Earth’s largest aquifer ecosystem resides in igneous oceanic crust, where chemosynthesis and water-rock reactions provide the carbon and energy that support an active deep biosphere. The Calvin Cycle is the predominant carbon fixation pathway in cool, oxic, crust; however, the energy and carbon metabolisms in the deep thermal basaltic aquifer are poorly understood. Anaerobic carbon fixation pathways such as the Wood-Ljungdahl pathway, which uses hydrogen (H2) and CO2, may be common in thermal aquifers since water-rock reactions can produce H2in hydrothermal environments and bicarbonate is abundant in seawater. To test this, we reconstructed the metabolisms of eleven bacterial and archaeal metagenome-assembled genomes from an olivine biofilm obtained from a Juan de Fuca Ridge basaltic aquifer. We found that the dominant carbon fixation pathway was the Wood-Ljungdahl pathway, which was present in seven of the eight bacterial genomes. Anaerobic respiration appears to be driven by sulfate reduction, and one bacterial genome contained a complete nitrogen fixation pathway. This study reveals the potential pathways for carbon and energy flux in the deep anoxic thermal aquifer ecosystem, and suggests that ancient H2-based chemolithoautotrophy, which once dominated Earth’s early biosphere, may thus remain one of the dominant metabolisms in the suboceanic aquifer today.
Volcanic ocean crust contains a global chemosynthetic microbial ecosystem that impacts ocean productivity, seawater chemistry, and geochemical cycling. We examined the mineralogical effect on community structure in the aquifer ecosystem by using a four-year in situ colonization experiment with igneous minerals and glasses in IODP Hole 1301A on the Juan de Fuca Ridge. Microbial community analysis and scanning electron microscopy revealed that olivine phases and iron-bearing minerals bore communities that were distinct from iron-poor phases. Communities were dominated by Archaeoglobaceae, Clostridia, Thermosipho, Desulforudis, and OP1 lineages. Our results suggest that mineralogy determines microbial composition in the subseafloor aquifer ecosystem.