Early response of methanogenic archaea to H(2) as evaluated by metagenomics and metatranscriptomics

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.