Microbial Architecture of Environmental Sulfur Processes: A Novel Syntrophic Sulfur-Metabolizing Consortia

Microbial oxidation of sulfur-rich mining waste materials drives acid mine drainage (AMD) and affects the global sulfur biogeochemical cycle. The generation of AMD is a complex, dynamic process that proceeds via multiple reaction pathways. The role of natural consortia of microbes in AMD generation, however, has received very little attention despite their widespread occurrence in mining environments. Through a combination of geochemical experimentation and modeling, scanning transmission X-ray microscopy, and fluorescent in situ hybridization, we show a novel interdependent metabolic arrangement of two ubiquitous and abundant AMD bacteria: chemoautotrophic sulfur-oxidizing Acidithiobacillus sp. and heterotrophic Acidiphilium sp. Highly reminiscent of anaerobic methane oxidation (AOM) consortia, these bacteria are spatially segregated within a planktonic macrostructure of extracellular polymeric substance in which they syntrophically couple sulfur oxidation and reduction reactions in a mutually beneficial arrangement that regenerates their respective sulfur substrates. As discussed here, the geochemical impacts of microbial metabolism are linked to the consortial organization and development of the pod structure, which affects cell−cell interactions and interactions with the surrounding geochemical microenvironment. If these pods are widespread in mine waters, echoing the now widespread discovery of AOM consortia, then AMD-driven CO2 atmospheric fluxes from H2SO4 carbonate weathering could be reduced by as much as 26 TgC/yr. This novel sulfur consortial discovery indicates that organized metabolically linked microbial partnerships are likely widespread and more significant in global elemental cycling than previously considered.