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

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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)Streptomycesspp.,Streptomyces cattleyaandRhodococcus equiby assaying for high-affinity hydrogenase (hhyL) genes and quantifying H2 uptake rates. We find that aerial structures (hyphae and spores) are important forStreptomycesH2 consumption; uptake was not observed inS. griseoflavusTu4000 (deficient in aerial structures) and was reduced by physical disruption ofStreptomycessp. HFI8 aerial structures. H2 consumption depended on the life cycle stage in developmentally distinct actinobacteria:Streptomycessp. HFI8 (sporulating) andR. equi(non-sporulating, non-filamentous). Strain HFI8 took up H2 only after forming aerial hyphae and sporulating, whileR. equionly consumed H2 in the late exponential and stationary phase. These observations suggest that conditions favouring 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.

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