Coupled Iron and Sulfur Transformations in Hydrothermal Springs

Abstract:

Iron (Fe) and sulfur (S) compounds are common constituents of terrestrial hydrothermal systems. The transformation of Fe and S compounds is inferred to be an ancient mechanism of energy conservation that is still represented in extant life inhabiting contemporary hydrothermal environments. While substantial research has been conducted to uncover the ability of microorganisms to couple Fe and S transformations with other biogeochemical cycles (e.g., H, O, C cycles) in hydrothermal environments, few studies have focused on the interplay between the Fe and S cycles. In particular, a paucity of studies has been conducted on this phenomenon in acidic high temperature ecosystems despite the common co-occurrence of Fe and S in these environments. Here, we report the isolation and physiological characterization of a metabolically diverse thermoacidiphilic and autotrophic archaeon from an acidic hot spring environment in Yellowstone National Park (YNP) that is capable of both direct and indirect coupling of the Fe and S cycles. Growth experiments indicate differential attachment requirements depending on the mode of growth and imply the importance of intermediate sulfur species in supporting its metabolism. Genomic analyses confirm the metabolic plasticity of this strain and suggest numerous other mechanisms by which this organism may exploit other geochemical cycles during Fe or S dependent growth. Cultivation and cultivation independent approaches suggest that the distribution of this archaeon is widespread in Fe and S rich hot spring environments in YNP and is likely a keystone population in these environments, responsible for a large proportion of primary productivity. These results underscore the utility of integrating geochemical, cultivation, physiological, and genomic approaches in understanding biogeochemical cycling in volcanic environments.