Atmospheric hydrogen scavenging: from enzymes to ecosystems

Abstract

We have known for 40 years that soils can consume the trace amounts of molecular hydrogen (H2) found in the Earth’s atmosphere.This process is predicted to be the most significant term in the global hydrogen cycle. However, the organisms and enzymes responsible for this process were only recently identified. Pure culture experiments demonstrated that several species of Actinobacteria, including streptomycetes and mycobacteria, can couple the oxidation of atmospheric H2 to the reduction of ambient O2. A combination of genetic, biochemical, and phenotypic studies suggest that these organisms primarily use this fuel source to sustain electron input into the respiratory chain during energy starvation. This process is mediated by a specialized enzyme, the group 5 [NiFe]-hydrogenase, which is unusual for its high affinity, oxygen insensitivity, and thermostability. Atmospheric hydrogen scavenging is a particularly dependable mode of energy generation, given both the ubiquity of the substrate and the stress tolerance of its catalyst. This minireview summarizes the recent progress in understanding how and why certain organisms scavenge atmospheric H2. In addition, it provides insight into the wider significance of hydrogen scavenging in global H2 cycling and soil microbial ecology.

FIG 1

Diversity and distribution of group 5 [NiFe]-hydrogenases. The hhyL genes of 60 representative [NiFe]-hydrogenases were aligned and visualized in a bootstrapped neighbor-joining phylogenetic tree. Actinobacterial hhyL genes (green), other hhyL genes (blue), and crenarchaeotal membrane-bound hydrogenase lineage genes (red) are indicated. The tree is rooted with sequences of the group 2a, group 3b, and oxygen-tolerant group 1 [NiFe]-hydrogenases.

FIG 2

Components of the group 5 [NiFe]-hydrogenase of Mycobacterium smegmatis. RT-PCR analysis has clarified that M. smegmatis encodes a five-gene structural operon (MSMEG_2718-2722) and a larger accessory/maturation operon (MSMEG_2705-2717) (27, 32). In Ralstonia eutropha, the purified enzyme forms a homodimer (30). On the basis of these findings, we predict that the group 5 [NiFe]-hydrogenase of M. smegmatis also forms a (HhyLS)₂ structure. Encoding a predicted [2Fe2S] cluster, HhyE is likely to accept single electrons and potentially serves as an electron transfer protein for respiration and reductive metabolic processes. The predicted functions of the gene products are indicated by color coding as follows: green for the large subunit, blue for the small subunit, yellow for electron transfer protein, orange for maturation proteins, dark gray for conserved hypothetical proteins, and light gray for hypothetical proteins.

FIG 3

Proposed physiological role of group 5 [NiFe]-hydrogenases during energy starvation in Mycobacterium smegmatis. When organic electron donors are limiting, primary dehydrogenases are downregulated in favor of uptake hydrogenases (27, 34). Oxidation of atmospheric H₂ by the group 5 [NiFe]-hydrogenase HhyLS (orange) leads to input of electrons into the respiratory chain (yellow) and proton translocation mediated by the terminal oxidase (red). This generates sufficient proton motive force to allow ATP synthesis by ATPase (blue) to sustain long-term survival. Solid arrows depict electron flow. NDH2, type II NAD(P)H:quinone oxidoreductases; MQ, menaquinone; MQH₂, menaquinol.