University
Han-Chung Lee: Monash University
Michael Milton: Monash University
Iresha Hanchapola: Monash University
Erwin Tanuwidjaya: Monash University
Ashleigh Kropp: Monash University
Hanna A. Peach: Wairakei
Carlo R. Carere: Wairakei
Matthew B. Stott: Wairakei
Ralf B. Schittenhelm: Monash University
Chris Greening: Monash University

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-47324-2

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