Geochemical Constraints on the Distribution and Function of Thermoproteales Populations in Yellowstone National Park

Abstract:

Metagenome surveys in Yellowstone National Park (YNP) indicate that members of the order Thermoproteales (phylum Crenarchaeota) are abundant in high-temperature (> 70 °C) geothermal systems. The goals of this study were to compare Thermoproteales sequences from different geothermal environments across YNP, and determine the variation in metabolic potential associated with their distribution. Thermoproteales sequence assemblies (> 0.5 Mbases) were curated from 10 habitats ranging in pH from 3 - 9 (with or without dissolved sulfide). The distribution of specific Thermoproteales is constrained by pH: Vulcanisaeta-like sequences are the most abundant Thermoproteales at pH < 6, Caldivirga-like sequences more important from pH 4 - 6, and Thermoproteus-like sequences abundant from ~ pH 5 - 7, and at pH > 7, Pyrobaculum­-like sequences are nearly the only Thermoproteales present. Thermoproteales populations are generally found in hypoxic systems where reduced forms of S and As often limit concentrations of dissolved oxygen. These environmental conditions are correlated with the presence or absence of system-defined respiratory complexes including different terminal oxidases (e.g., aa₃ or bd), numerous DMSO-molybdopterins, and dissimilatory sulfate reductases. Metabolic reconstruction of different genera revealed similar pathways for the degradation of carbohydrates, amino acids, and lipids across sites. Only the Thermoproteus and Pyrobaculum populations contained the three marker genes for the dicarboxylate/4-hyhdroxybutyrate cycle, which is responsible for the fixation of inorganic carbon. Most Thermoproteales populations have the metabolic capacity to synthesize their requirements for vitamins, cofactors, amino acids, and/or nucleotides. Our results indicate that Thermoproteales populations are important members of high-temperature microbial communities across a wide pH range, are responsible for the degradation of organic carbon, and may also serve as a source of metabolites required by other community members. Thermoproteales genera are abundant thermophiles in many hypoxic (and especially sulfidic) systems; however, the presence of introns in the 16S rRNA gene of many Thermoproteales often precludes accurate abundance estimates using universal primers.