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 (H[subscript 2]). The diversity and ecophysiological role of soil microorganisms that can consume low atmospheric abundances of H[subscript 2] with high-affinity [NiFe]-hydrogenases is unknown. We expanded the library of atmospheric H[subscript 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[subscript 2] uptake rates. We find that aerial structures (hyphae and spores) are important for Streptomyces H[subscript 2] consumption; uptake was not observed in S. griseoflavus Tu4000 (deficient in aerial structures) and was reduced by physical disruption of Streptomyces sp. HFI8 aerial structures. H[subscript 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[subscript 2] only after forming aerial hyphae and sporulating, while R. equi only consumed H[subscript 2] in the late exponential and stationary phase. These observations suggest that conditions favouring H[subscript 2] uptake by actinobacteria are associated with energy and nutrient limitation. Thus, H[subscript 2] may be an important energy source for soil microorganisms inhabiting systems in which nutrients are frequently limited.