Lithogenic hydrogen supports microbial primary production in subglacial and proglacial environments

Abstract

Life in environments devoid of photosynthesis, such as on early Earth or in contemporary dark subsurface ecosystems, is supported by chemical energy. How, when, and where chemical nutrients released from the geosphere fuel chemosynthetic biospheres is fundamental to understanding the distribution and diversity of life, both today and in the geologic past. Hydrogen (H2) is a potent reductant that can be generated when water interacts with reactive components of mineral surfaces such as silicate radicals and ferrous iron. Such reactive mineral surfaces are continually generated by physical comminution of bedrock by glaciers. Here, we show that dissolved H2 concentrations in meltwaters from an iron and silicate mineral-rich basaltic glacial catchment were an order of magnitude higher than those from a carbonate-dominated catchment. Consistent with higher H2 abundance, sediment microbial communities from the basaltic catchment exhibited significantly shorter lag times and faster rates of net H2 oxidation and dark carbon dioxide (CO2) fixation than those from the carbonate catchment, indicating adaptation to use H2 as a reductant in basaltic catchments. An enrichment culture of basaltic sediments provided with H2, CO2, and ferric iron produced a chemolithoautotrophic population related to Rhodoferax ferrireducens with a metabolism previously thought to be restricted to (hyper)thermophiles and acidophiles. These findings point to the importance of physical and chemical weathering processes in generating nutrients that support chemosynthetic primary production. Furthermore, they show that differences in bedrock mineral composition can influence the supplies of nutrients like H2 and, in turn, the diversity, abundance, and activity of microbial inhabitants.