Genome-resolved metagenomics reveals how soil bacterial communities respond to elevated H2 availability

Abstract

Molecular hydrogen (H2) is a major energy source supporting bacterial growth and persistence in soil ecosystems. While recent studies have uncovered mediators of atmospheric H2 consumption, far less is understood about how soil microbial communities respond to elevated H2 levels produced through natural or anthropogenic processes. Here we performed microcosm experiments to resolve how microbial community composition, capabilities, and activities change in upland and wetland soils following H2 supplementation (at mixing doses from 0.5 to 50,000 ppmv). Genome-resolved metagenomic profiling revealed that these soils harbored diverse bacteria capable of using H2 as an electron donor for aerobic respiration (46 of the 196 MAGs from eight phyla) and carbon fixation (15 MAGs from three phyla). H2 stimulated the growth of several of these hydrogenotrophs in a dose-dependent manner, though the lineages stimulated differed between the soils; whereas actinobacterial lineages encoding group 2a [NiFe]-hydrogenases grew most in the upland soils (i.e. Mycobacteriaceae, Pseudonocardiaceae), proteobacterial lineages harboring group 1d [NiFe]-hydrogenases were most enriched in wetland soils (i.e. Burkholderiaceae). Hydrogen supplementation also influenced the abundance of various other genes associated with biogeochemical cycling and bioremediation pathways to varying extents between soils. Reflecting this, we observed an enrichment of a hydrogenotrophic Noviherbaspirillum MAG capable of biphenyl hydroxylation in the wetland soils and verified that H2 supplementation enhanced polychlorinated biphenyl (PCB) degradation in these soils, but not the upland soils. This study constitutes the first genome-resolved analysis of how soil microbial communities respond to elevated H2 availability. Overall, our findings suggest that soils harbour different hydrogenotrophic bacteria that rapidly grow following elevated H2 exposure. In turn, this adds to growing evidence of a large and robust soil H2 sink capable of counteracting growing anthropogenic emissions.