Time-series transcriptomics from cold, oxic subseafloor crustal fluids reveals a motile, mixotrophic microbial community

The rock-hosted oceanic crustal aquifer is one of the largest habitable volumes on Earth, and it harbors a reservoir of microbial life that influences global-scale biogeochemical cycles. Here, we use time series metagenomic and metatranscriptomic data from a low-temperature, ridge flank environment that is representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics. The data suggest that the microbial community in this subseafloor habitat is motile, chiefly heterotrophic or mixotrophic, and capable of using alternative electron acceptors such as nitrate and thiosulfate, in addition to oxygen. Anaerobic processes are most abundant in subseafloor horizons deepest in the aquifer, furthest from connectivity with the deep ocean, and there was little overlap in the active microbial populations between sampling horizons. Together, our results indicate the microbial community in the North Pond aquifer plays an important role in the oxidation of organic carbon within the crust, and is also metabolically flexible, with the ability to switch from autotrophy to heterotrophy, as well as function under low oxygen conditions. This work highlights the heterogeneity of microbial life in the subseafloor aquifer and provides new insights into biogeochemical cycling in ocean crust.