Abstract

The 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 representative of the majority of global hydrothermal fluid circulation in the ocean to reconstruct microbial metabolic potential, transcript abundance, and community dynamics. We also present metagenome-assembled genomes from recently collected fluids that are furthest removed from drilling disturbances. Our results suggest that the microbial community in the North Pond aquifer plays an important role in the oxidation of organic carbon within the crust. This community is motile and metabolically flexible, with the ability to use both autotrophic and organotrophic pathways, as well as function under low oxygen conditions by using alternative electron acceptors such as nitrate and thiosulfate. 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. This work highlights the heterogeneity of microbial life in the subseafloor aquifer and provides new insights into biogeochemical cycling in ocean crust.

Highlights

  • Seawater circulating through porous, basaltic oceanic crust constitutes the largest actively flowing aquifer system on Earth, and represents ~2% of the ocean fluid volume (~27 million km3 of water; [1,2,3])

  • We examined over one billion high-quality paired-end Illumina sequencing reads from 11 metagenomes and 10 metatranscriptomes over three sampling periods spanning 5 years from four different subseafloor fluid horizons and deep bottom water at the North Pond site (Table 1, Supplementary Data)

  • Low-temperature, off-axis environments represent the majority of global hydrothermal fluid circulation in the ocean, but the microbial communities in the subseafloor of young ridge flank oceanic crust are sparsely sampled or understood in comparison to other subseafloor habitats such as marine sediments

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Summary

Introduction

Basaltic oceanic crust constitutes the largest actively flowing aquifer system on Earth, and represents ~2% of the ocean fluid volume (~27 million km of water; [1,2,3]). Much of the remaining crustal pore volume is composed of cold, oxygenated deep ocean water that enters and exits the basaltic crust through seafloor exposures [7, 8]. These crustal fluids are chemically similar to seawater, but slightly enriched in DIC and depleted in DOC and O2 [9,10,11,12]. Microbial communities in the crustal fluids are distinct from those in the overlying bottom water [9, 13], but the lifestyle and adaptive strategies of microbial communities and the biogeochemical processes they mediate in the oligotrophic, oxic subseafloor aquifer remain poorly constrained

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