Perspective: Microbial hydrogen metabolism in rock-hosted ecosystems

Hydrogen (H-2) is among the most common and widely utilized electron donors in microbial metabolism. This is particularly true for microorganisms that inhabit subsurface environments where H-2 concentrations can be high due to H-2 generation via one or more abiotic and biotic processes, such as serpentinization, radiolysis, cataclasis, and microbial fermentation. A surge in interest in the exploration for and exploitation of geologic (i.e., white and orange) H-2 as a clean low carbon fuel therefore necessitates an evaluation of the influence of microorganisms on its flux and potential recovery from subsurface systems. The widespread application of high throughput metagenomic sequencing approaches to rock-hosted ecosystems now makes it possible to readily identify microorganisms that harbor the potential to metabolize H-2 and to predict their mode of coupling H-2 oxidation with available oxidants using comparative genomic data from natural samples alone. When combined with several recent reports of measured rates of net microbial H-2 consumption in rock-hosted ecosystems, such information provides new perspective on the potential for microorganisms to impact the economics of H-2 recovery from geologic systems. In this perspective, the different classes of enzymes that microorganisms use to reversibly oxidize H-2 to fuel their energy metabolism are introduced and their distribution in several rock-hosted ecosystems is discussed. A compilation of net microbial H-2 oxidation activities in rock-hosted ecosystems is also presented to enable estimates of potential H-2 loss from natural or stimulated geologic reservoirs during mining activities, with an example provided from the Samail Ophiolite that indicates >90% of geologic H-2 produced could be lost to microbial consumption. Finally, avenues to guide future microbial research in environments where geologic H-2 mining is planned are discussed.