Microbial sulfur cycling determinants and implications for environmental impacts

Abstract

Sulfur-oxidizing bacteria (SOB) play a vital role in the occurrence of sulfur oxidation intermediate (SOI) compounds often recalcitrant to currently available, abiotic treatment within metal mine tailings impoundments (TI). As inadvertent SOI discharge post-treatment can lead to the uncontrolled acidification of receiving environments, it becomes increasingly important to elucidate the environmental controls on SOB identities and sulfur cycling within these relatively unstudied systems. Here, results identified controlling factors on SOB community differentiation and associated metabolic pathway occurrence through integrated physicochemical, geochemical, and microbial field and experimental investigation across three summers (2016, 2017, 2021) in a stratified Northern Ontario base metal TI. Dynamic shifts in SOB communities and sulfur oxidation pathways were primarily driven by [S₂O₃²⁻] and further influenced by pH, [O₂], and conductivity. At [S₂O₃²⁻] above 0.03 mM, Halothiobacillus spp. was observed to dominate in lower pH, higher conductivity conditions where complete SOI oxidation, mediated through the complete Sox pathway, is suggested to reduced [SOI] in treated discharge waters. At [S₂O₃²⁻] below 0.03 mM, an SOB assemblage (Thiovirga spp., Thiobacillus spp., and Sediminibacterium spp.) was observed to collectively dominate under higher pH and lower conductivity, associated with SOI persistence due to SOI recycling pathways (incomplete Sox, rDSR, S₄I). Targeted SOB enrichment cultures confirmed the importance of S₂O₃²⁻ availability in driving SOB community shifts and the capability of Halothiobacillus to outcompete other SOB under oxygenated, high [S₂O₃²⁻] conditions. Trends observed here for mine TI associated SOB were found to also occur across a broader suite of contexts using literature data, indicating their wider ecological relevance in interpreting outcomes associated with SOB activity. Results also provide new insights into improved, biologically informed management of sulfur associated risks with potential SOB manipulation through [S₂O₃²⁻], pH, and/or [O₂] controls.