A review of the mechanisms of mineral-based metabolism in early Earth analog rock-hosted hydrothermal ecosystems

Abstract

Prior to the advent of oxygenic photosynthesis similar to 2.8-3.2Ga, life was dependent on chemical energy captured from oxidation-reduction reactions involving minerals or substrates generated through interaction of water with minerals. Terrestrial hydrothermal environments host abundant and diverse non-photosynthetic communities and a variety of minerals that can sustain microbial metabolism. Minerals and substrates generated through interaction of minerals with water are differentially distributed in hot spring environments which, in turn, shapes the distribution of microbial life and the metabolic processes that support it. Emerging evidence suggests that terrestrial hydrothermal environments may have played a role in supporting the metabolism of the earliest forms of microbial life. It follows that these environments and their microbial inhabitants are increasingly being studied as analogs of early Earth ecosystems. Here we review current understanding of the processes that lead to variation in the availability of minerals or mineral-sourced substrates in terrestrial hydrothermal environments. In addition, we summarize proposed mechanisms of mineral substrate acquisition and metabolism in microbial cells inhabiting terrestrial hydrothermal environments, highlighting the importance of the dynamic interplay between biotic and abiotic reactions in influencing mineral substrate bioavailability. An emphasis is placed on mechanisms involved in the solubilization, acquisition, and metabolism of sulfur- and iron-bearing minerals, since these elements were likely integrated into the metabolism of the earliest anaerobic cells.