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

Abstract

Microbe-mediated soil uptake is the largest and most uncertain variable in the budget of atmospheric hydrogen (H2). The diversity and ecophysiological role of soil microorganisms that can consume low atmospheric abundances of H2 with high-affinity [NiFe]-hydrogenases is unknown. We expanded the library of atmospheric H2-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 H2 uptake rates. We find that aerial structures (hyphae and spores) are important for Streptomyces H2 consumption; uptake was not observed in Streptomyces griseoflavus Tu4000 (deficient in aerial structures) and was reduced by physical disruption of Streptomyces sp. HFI8 aerial structures. H2 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 H2 only after forming aerial hyphae and sporulating, while R. equi only consumed H2 in the late exponential and stationary phase. These observations suggest that conditions favoring H2 uptake by actinobacteria are associated with energy and nutrient limitation. Thus, H2 may be an important energy source for soil microorganisms inhabiting systems in which nutrients are frequently limited.