Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria

Microbe-mediated soil uptake is the largest and most uncertain variable in the budget of atmospheric hydrogen (H-2). The diversity and ecophysiological role of soil microorganisms that can consume low atmospheric abundances of H-2 with high-affinity [NiFe]-hydrogenases is unknown. We expanded the library of atmospheric H-2-consuming strains to include four soil Harvard Forest Isolate (HFI) Streptomyces spp., Streptomyces cattleya and Rhodococcus equi by assaying for high-affinity hydrogenase (hhyL) genes and quantifying H-2 uptake rates. We find that aerial structures (hyphae and spores) are important for StreptomycesH(2) consumption; uptake was not observed in S.griseoflavusTu4000 (deficient in aerial structures) and was reduced by physical disruption of Streptomyces sp. HFI8 aerial structures. H-2 consumption depended on the life cycle stage in developmentally distinct actinobacteria: Streptomyces sp. HFI8 (sporulating) and R.equi (non-sporulating, non-filamentous). Strain HFI8 took up H-2 only after forming aerial hyphae and sporulating, while R.equi only consumed H-2 in the late exponential and stationary phase. These observations suggest that conditions favouring H-2 uptake by actinobacteria are associated with energy and nutrient limitation. Thus, H-2 may be an important energy source for soil microorganisms inhabiting systems in which nutrients are frequently limited.