Carbon Assimilation Strategies in Ultrabasic Groundwater: Clues from the Integrated Study of a Serpentinization-Influenced Aquifer

Abstract

Serpentinization is a low-temperature metamorphic process by which ultramafic rock chemically reacts with water. These reactions provide energy and materials that may be harnessed by chemosynthetic microbial communities at hydrothermal springs and in the subsurface. However, the biogeochemistry of microbial populations that inhabit these environments are understudied and are complicated by overlapping biotic and abiotic processes. We applied metagenomics, metatranscriptomics, and untargeted metabolomics techniques to environmental samples taken from the Coast Range Ophiolite Microbial Observatory (CROMO), a subsurface observatory consisting of twelve wells drilled into the ultramafic and serpentinite melange of the Coast Range Ophiolite in California. Using a combination of DNA and RNA sequence data and mass spectrometry data, we determined that several carbon assimilation strategies, including the Calvin-Benson-Bassham cycle, the reverse tricarboxylic acid cycle, the reductive acetyl-CoA pathway, and methylotrophy are used by the microbial communities inhabiting the serpentinite-hosted aquifer. Our data also suggests that the microbial inhabitants of CROMO use products of the serpentinization process, including methane and formate, as carbon sources in a hyperalkaline environment where dissolved inorganic carbon is unavailable.\n\nImportanceThis study describes the metabolic pathways by which microbial communities in a serpentinite-influenced aquifer may produce biomass from the products of serpentinization. Serpentinization is a widespread geochemical process, taking place over large regions of the seafloor, particularly in slow-spreading mid ocean ridge and subduction zone environments. The serpentinization process is implicated in the origin of life on Earth and as a possible environment for the discovery of life on other worlds in our solar system. Because of the difficulty in delineating abiotic and biotic processes in these environments, major questions remain related to microbial contributions to the carbon cycle and physiological adaptation to serpentinite habitats. This research explores multiple mechanisms of carbon assimilation in serpentinite-hosted microbial communities.