Microbial chemolithotrophic oxidation of pyrite in a subsurface shale weathering environment: Geologic considerations and potential mechanisms

Abstract

Oxidative weathering of pyrite plays an important role in the biogeochemical cycling of Fe and S in terrestrial environments. While the mechanism and occurrence of biologically accelerated pyrite oxidation under acidic conditions are well established, much less is known about microbially mediated pyrite oxidation at circumneutral pH. Recent work (Percak‐Dennett et al., 2017, Geobiology, 15, 690) has demonstrated the ability of aerobic chemolithotrophic microorganisms to accelerate pyrite oxidation at circumneutral pH and proposed two mechanistic models by which this phenomenon might occur. Here, we assess the potential relevance of aerobic microbially catalyzed circumneutral pH pyrite oxidation in relation to subsurface shale weathering at Susquehanna Shale Hills Critical Zone Observatory (SSHCZO) in Pennsylvania, USA. Specimen pyrite mixed with native shale was incubated in groundwater for 3 months at the inferred depth of in situ pyrite oxidation. The colonized materials were used as an inoculum for pyrite‐oxidizing enrichment cultures. Microbial activity accelerated the release of sulfate across all conditions. 16S rRNA gene sequencing and metagenomic analysis revealed the dominance of a putative chemolithoautotrophic sulfur‐oxidizing bacterium from the genus Thiobacillus in the enrichment cultures. Previously proposed models for aerobic microbial pyrite oxidation were assessed in terms of physical constraints, enrichment culture geochemistry, and metagenomic analysis. Although we conclude that subsurface pyrite oxidation at SSCHZO is largely abiotic, this work nonetheless yields new insight into the potential pathways by which aerobic microorganisms may accelerate pyrite oxidation at circumneutral pH. We propose a new “direct sulfur oxidation” pathway, whereby sulfhydryl‐bearing outer membrane proteins mediate oxidation of pyrite surfaces through a persulfide intermediate, analogous to previously proposed mechanisms for direct microbial oxidation of elemental sulfur. The action of this and other direct microbial pyrite oxidation pathways have major implications for controls on pyrite weathering rates in circumneutral pH sedimentary environments where pore throat sizes permit widespread access of microorganisms to pyrite surfaces.

Potential autotrophic carbon-fixer and Fe(II)-oxidizer Alcanivorax sp. MM125-6 isolated from Wocan hydrothermal field

“…The dominant genus Marinobacter , involved in iron oxidation ( Edwards et al, 2003b ), and the genus Halomonas , affiliated with acid-producing bacteria ( Sanchez-Porro et al, 2010 ), were both adhered to the slabs, which probably contribute to release of Zn from sulfide minerals. In our laboratory enrichment, we found that three genera, Pseudomonas, Paracoccus , and Alcanivorax from the slab were effectively enriched and eventually attached to the metal sulfide powder ( Figures 1 , 2 ), indicating their potential for iron or sulfur oxidation and interaction between cells and sulfide minerals ( Napieralski et al, 2021 ).…”

The contribution of living organisms to rock weathering in the critical zone

“…Since mechanisms of mineral weathering are relatively well known and ubiquitously distributed among bacterial and fungal communities, and since the relationship between dissolution rate enhancement and the nature of the different weathering agents has already been well explored, there is a need to focus upcoming studies on the screening of these functions and of their expression in field-relevant settings, using metagenomic and metabolomic tools (while taxonomic survey only provide at best indirect information on that matter). Such developments are currently ongoing, with the application of terabase-scale cultivationindependent metagenomics to BW systems, which is able to accurately reconstruct the metabolism and ecological roles of microbial consortia from natural samples [195][196][197] . In parallel, a growing corpus of literature is actively seeking for the genes involved in microbial weathering-or the "weathering microbiome" 196 -e.g.…”

Microbially-mediated aerobic oxidation of trace element-bearing pyrite in neutral-pH sandstone aquifer sediments

“…14,15 Only recently, however, has explicit evidence for microbially accelerated aerobic pyrite oxidation at neutral pH been obtained. 16,17 Percak-Dennett et al 16 demonstrated sustained enhancement of sulfate release in the presence of a live, natural inoculum over multiple generations in cultures grown on synthetic framboidal pyrite. Napieralski et al 17 demonstrated 2–5 fold accelerated oxidation of specimen pyrite by organisms that had previously colonized pyrite incubated in situ in a pyrite-bearing shale formation in central Pennsylvania.…”