Martina Cascone, Guillermo Climent Gargallo, Flavia Migliaccio, Davide Corso, Luca Tonietti, Angelina Cordone, Ilaria Pietrini, Elisabetta Franchi, Giovanna Carpani, Almerinda di Benedetto, Giuseppina Luciani, Giuseppina Anzelmo, Andrea Giovannelli, DaVID Iacopini, Mariano Parente, Katriona Edlmann, Marco Moracci, Donato Giovannelli

Hydrogen is a fundamental electron donor in diverse microbial metabolisms and it is considered the energetic currency exchanged within microbial communities in anaerobic environments. Hydrogen is also the major actor in the transition to alternative low-carbon energy sources, primarily due to its dual role as energy source and energy carrier and to the production of water as a byproduct of its combustion. The geological storage of hydrogen gas produced from diverse sources in stable terrestrial reservoirs, known also as Underground Hydrogen Storage (UHS), is a key prerequisite to decouple production from utilization. UHS targets include depleted porous natural gas reservoirs, salt caverns and deep aquifers. Studies carried out in the past 30 years have unveiled a large subsurface ecosystem able to interact with the geochemical cycles and volatiles present in Earth’s crust. When hydrogen is stored underground, the microbial communities present in situ can interact with it, consuming it as electron donor, potentially producing undesired metabolic byproducts capable of affecting the success of UHS operations. Additionally, subsurface microbial communities might impact the geological production, migration and accumulation of hydrogen in natural reservoirs. Here, we review the current state of knowledge in hydrogenotrophic metabolisms capable of affecting UHS operations and natural hydrogen prospecting, and discuss how the microbiology of natural hydrogen-rich springs can be used as analog to model the state space of hydrogen operations. We discuss our current knowledge of the limits of life in the context of hydrogen economy, and the complex trophic network that hydrogen might sustain in the subsurface. While energy demands increase globally, the ability to effectively operate geological hydrogen storage and identify natural hydrogen deposits will become a key prerequisite to reduce the global carbon footprint. Understanding the potential for microbes to interact with hydrogen in the subsurface is therefore at the forefront of the ecological transition.