Anoxygenic phototrophs span geochemical gradients and diverse morphologies in terrestrial geothermal springs

Extant anoxygenic phototrophs are taxonomically, physiologically, and metabolically diverse and include examples from all seven bacterial phyla with characterized phototrophic members. pH, temperature, and sulfide are known to constrain phototrophs, but how these factors dictate the distribution and activity of specific taxa of anoxygenic phototrophs has not been reported. Here, we hypothesized that within the known limits of pH, temperature, and sulfide, the distribution, abundance, and activity of specific anoxygenic phototrophic taxa would vary due to key differences in the physiology of these organisms. To test this hypothesis, we examined the distribution, abundance, and potential activity of anoxygenic phototrophs in filaments, microbial mats, and sediments across geochemical gradients in geothermal features of Yellowstone National Park, which ranged in pH from 2.2 to 9.4 and in temperature from 31.5°C to 71.0°C. Indeed, our data indicate putative aerobic anoxygenic phototrophs within the Proteobacteria are more abundant at lower pH and lower temperature, while phototrophic Chloroflexi are prevalent in circumneutral to alkaline springs. In contrast to previous studies, our data suggest sulfide is not a key determinant of anoxygenic phototrophic taxa. Finally, our data underscore a role for photoheterotrophy (or photomixotrophy) across geochemical gradients in terrestrial geothermal ecosystems. Importance: There is a long and rich history of literature on phototrophs in terrestrial geothermal springs. These studies have revealed sulfide, pH, and temperature are the main constraints on phototrophy. However, the taxonomic and physiological diversity of anoxygenic phototrophs suggests that, within these constraints, specific geochemical parameters determine the distribution and activity of individual anoxygenic phototrophic taxa. Here, we report the recovery of sequences affiliated with characterized anoxygenic phototrophs in sites that range in pH from 2 to 9 and in temperature from 31°C to 71°C. Transcript abundance indicates anoxygenic phototrophs are active across this temperature and pH range. Our data suggest sulfide is not a key determinant of anoxygenic phototrophic taxa and underscore a role for photoheterotrophy in terrestrial geothermal ecosystems. These data provide the framework for high-resolution sequencing and in situ activity approaches to characterize the physiology of specific anoxygenic phototrophic taxa across a broad range of temperatures and pH.