Relationships among geochemical processes and microbial community structure in a unique high-arsenic, sulfidic geothermal spring in Yellowstone National Park

Abstract

The metabolisms of chemotrophic microorganisms are linked with the geochemical transformation of redox-active chemical species and mineral precipitation-dissolution reactions in geothermal environments. The objectives of the current work were to correlate the spatial distribution of microbial populations with changes in aqueous geochemistry and mineralogy in a unique Yellowstone National Park (YNP) geothermal spring, and to cultivate thermophilic microorganisms with phylogenetic and metabolic relevance to spring conditions. The geothermal spring (hereafter referenced as Joseph's Coat Spring -JC3) contains the highest reported concentrations of arsenic, antimony and thiosulfate of any geothermal feature studied in YNP. A suite of analytical and molecular approaches including aqueous geochemical and dissolved gas analysis, solid phase characterization, energetic calculations, microscopy and 16S rRNA gene sequence distribution were utilized to correlate specific microbial populations with biogeochemical processes. Predominant geochemical changes observed within the outflow channel were disappearance of methane, dissolved sulfide and ingassing of dissolved oxygen. Oxidation of arsenite was significant within the outflow channel despite the slow ingassing rates of dissolved oxygen. Microbial 16S rRNA gene sequences were determined at locations in the source pool and within the outflow channel.

Shifts in microbial community structure were observed as a function of distance from the source. Source pool pyritic phases and Sb and S rich sediments were dominated by Geothermobacterium, Desulfurococcus, and Thermofilum-like sequences. Shifts in microbial community structure were observed within the outflow channel including appearance of Aquificales and Thermales sequences down gradient. Cultivation strategies based on spring geochemistry and energetic analysis were successful in isolating two novel thermophilic Crenarchaeota with high 16S rRNA gene sequence similarity to those determined within the spring sediments. An anaerobic, heterotrophic, S-respiring Thermofilum-like strain (WP28t) exhibits characteristics consistent with spring geochemistry, and confirms the importance of microbial reduction of elemental S in this spring. Detailed geochemical characterization and phylogenetic analysis of 16S rRNA gene sequences will continue to guide cultivation strategies for isolating novel microorganisms. This research indicates the importance of correlating microbial community analysis with geochemical measurements as an integrated approach for understanding the primary carbon and energy sources that link microbial populations with specific geochemical processes.