Geochemical and Genomic Characterization of a Microbially-Mediated Dynamic Sulfur Cycle in Santa Paula Creek, CA

The role of microbes in the terrestrial sulfur cycle is relatively understudied compared to marine systems. Although these communities may represent some of earliest colonizers of land, the geochemical effects associated with their metabolisms remain poorly constrained. Here we present microbiological diversity and isotopic data which map the organisms and sulfur processes present throughout Santa Paula Creek (SPC; Ventura, CA), a unique fluvial system charged with sulfur and heavy hydrocarbons from the underlying sulfide and organic-rich Monterey Formation. Microbial ecology in algal mats and filamentous streamers was analyzed by microscopy and 16S rRNA sequencing, while organic samples and submerged silver strips were subjected to high-resolution elemental and d³⁴S isotopic measurements.

These multidisciplinary analyses demonstrate the biogeochemical cycling of elemental, reduced, and oxidized sulfur facilitated by diverse microbial communities. Genomic data reveal that streamers in fast-flowing and deeper areas of SPC are dominated by closely associated communities of sulfur oxidizers (Thiothrix spp.) and the polyphosphate-accumulating bacterium 'Ca. Accumulibacter phosphatis.' Bulk d³⁴S data and incubations of streamers with ¹⁵NH₄⁺, analyzed by NanoSIMS, confirm the presence of diverse metabolisms which cycle sulfur under both oxic and anoxic conditions and induce an isotope effect. In contrast, the algal and bacterial mats in slow-flowing waters host communities of anoxygenic phototrophic sulfur bacteria, sulfate-reducing bacteria, and 'Ca. A. phosphatis.' SIMS analyses of silver strips subjected to simulated day/night conditions within the mats reveal a dynamic diurnal cycling of sulfur oxidizers and sulfate reducers associated with a vertical sulfide abundance gradient and d³⁴S range (-28 to +8‰). Overall, our results suggest the presence of sulfidic and dysoxic microenvironments within the stream, similar to ancient black shales preserved under euxinic conditions. Further study of SPC will elucidate the role of microbes in intermittently reducing conditions and help develop a geochemical proxy for ancient terrestrial communities which may have driven a complex sulfur cycle.