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

Abstract

Uptake of molecular hydrogen (H2) by soil is a biological reaction responsible for approximately 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 10(6)-10(7) 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.

A soil actinobacterium scavenges atmospheric H 2 using two membrane-associated, oxygen-dependent [NiFe] hydrogenases

“…We definitively confirm that group 5 [NiFe] hydrogenases can mediate high-affinity H 2 oxidation and provide strong support for the hypothesis that these enzymes are the principal sinks for atmospheric H 2 . The kinetic parameters of whole-cell H 2 oxidation by Hyd2, as observed in isolation in the Δhyd13 strain and deleted in the Δhyd2 strain, are very similar to the high-affinity processes observed in whole soil samples (9, 10) and cultured streptomycetes (12,15) (Fig. 4).…”

“…It is proposed that group 5 [NiFe] hydrogenases are responsible for high-affinity H 2 oxidation in streptomycetes (12,17). The genes encoding this newly discovered hydrogenase lineage (hhyLS) are highly conserved and taxonomically restricted; among sequenced genomes, this hydrogenase is only widespread in environmental actinomycetes, including Streptomyces, Mycobacterium, Rhodococcus, and Frankia species (Fig.…”

“…However, it has recently been shown that certain soil-dwelling actinomycetes are capable of scavenging H 2 at tropospheric concentrations (12,15). The first isolated highaffinity H 2 -oxidizer, Streptomyces sp.…”

“…These activities are thought to be catalyzed by [NiFe] hydrogenases, of which there are five defined phylogenetically and functionally distinct groups (11,12).…”

Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival

“…It was recently shown that some aerobic soil actinobacteria and acidobacteria persist by scavenging H 2 from the lower atmosphere (Constant et al, 2010;Greening et al, , 2015a, overturning long-held beliefs that hydrogen metabolism is restricted to low O 2 , high H 2 environments and highlighting the importance of H 2 for survival in addition to growth . Biochemists have simultaneously elucidated mechanisms dependent on reversed electron flow that enable certain hydrogenases to function in the presence of the oxygen (traditionally an inhibitor of their active sites) (Fritsch et al, 2011;Shomura et al, 2011;Horch et al, 2015).…”