Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase

• Published in: Environmental microbiology Vol. 12; no. 3; pp. 821 - 829
• Main Authors: Constant, Philippe, Chowdhury, Soumitra Paul, Pratscher, Jennifer, Conrad, Ralf
• Format: Journal Article
• Language: English
• Published: Oxford, UK Oxford, UK : Blackwell Publishing Ltd 01.03.2010; Blackwell Publishing Ltd
• Subjects: Actinobacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Hydrogen - metabolism; Hydrogenase - genetics; Hydrogenase - metabolism; Phylogeny; RNA, Ribosomal, 16S - genetics; Soil Microbiology; Streptomyces; Streptomyces - classification; Streptomyces - cytology; Streptomyces - enzymology; Streptomyces - genetics; Streptomycetes
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/j.1462-2920.2009.02130.x

Uptake of molecular hydrogen (H₂) by soil is a biological reaction responsible for ~80% of the global loss of atmospheric H₂. Indirect evidence obtained over the last decades suggests that free soil hydrogenases with an unusually high affinity for H₂ are carrying out the reaction. This assumption has recently been challenged by the isolation of Streptomyces sp. PCB7, displaying the high-affinity H₂ uptake activity previously attributed to free soil enzymes. While this finding suggests that actinobacteria could be responsible for atmospheric H₂ soil uptake, the ecological importance of H₂-oxidizing streptomycetes remains to be investigated. Here, we show that high-affinity H₂ uptake activity is widespread among the streptomycetes. Among 14 streptomycetes strains isolated from temperate forest and agricultural soils, six exhibited a high-affinity H₂ uptake activity. The gene encoding the large subunit of a putative high-affinity [NiFe]-hydrogenase (hydB-like gene sequence) was detected exclusively in the isolates exhibiting high-affinity H₂ uptake. Catalysed reporter deposition-fluorescence in situ hybridization (CARD-FISH) experiments targeting hydB-like gene transcripts and H₂ uptake assays performed with strain PCB7 suggested that streptomycetes spores catalysed the H₂ uptake activity. Expression of the activity in term of biomass revealed that 10⁶-10⁷ H₂-oxidizing bacteria per gram of soil should be sufficient to explain in situ H₂ uptake by soil. We propose that specialized H₂-oxidizing actinobacteria are responsible for the most important sink term in the atmospheric H₂ budget.