Dunham, and four co-authors, reported in late 2020 that in the absence of light, biomass production is driven by chemical energy through microbial chemosynthesis. H2, a potent reductant capable of supporting chemosynthesis, is readily generated by reactions between iron and silicate minerals and water. Here, we show that lithogenic H2 produced by glacial comminution of iron- and silica-rich basaltic bedrock supports microbial chemosynthesis. Lithogenic production of H2 in cold, dark subglacial environments and its use to generate chemosynthetic biomass suggest the potential for subglacial habitats to serve as refugia for microbial communities in the absence of sunlight, such as during Snowball Earth episodes or on icy planets where photosynthesis may not yet have evolved or where light is restricted.
The authors concluded that both silicate- and iron-bearing minerals can generate H2 through cataclastic radical and reductive mechanisms in the presence of water. These minerals are chemically altered in the process, however, thereby preventing sustained reactivity unless they are resurfaced. Glacial comminution is one mechanism of generating fresh mineral surfaces capable of reacting with water on a continual basis. Thus, subglacial environments have the potential to provide continuous sources of chemical energy, in the form of disequilibrium between H2 and oxidized minerals, that can support chemolithotrophic microbial primary production in subglacial and downstream proglacial environments.
Meltwaters from KJ, which overlays a basaltic catchment, had an order of magnitude more dissolved H2 than those from RG, which sits in a carbonate catchment. The sediment community at KJ exhibited shorter lag times and significantly faster rates of H2 oxidation and CO2 fixation than those measured for the RG sediment community. Metabolic activity assays and MPN experiments show that at least two populations of autotrophic hydrogenotrophs inhabit KJ sediments: one metabolically flexible mixotroph (Glaciimonas sp.) and one that can, at a minimum, utilize H2, CO2, and Fe(III) or NO3 − (Rhodoferax sp.). In RG sediments, however, differing lag times between H2 oxidation and CO2 fixation experiments suggest that the two processes are not tightly coupled. A potential explanation for this comes from a prior study that showed the dominant primary producer in RG sediments depended primarily on FeS2 or derivatives of its oxidation (i.e., thiosulfate) as reductants. Thus, H2 oxidation in RG sediment populations may be attributable to a mixotrophic or chemolithoheterotrophic metabolism, as has been recently demonstrated in other taxa.
(Meta)genomic sequencing of the most dilute MPN assays from KJ identified a relative of the NO3−- and Fe(III)-reducing Rhodoferax and a population of Glaciimonas as the dominant H2 oxidizing autotrophs and/or mixotrophs in this system. Transfers of the Rhodoferax MPN culture into fresh medium further demonstrated the ability of this population to grow autotrophically using the H2/Fe(III) redox couple. This represents the only report to date of chemolithoautotrophic, H2-dependent iron reduction in a nonhyperthermophilic or acidophilic organism, and experiments to further characterize this bacterium are underway.
Collectively, these results indicate that differences in bedrock mineral composition likely influence supplies of lithogenic H2 and oxidants and that these, in turn, influence the diversity, abundance, and activity of H2-dependent autotrophs in subglacial and proglacial habitats. More broadly, they further underscore the importance of physical and chemical weathering processes in releasing nutrients capable of sustaining microbial primary production in these habitats, corroborating recent evidence that such communities could be supported by chemolithotrophic primary production, independent of photosynthetically fixed carbon. This finding has important implications for the survival of terrestrial life through Snowball Earth periods of globally extensive glaciation and for the possibility of discovering life on other icy planetary bodies. Indeed, the recent discovery of H2 gas in plumes of material erupting from the icy crust of Enceladus points to active rock–water interactions occurring beneath the ice surface and implies a subsurface geochemical system with potentially important parallels to that of KJ and other glaciers in basaltic terrains.
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