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Background  The molecular machinery of the complex microbiological cell factory of biomethane production is not fully understood. One of the process control elements is the regulatory role of hydrogen (H 2 ). Reduction of carbon dioxide (CO 2 ) by H 2  is rate limiting factor in methanogenesis, but the community intends to keep H 2  concentration low in order to maintain the redox balance of the overall system. H 2  metabolism in methanogens becomes increasingly important in the Power-to-Gas renewable energy conversion and storage technologies.    Results  The early response of the mixed mesophilic microbial community to H 2  gas injection was investigated with the goal of uncovering the first responses of the microbial community in the CH 4  formation and CO 2  mitigation Power-to-Gas process. The overall microbial composition changes, following a 10 min excessive bubbling of H 2  through the reactor, was investigated via metagenome and metatranscriptome sequencing. The overall composition and taxonomic abundance of the biogas producing anaerobic community did not change appreciably 2 hours after the H 2  treatment, indicating that this time period was too short to display differences in the proliferation of the members of the microbial community. There was, however, a substantial increase in the expression of genes related to hydrogenotrophic methanogenesis of certain groups of Archaea. As an early response to H 2  exposure the activity of the hydrogenotrophic methanogenesis in the genus  Methanoculleus  was upregulated but the hydrogenotrophic pathway in genus  Methanosarcina  was downregulated. The RT-qPCR data corroborated the metatranscriptomic    Results  H 2  injection also altered the metabolism of a number of microbes belonging in the kingdom Bacteria. Many Bacteria possess the enzyme sets for the Wood-Ljungdahl pathway. These and the homoacetogens are partners for syntrophic community interactions between the distinct kingdoms of Archaea and Bacteria.    Conclusions  External H 2  regulates the functional activity of certain Bacteria and Archaea. The syntrophic cross-kingdom interactions in H 2  metabolism are important for the efficient operation of the Power-to-Gas process. Therefore, mixed communities are recommended for the large scale Power-to-Gas process rather than single hydrogenotrophic methanogen strains. Fast and reproducible response from the microbial community can be exploited in turn-off and turn-on of the Power-to-Gas microbial cell factories.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12934-021-01618-y.

Early response of methanogenic archaea to H2 as evaluated by metagenomics and metatranscriptomics