Flexibility in the mineral dependent metabolism of a thermoacidophilic crenarchaeote
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Date
2017
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Montana State University - Bozeman, College of Letters & Science
Abstract
This dissertation focuses on understanding the metabolic flexibility of a thermoacidophilic crenarchaeote, the mechanisms underlying its physiology, and the consequences for its ecology. Acidianus strain DS80 was isolated from an acidic spring in Yellowstone National Park (YNP) and displays versatility in energy metabolism, using soluble and insoluble substrates during chemolithoautotrophic, chemoheterotrophic, and/or chemolithoheterotrophic growth, and is widely distributed among YNP springs. This flexibility suggests that strain DS80 is of utility as a model thermoacidophile that allows investigation towards how metabolically flexible microorganisms select among available substrates and how these traits influence their natural distributions. Moreover, this plasticity allows investigation of the agreement between thermodynamic metabolic predictions and physiological measurements. Here, I showed that strain DS80 prefers growth with redox couples that provide less energy (H2/S°) when compared to other redox couples (H2/Fe3+ or S°/Fe3+). I present a bioenergetic-physiological argument for this preference, suggesting that the preferential use of substrates in metabolically versatile strains, such as strain DS80, is dictated by differences in the energy demand of electron transfer reactions rather than the energy supply. These observations may help explain why thermodynamic approaches alone are often not enough to accurately predict the distribution and activity of microorganisms in environments. I then showed that genome-guided predictions of energy and carbon metabolism of organisms may not agree with physiological observations in the laboratory, and by extension, the environment. Using a suite of physiological experiments, I provide evidence that the availability of electron acceptors influences the spectrum of potential electron donors and carbon sources that can sustain growth. Similarly, the availability of H2 enables the use of organic carbon sources in DS80 cells respiring S°, thereby expanding the ecological niche of this organism by allowing them to compete for a wider array of substrates that are available in dynamic environments. Finally, I showed that strain DS80 can use several minerals for chemolithotrophy and that the use of specific metabolisms dictates the requirement for direct access to these minerals. Taken together, the results shown here provide novel insight into the extent and mechanisms of metabolic flexibility of chemolithotrophs and the consequences for their ecology.