Atmospheric Hydrogen Scavenging: from Enzymes to Ecosystems

Abstract

fWe have known for 40 years that soils can consume the trace amounts of molecular hydrogen (H 2 ) 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 H 2 to the reduction of ambient O 2 . 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 H 2 . In addition, it provides insight into the wider significance of hydrogen scavenging in global H 2 cycling and soil microbial ecology.

Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival

“…Most significantly, the group 1h [NiFe]-hydrogenases that mediate tropospheric H 2 oxidation are encoded in multiple representatives of undercultured, slowgrowing phyla (that is, Acidobacteria, Verrucomicrobia, Chloroflexi and Planctomycetes). These findings are consistent with our recent hypothesis that H 2 serves as an energy source for the maintenance of dormant soil bacteria (Greening et al, 2015b). Hydrogenase-encoding genes were also identified in the genomes of multiple seemingly obligate methane oxidisers, ammonia oxidisers and nitrite oxidisers (Supplementary Table S1), suggesting H 2 may serve as a fuel source for growth or survival of these bacteria and archaea.…”

“…Furthermore, detailed biochemical information and atomicresolution structures are available for only a subset of hydrogenases (Volbeda et al, 1995;Peters et al, 1998;Shima et al, 2008;Fritsch et al, 2011;Mills et al, 2013). Although the contribution of H 2 metabolism to total ecosystem processes is recognised in some environments (for example, anoxic sediments, animal guts and hydrothermal vents; Vignais and Billoud, 2007;Schwartz et al, 2013), the role of hydrogenases in general soil and aquatic ecosystems remains largely unresolved (Barz et al, 2010;Constant et al, 2011;Beimgraben et al, 2014;Greening et al, 2015b). Consequently, the influence of H 2 evolution and consumption on community structuring and global biogeochemical cycling requires further investigation (Schwartz et al, 2013;Greening et al, 2015b).…”

Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging

“…This behavior significantly differs from that of M. smegmatis, which strictly depends on the presence exogenous O 2 for H 2 oxidation to be detectable (22,24). Furthermore, the P. methylaliphatogenes hydrogenase has a weaker membrane-association than the M. smegmatis hydrogenase (7,24) and runs as a single band rather than triplet of bands during native polyacrylamide gel electrophoresis. Although the reasons for these behaviors are not yet understood, these results suggest that there are substantial differences in the oligomerisation or interactions of Group 5 [NiFe]-hydrogenases in Acidobacteria compared with Actinobacteria.…”

“…Given the reduction in long-term viability of M. smegmatis strains lacking the Group 5 [NiFe]-hydrogenase (23, 26), we nevertheless infer that atmospheric H 2 scavenging may enhance the survival of P. methyaliphatogenes. As atmospheric H 2 is ubiquitous and diffusible, this gas acts as a highly dependable source of energy for bacterial persistence (7,28). A model of the role of atmospheric H 2 scavenging in energy-generation during persistence of P. methylaliphatogenes is shown in Fig.…”

“…Several processes have been linked to energymaintenance in dormant states, ranging from triacylglycerol storage in nonreplicative persistent mycobacteria (5), to predation and cannibalism by sporulating bacilli (6). More recently, it has been proposed that consumption of atmospheric trace gases such as molecular hydrogen (H 2 ) serves as a dependable mechanism to generate maintenance energy in several organisms during persistence (4,(7)(8)(9).…”