Thermodynamics of Acidophiles: Energetics of Microbial Growth, Response to Substrate Availability, and Interactions with Heavy Metal

Chemical and physical properties play a crucial role in the type and efficiency of microbial activity that can be supported within an ecosystem. In return, the presence of microbial activity affects the surrounding environment, driving biogeochemical cycles, altering chemical fluxes via metabolism and surface interactions, and affecting the lithosphere through mineral precipitation or dilution. Fluctuations in aqueous geochemistry, however, can alter growth efficiency and overall energetic demands of microorganisms. This dissertation uses a thermodynamic approach to explore energy requirements of acidophilic microorganisms in response to chemical changes and how their cell surfaces interact with heavy metals. Chapter 2 explores the effects of energy source availability on microbial energetics with the sulfur-oxidizing Archaea Acidianus ambivalens in three decreasing concentrations of dissolved oxygen, from aerobic to microaerobic. The results show that growth proceeds most efficiently under low levels of oxygen while high levels of oxygen require the most energy, likely due to higher maintenance energy demands as a result of oxidative stress. Chapter 3 studies the energetic response to environmental redox conditions by quantifying bioenergetics of A. ambivalens during anaerobic growth with H2 and sulfur. A. ambivalens growth was not affected by environmental oxidation state and shows similar growth efficiencies and energy budgets between anaerobic and microaerobic conditions. However, microaerobic growth required less overall Gibbs energy, suggesting a slight preference for growth on sulfur and O2 in low-oxygen environments. Chapter 4 characterizes the thermodynamics of growth for two mesophilic bacteria, Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans. Energetics were determined during aerobic growth with Fe2+ and oxygen for A. ferrooxidans and with sulfur and oxygen for both A. ferrooxidans and A. thiooxidans. A. ferrooxidans grew most efficiently with sulfur and O2, indicating a preference over growth with Fe2+. Energetics for all three sulfur oxidizers, A. ambivalens, A. ferrooxidans, and A. thiooxidans , are compared and show a significant correlation between Gibbs energy consumed, enthalpies of growth, and biomass yield, suggesting growth energetics are impacted more by chemistry changes via catabolism than biochemical differences between species. In Chapter 5, I measure cadmium adsorption to the thermoacidophile Sulfolobus acidocaldarius cell surfaces and provide the first thermodynamic description of surface adsorption of Cd by S. acidocaldarius. These results will not only help us understand interactions between natural environments and microbial activity, but will also help evaluate habitability of environments and energy available for life elsewhere.