pH and thiosulfate dependent microbial sulfur oxidation strategies across diverse environments

• Published in: Frontiers in microbiology Vol. 15; p. 1426584
• Main Authors: Twible, Lauren E, Whaley-Martin, Kelly, Chen, Lin-Xing, Colenbrander Nelson, Tara, Arrey, James L S, Jarolimek, Chad V, King, Josh J, Ramilo, Lisa, Sonnenberg, Helga, Banfield, Jillian F, Apte, Simon C, Warren, Lesley A
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Media S.A 19.07.2024
• Subjects: sox genes; sulfur oxidizing bacteria (SOB); tailings impoundments; thiosulfate; pH; sox genes; sulfur oxidizing bacteria (SOB); tailings impoundments; thiosulfate
• ISSN: 1664-302X; 1664-302X
• DOI: 10.3389/fmicb.2024.1426584

Sulfur oxidizing bacteria (SOB) play a key role in sulfur cycling in mine tailings impoundment (TI) waters, where sulfur concentrations are typically high. However, our understanding of SOB sulfur cycling via potential S oxidation pathways ( , r , and S I) in these globally ubiquitous contexts, remains limited. Here, we identified TI water column SOB community composition, metagenomics derived metabolic repertoires, physicochemistry, and aqueous sulfur concentration and speciation in four Canadian base metal mine, circumneutral-alkaline TIs over four years (2016 - 2019). Identification and examination of genomes from nine SOB genera occurring in these TI waters revealed two pH partitioned, metabolically distinct groups, which differentially influenced acid generation and sulfur speciation. Complete (c ) dominant SOB (e.g., spp., spp.) drove acidity generation and S O consumption via the c pathway at lower pH (pH ~5 to ~6.5). At circumneutral pH conditions (pH ~6.5 to ~8.5), the presence of non-c dominant SOB (hosting the incomplete , r , and/or other S oxidation reactions; e.g. spp., spp.) were associated with higher [S O ] and limited acidity generation. The S I pathway part 1 ( ; S O to S O ), was not constrained by pH, while S4I pathway part 2 (S O disproportionation via ) was limited to spp. and thus circumneutral pH values. Comparative analysis of low, natural (e.g., hydrothermal vents and sulfur hot springs) and high (e.g., Zn, Cu, Pb/Zn, and Ni tailings) sulfur systems literature data with these TI results, reveals a distinct TI SOB mining microbiome, characterized by elevated abundances of c dominant SOB, likely sustained by continuous replenishment of sulfur species through tailings or mining impacted water additions. Our results indicate that under the primarily oxic conditions in these systems, S O availability plays a key role in determining the dominant sulfur oxidation pathways and associated geochemical and physicochemical outcomes, highlighting the potential for biological management of mining impacted waters via pH and [S O ] manipulation.