Hydrothermal circulation within the sea floor, through lithosphere older than one million years (Myr), is responsible for 30% of the energy released from plate cooling, and for 70% of the global heat flow anomaly (the difference between observed thermal output and that predicted by conductive cooling models). Hydrothermal fluids remove significant amounts of heat from the oceanic lithosphere for plates typically up to about 65 Myr old. But in view of the relatively impermeable sediments that cover most ridge flanks, it has been difficult to explain how these fluids transport heat from the crust to the ocean. Here we present results of swath mapping, heat flow, geochemistry and seismic surveys from the young eastern flank of the Juan de Fuca ridge, which show that isolated basement outcrops penetrating through thick sediments guide hydrothermal discharge and recharge between sites separated by more than 50 km. Our analyses reveal distinct thermal patterns at the sea floor adjacent to recharging and discharging outcrops. We find that such a circulation through basement outcrops can be sustained in a setting of pressure differences and crustal properties as reported in independent observations and modelling studies.

Oceanic crust comprises the largest hydrogeologic reservoir on Earth, containing fluids in thermodynamic disequilibrium with the basaltic crust. Little is known about microbial ecosystems that inhabit this vast realm and exploit chemically favorable conditions for metabolic activities. Crustal samples recovered from ocean drilling operations are often compromised for microbiological assays, hampering efforts to resolve the extent and functioning of a subsurface biosphere. We report results from the first in situ experimental observatory systems that have been used to study subseafloor life. Experiments deployed for 4 years in young (3.5 Ma) basaltic crust on the eastern flank of the Juan de Fuca Ridge record a dynamic, post-drilling response of crustal microbial ecosystems to changing physical and chemical conditions. Twisted stalks exhibiting a biogenic iron oxyhydroxide signature coated the surface of mineral substrates in the observatories; these are biosignatures indicating colonization by iron oxidizing bacteria during an initial phase of cool, oxic, iron-rich conditions following observatory installation. Following thermal and chemical recovery to warmer, reducing conditions, the in situ microbial structure in the observatory shifted, becoming representative of natural conditions in regional crustal fluids. Firmicutes, metabolic potential of which is unknown but may involve N or S cycling, dominated the post-rebound bacterial community. The archaeal community exhibited an extremely low diversity. Our experiment documented in situ conditions within a natural hydrological system that can pervade over millennia, exemplifying the power of observatory experiments for exploring the subsurface basaltic biosphere, the largest but most poorly understood biotope on Earth.

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The rock-hosted subseafloor crustal aquifer harbors a reservoir of microbial life that may influence global marine biogeochemical cycles. Here we utilized metagenomic libraries of crustal fluid samples from North Pond, located on the flanks of the Mid-Atlantic Ridge, a site with cold, oxic subseafloor fluid circulation within the upper basement to query microbial diversity. Twenty-one samples were collected during a 2-year period to examine potential microbial metabolism and community dynamics. We observed minor changes in the geochemical signatures over the 2 years, yet the microbial community present in the crustal fluids underwent large shifts in the dominant taxonomic groups. An analysis of 195 metagenome-assembled genomes (MAGs) were generated from the data set and revealed a connection between litho- and autotrophic processes, linking carbon fixation to the oxidation of sulfide, sulfur, thiosulfate, hydrogen, and ferrous iron in members of the Proteobacteria, specifically the Alpha-, Gamma- and Zetaproteobacteria, the Epsilonbacteraeota and the Planctomycetes. Despite oxic conditions, analysis of the MAGs indicated that members of the microbial community were poised to exploit hypoxic or anoxic conditions through the use of microaerobic cytochromes, such as cbb3- and bd-type cytochromes, and alternative electron acceptors, like nitrate and sulfate. Temporal and spatial trends from the MAGs revealed a high degree of functional redundancy that did not correlate with the shifting microbial community membership, suggesting functional stability in mediating subseafloor biogeochemical cycles. Collectively, the repeated sampling at multiple sites, together with the successful binning of hundreds of genomes, provides an unprecedented data set for investigation of microbial communities in the cold, oxic crustal aquifer.