Soil microbial communities are continuously exposed to H₂ diffusing into the soil from the atmosphere. N₂-fixing nodules represent a peculiar microniche in soil where H₂ can reach concentrations up to 20,000 fold higher than in the global atmosphere (0.530 ppmv). In this study, we investigated the impact of H₂ exposure on soil bacterial community structure using dynamic microcosm chambers simulating soil H₂ exposure from the atmosphere and N₂-fixing nodules. Biphasic kinetic parameters governing H₂ oxidation activity in soil changed drastically upon elevated H₂ exposure, corresponding to a slight but significant decay of high affinity H₂-oxidizing bacteria population, accompanied by an enrichment or activation of microorganisms displaying low-affinity for H₂. In contrast to previous studies that unveiled limited response by a few species, the relative abundance of 958 bacterial ribotypes distributed among various taxonomic groups, rather than a few distinct taxa, was influenced by H₂ exposure. Furthermore, correlation networks showed important alterations of ribotype covariation in response to H₂ exposure, suggesting that H₂ affects microbe-microbe interactions in soil. Taken together, our results demonstrate that H₂-rich environments exert a direct influence on soil H₂-oxidizing bacteria in addition to indirect effects on other members of the bacterial communities.