Hydrogen and Primary Productivity: Inference of Biogeochemistry from Phylogeny in a Geothermal Ecosystem

The geochemical energy sources for microbial primary productivity in the >70°C geothermal springs of Yellowstone National Park have not been understood. Results from phylogenetic studies of geothermal communities indicate, unexpectedly, that hydrogen-metabolizing organisms, both known and novel, dominate these communities. Hydrogen (H2) is the basis of diverse microbial metabolisms, yet little is known about how this important energy source functions in natural microbial communities. We measured source waters in the Yellowstone geothermal area by gas chromatography to survey the potential distribution of hydrogen concentrations in high-temperature waters (hot springs, streams, geothermal vents, and a well). The results indicate levels in excess of 300 nM H2 in chemically diverse settings. Extensive, culture-independent molecular phylogenetic surveys of microbial communities from several locations with different chemistries also were conducted. These surveys were based on cloning and sequencing of 16S rRNA genes for phylogenetic analyses to determine the nature and quantities of microbial diversity that constitute these communities. Analyses of DNA sequences show a dominance of organisms of the phylogenetic kinds known to metabolize H2 as an energy source. Sulfur metabolism is commonly invoked in geothermal bioenergetics, and organisms of the kinds that rely on sulfur metabolism occur in these settings but are not numerically prominent. Thermodynamic modeling of potential energy sources in these settings shows that a microaerophilic hydrogen-based metabolism is most energetically favorable, even in the presence of high concentrations of sulfide. Consequently, we propose that molecular hydrogen provides the main driving energy for primary productivity in this, and probably other, geothermal ecosystems.