One-Year In Situ Incubation of Pyrite at the Deep Seafloor and Its Microbiological and Biogeochemical Characterizations.

Abstract

In this study, we performed a year-long in situ incubation experiment on a common ferrous sulfide (Fe-S) mineral, pyrite, at the oxidative deep seafloor in the hydrothermal vent field in the Izu-Bonin arc, Japan, and characterized its microbiological and biogeochemical properties to understand the microbial alteration processes of the pyrite, focusing on Fe(II) oxidation. The microbial community analysis of the incubated pyrite showed that the domain Bacteria heavily dominated over Archaea compared with that of the ambient seawater, and Alphaproteobacteria and Gammaproteobacteria distinctively codominated at the class level. The mineralogical characterization by surface-sensitive Fe X-ray absorption near-edge structure (XANES) analysis revealed that specific Fe(III) hydroxides (schwertmannite and ferrihydrite) were locally formed at the pyrite surface as the pyrite alteration products. Based on the Fe(III) hydroxide species and proportion, we thermodynamically calculated the pH value at the pyrite surface to be pH 4.9 to 5.7, indicating that the acidic condition derived from pyrite alteration was locally formed at the surface against neutral ambient seawater. This acidic microenvironment at the pyrite surface might explain the distinct microbial communities found in our pyrite samples. Also, the acidity at the pyrite surface indicates that the abiotic Fe(II) oxidation rate was much limited at the pyrite surface kinetically, 3.9 × 103- to 1.6 × 105-fold lower than that in the ambient seawater. Moreover, nanoscale characterization of microbial biomolecules using carbon near-edge X-ray absorption fine-structure (NEXAFS) analysis showed that the sessile cells attached to pyrite excreted the acidic polysaccharide-rich extracellular polymeric substances at the pyrite surface, which can lead to the promotion of biogenic Fe(II) oxidation and pyrite alteration. IMPORTANCE Pyrite is one of the most common Fe-S minerals found in submarine hydrothermal environments. Previous studies demonstrated that the Fe-S mineral can be a suitable host for Fe(II)-oxidizing microbes in hydrothermal environments; however, the details of microbial Fe(II) oxidation processes with Fe-S mineral alteration are not well known. The spectroscopic and thermodynamic examination in the present study suggests that a moderately acidic pH condition was locally formed at the pyrite surface during pyrite alteration at the seafloor due to proton releases with Fe(II) and sulfidic S oxidations. Following previous studies, the abiotic Fe(II) oxidation rate significantly decreases with a decrease in pH, but the biotic (microbial) Fe(II) oxidation rate is not sensitive to the pH decrease. Thus, our findings clearly suggest that the pyrite surface is a unique microenvironment where abiotic Fe(II) oxidation is limited and biotic Fe(II) oxidation is more prominent than that in neutral ambient seawater.