Abstract
Significant rates of atmospheric dihydrogen (H2) consumption have been observed in temperate soils due to the activity of high-affinity enzymes, such as the group 1h [NiFe]-hydrogenase. We designed broadly inclusive primers targeting the large subunit gene (hhyL) of group 1h [NiFe]-hydrogenases for long-read sequencing to explore its taxonomic distribution across soils. This approach revealed a diverse collection of microorganisms harboring hhyL, including previously unknown groups and taxonomically not assignable sequences. Acidobacterial group 1h [NiFe]-hydrogenase genes were abundant and expressed in temperate soils. To support the participation of acidobacteria in H2 consumption, we studied two representative mesophilic soil acidobacteria, which expressed group 1h [NiFe]-hydrogenases and consumed atmospheric H2 during carbon starvation. This is the first time mesophilic acidobacteria, which are abundant in ubiquitous temperate soils, have been shown to oxidize H2 down to below atmospheric concentrations. As this physiology allows bacteria to survive periods of carbon starvation, it could explain the success of soil acidobacteria. With our long-read sequencing approach of group 1h [NiFe]-hydrogenase genes, we show that the ability to oxidize atmospheric levels of H2 is more widely distributed among soil bacteria than previously recognized and could represent a common mechanism enabling bacteria to persist during periods of carbon deprivation.
Highlights
Primers were designed for the large and small subunits of the group 1h [NiFe]-hydrogenase of E. aggregans and Acidobacteriaceae bacterium KBS 83 targeting the same region of the respective gene, along with the homolog of the hhyS as was done previously [21]
Hydrogen consumption controls were run on uninoculated medium, heat-killed Acidobacteriaceae bacterium KBS 83 cells and an acidobacterial strain (Terriglobus roseus KBS 63) that does not contain group 1h [NiFe]-hydrogenase genes [29] over a period of 24 h with starting H2 concentrations of ~80 ppmv to ensure any potential consumption activity would be sufficiently high for detection (Fig. S3)
[NiFe]-hydrogenase genes, in addition to Acidobacteria, Actinobacteria, Bacteriodetes, Chloroflexi, Planctomycetes, Proteobacteria (Alpha- and Beta-) and Verrucomicrobia (Figs. 2 and S8) in accordance with previous surveys [9, 10, 14, 16]. These phyla are commonly found in soils with varying relative abundances [64]; it should be noted that with the exception of the Acidobacteria and Actinobacteria, group 1h [NiFe]-hydrogenases are present in less than 3% of genomes from each of these phyla (Fig. S8)
Summary
A recent large-scale comparative genome analysis of acidobacteria identified the genes encoding the large and small subunits of the group 1h [NiFe]-hydrogenase (hhyL and hhyS, respectively) in genomes of various mesophilic soil acidobacteria, along with the necessary maturation and accessory genes [29] It remained unknown whether mesophilic acidobacteria can scavenge H2, which are highly abundant in temperate soils where atmospheric H2 consumption was previously reported [30,31,32]. Sequencing of almost the complete large subunit gene further enables improved phylogenetic placement and identification of the amplified genes from soil samples Using this new primer pair, we demonstrate that group 1h [NiFe] hydrogenases are widespread across many phyla, including previously unidentified groups. This work reveals new mediators in the biogeochemically and ecologically important process of atmospheric H2 oxidation, and supports growing evidence that trace gases might be a universal energy source for bacterial persistence
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