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.