Microbial life at the glass-palagonite interface

Abstract

The majority of the upper 500 m of oceanic crust is made up from extrusive volcanic rocks, predominantly basalts and hyaloclastites (volcanic rocks very rich in fresh glass). When the upper oceanic crust alters under the influence of seawater, its geochemistry, hydrology, and physical conditions change considerably, which shapes the bioenergetical landscape, i.e. the thermodynamics of chemical reactions, which microorganisms can exploit for their energy gain. Basalt that is exposed to oxygenated aqueous solutions, forms rims of palagonite along fractures at the expense of glass. Radioactive elements are enriched in palagonite relative to fresh glass, reaching concentrations where radiolytic production of molecular hydrogen (H2) may play a significant role. In older flanks, crustal sealing and sediment accumulation have slowed down seawater circulation and radiolytically produced hydrogen might reach concentrations where molecular hydrogen (H2) may be a significant energy source. Based on these results, the hypothesis that microbial ecosystems in ridge flank habitats undergo a transition in the principal energy carrier, fueling carbon fixation from Fe oxidation in very young crust to H2 consumption in older crust, was formed. Unless the H2 is swept away by rapid fluid flow (i.e., in young flanks), it may easily accumulate to levels high enough to support chemolithoautotrophic life. In older flanks the influence of H2 for catalytic energy supply is expected to increase greatly. Similar habitats on other planetary surfaces are theoretically possible; as accumulation of radiolytically produced hydrogen merely requires the presence of H2O molecules and a porous medium, from which the hydrogen is not lost. Within these fluids, Si concentrations increases due to palagonitization and eventually void space is (partially) filled by zeolites. Alteration of primary phases also changes the mineral interface to the fluid. One of the major factors controlling radiolytic H2 production is the mineralogy in the immediate proximity of void space in the basalts, as the radioactive doses decrease, while traveling through a mineral matrix. Hence, the importance of iron oxidation for microbial metabolism likely decreases, and we hypothesize that radiolytically produced hydrogen might become the universal electron donor in aging ridge flank systems, possibly extending our view of habitable areas on Earth.