New roles for aerobic hydrogen metabolism: from enzymes to ecosystems

Diverse microorganisms consume and produce hydrogen gas (H2) using metalloenzymes called hydrogenases. While this metabolism is traditionally associated with anaerobes, several lineages of bacteria and archaea are known to support aerobic growth on H2. In this seminar, I will reveal that the dominant bacteria inhabiting global soil ecosystems are also facultative H2 oxidisers. These bacteria use atmospheric H2 as a respiratory electron donor to sustain long-term survival when exhausted for preferred organic carbon sources. This process is mediated by a newly discovered hydrogenase lineage, the group 1h [NiFe]-hydrogenase, which is extraordinary for its nanomolar affinity for H2 and complete insensitivity to inhibition by O2. We show through genetic studies on mycobacteria that this alternative metabolic pathway is tightly regulated, critical for redox homeostasis and necessary for long-term survival. The genes encoding this enzyme are widespread in the genomes of aerobic bacteria and we have experimentally validated that they mediate atmospheric H2 scavenging in four dominant soil phyla, namely Actinobacteria, Acidobacteria, Verrucomicrobia, and Chloroflexi. Moreover, biogeochemical and metagenomic profiles show that trace gas scavenging is highly active at the ecosystem level. Atmospheric H2 is a particularly important energy sources for bacterial communities in highly oligotrophic ecosystems, notably Antarctic desert soils, where it serves as the main energy sources supporting primary production. These findings in turn have implications for understanding biogeochemical cycling, mycobacterial dormancy, and metalloenzyme evolution.