Enzymatic microbial Mn(II) oxidation and Mn biooxide production in the Guaymas Basin deep-sea hydrothermal plume

Microorganisms play important roles in mediating biogeochemical reactions in deep-sea hydrothermal plumes, but little is known regarding the mechanisms that underpin these transformations. At Guaymas Basin (GB) in the Gulf of California, hydrothermal vents inject fluids laden with dissolved Mn(II) (dMn) into the deep waters of the basin where it is oxidized and precipitated as particulate Mn(III/IV) oxides, forming turbid hydrothermal “clouds”. Previous studies have predicted extremely short residence times for dMn at GB and suggested they are the result of microbially-mediated Mn(II) oxidation and precipitation. Here we present biogeochemical results that support a central role for microorganisms in driving Mn(II) oxidation in the GB hydrothermal plume, with enzymes being the primary catalytic agent. dMn removal rates at GB are remarkably fast for a deep-sea hydrothermal plume (up to 2 nM/h). These rapid rates were only observed within the plume, not in background deep-sea water above the GB plume or at GB plume depths (∼1750-2000 m) in the neighboring Carmen Basin, where there is no known venting. dMn removal is dramatically inhibited under anoxic conditions and by the presence of the biological poison, sodium azide. A conspicuous temperature optimum of dMn removal rates (∼40 °C) and a saturation-like (i.e. Michaelis-Menten) response to O2 concentration were observed, indicating an enzymatic mechanism. dMn removal was resistant to heat treatment used to select for spore-forming organisms, but very sensitive to low concentrations of added Cu, a cofactor required by the putative Mn(II)-oxidizing enzyme. Extended X-ray absorption fine structure spectroscopy (EXAFS) and synchrotron radiation-based X-ray diffraction (SR-XRD) revealed the Mn oxides to have a hexagonal birnessite or δ-MnO2-like mineral structure, indicating that these freshly formed deep-sea Mn oxides are strikingly similar to primary biogenic Mn oxides produced by laboratory cultures of bacteria. Overall, these results reveal a vigorous Mn biogeochemical cycle in the GB hydrothermal plume, where a distinct microbial community enzymatically catalyzes rapid Mn(II) oxidation and the production of Mn biooxides.