Microbial acceleration of aerobic pyrite oxidation at circumneutral pH

Abstract

Pyrite (FeS ) is the most abundant sulfide mineral on Earth and represents a significant reservoir of reduced iron and sulfur both today and in the geologic past. In modern environments, oxidative transformations of pyrite and other metal sulfides play a key role in terrestrial element partitioning with broad impacts to contaminant mobility and the formation of acid mine drainage systems. Although the role of aerobic micro-organisms in pyrite oxidation under acidic-pH conditions is well known, to date there is very little known about the capacity for aerobic micro-organisms to oxidize pyrite at circumneutral pH. Here, we describe two enrichment cultures, obtained from pyrite-bearing subsurface sediments, that were capable of sustained cell growth linked to pyrite oxidation and sulfate generation at neutral pH. The cultures were dominated by two Rhizobiales species (Bradyrhizobium sp. and Mesorhizobium sp.) and a Ralstonia species. Shotgun metagenomic sequencing and genome reconstruction indicated the presence of Fe and S oxidation pathways in these organisms, and the presence of a complete Calvin-Benson-Bassham CO fixation system in the Bradyrhizobium sp. Oxidation of pyrite resulted in thin (30-50 nm) coatings of amorphous Fe(III) oxide on the pyrite surface, with no other secondary Fe or S phases detected by electron microscopy or X-ray absorption spectroscopy. Rates of microbial pyrite oxidation were approximately one order of magnitude higher than abiotic rates. These results demonstrate the ability of aerobic microbial activity to accelerate pyrite oxidation and expand the potential contribution of micro-organisms to continental sulfide mineral weathering around the time of the Great Oxidation Event to include neutral-pH environments. In addition, our findings have direct implications for the geochemistry of modern sedimentary environments, including stimulation of the early stages of acid mine drainage formation and mobilization of pyrite-associated metals.

Microbial metal‐sulfide oxidation in inactive hydrothermal vent chimneys suggested by metagenomic and metaproteomic analyses

“…Apart from iron-oxidizers isolated earlier from inactive sulfides in the East Pacific (Eberhard et al, 1995;Edwards et al, 2003), a Thiomicrospira strain capable of autotrophic growth with pyrrhotite as electron donor was recently isolated from surface sediment near Santa Catalina Island . Biotic acceleration of pyrite oxidation at neutral pH by freshwater Alpha-and Betaproteobacteria was also recently shown in borehole sediment (Washington, USA) enrichment cultures (Percak-Dennett et al, 2017). Notably, the genomes obtained from these enrichments by Percak-Dennett et al (2017) encoded the same metabolic potential in terms of cytochromes, sulfur oxidation and carbon fixation pathways as the gammaproteobacterial bins obtained in this study.…”

“…Biotic acceleration of pyrite oxidation at neutral pH by freshwater Alpha-and Betaproteobacteria was also recently shown in borehole sediment (Washington, USA) enrichment cultures (Percak-Dennett et al, 2017). Notably, the genomes obtained from these enrichments by Percak-Dennett et al (2017) encoded the same metabolic potential in terms of cytochromes, sulfur oxidation and carbon fixation pathways as the gammaproteobacterial bins obtained in this study. Supporting the hypothesis of active interaction with the mineral surface, we found a gammaproteobacterial multi-heme cytochrome c to be the third most abundant annotated protein in the StM-R1 metaproteome.…”

“…Notably, the genomes obtained from these enrichments by Percak‐Dennett et al . () encoded the same metabolic potential in terms of cytochromes, sulfur oxidation and carbon fixation pathways as the gammaproteobacterial bins obtained in this study. Supporting the hypothesis of active interaction with the mineral surface, we found a gammaproteobacterial multi‐heme cytochrome c to be the third most abundant annotated protein in the StM‐R1 metaproteome.…”

Pyrite oxidation mechanism in aqueous medium

“…According to Rojaschapana et al, the oxidizability of Leptospirillum ferrooxidans went beyond that of Fe 3+ alone. To further understand the oxidation mechanism of pyrite in the presence of microorganisms, Percak‐Dennett et al conducted their experiment in circumneutral pH. They found that the thin (30–50 nm) coatings of amorphous Fe(III) oxide were formed during the pyrite oxidation process, with no other secondary Fe or S phases detected.…”

“…Biegler and Swift [86] found that SO 4 2− and S 0 were formed in the anodization process in H 2 SO 4 solution. At the TABLE 1 Pyrite oxidation mechanism proposed by Percak-Dennett et al [68] Reaction Mechanism [31] pyrite went through the following steps during the electrochemical oxidation process. The first step is: FeS 2 !…”