Investigating Geobiological Feedbacks During the Evolution of Acidophilic Microorganisms

Microbial communities drive global biogeochemical cycles and link critical ecosystem processes influencing plant, animal, and environmental health. Consequently, a central goal in the geosciences is to develop new understanding of the interactions between the geosphere and the biosphere that have influenced the evolution of geochemical cycles and the diversification of life. Perhaps the most prominent of such interactions involves the emergence of oxygenic phototrophs and the product of their metabolic activity, oxygen (O2). Accumulating evidence indicates that the introduction of oxygen to an anaerobic biosphere had a profound influence on geochemical cycles and the functional diversification of microbial life. While the fingerprint of oxygen on the cycling of elements in the geosphere and biosphere over geological time is increasingly coming into focus, key questions remain on the nature of the dynamic feedbacks between the coupled evolution of the geosphere and the biosphere and on the timescales over which key events took place. New data suggests that the co-evolution of organisms that characteristically inhabit acidic hot springs (thermoacidophiles) and the acidic nature of the hot spring habitats themselves was likely driven by a series of geobiological feedbacks that have taken place over the past one billion years, near to the time when atmospheric oxygen is thought have reached near present-day levels. These unique low complexity acidic ecosystems provide an opportunity to test and further develop integrated concepts in the geosciences, including identifying the dynamics between the coupled evolution of geochemical habitats and the metabolic potential of their microbial inhabitants. The new understanding and analytical tools that are developed from the study of low complexity acidic ecosystems will be applicable to more complex ecosystems and processes, including those that have direct bearing on the geobiological feedbacks that sustain plant, animal, and environmental health. Results from these studies will be disseminated by students, postdocs, and the senior scientists supported by the project through presentations at national and international conferences and through submission of journal articles, thereby boosting professional development. <br/><br/>There is widespread recognition of the role of feedbacks between biological and geological processes in the co-evolution of environmental landscapes and the biodiversity they support. However, far less is known of the nature of these feedbacks and the time scales over which they occur, especially from the biological perspective. This is due, in part, to the complexity of most contemporary ecosystems and the difficulty this presents in deconvoluting the geobiological interactions that have shaped these habitats and their inhabitants. This knowledge gap prevents the development of a more complete understanding of the generation of biological diversity, both today and in the geological past, and perhaps more importantly, limits our ability to link geochemical and biological biomarkers in the rock record. New data suggests that the evolution of thermoacidophilic microorganisms and the largescale generation of acidic habitats was likely driven by a series of geobiological feedbacks that have taken place over the past one billion years. More specifically, data indicates that at least two divergent archaeal lineages converged evolutionarily upon similar, oxygen-dependent metabolic strategies to survive acid conditions, and we have hypothesized that, in doing so, they have constructed highly acidic ecological niches. In this work we will address this hypothesis by combining field- and laboratory-based analyses aimed at defining constraints on the kinetics of abiotic and biotic sulfur oxidation, the physiology of thermoacidophiles, and the coupled evolution of acidic habitats and their thermoacidophilic inhabitants. Specifically, we will apply state of the art molecular, physiological, evolutionary, geochemical, and modeling approaches to test our primary hypothesis that taxonomic and functional diversity of microorganisms in acidic hot spring environments evolved in concert with the oxygen-dependent, biologically induced acidification of those environments. In this work, we will evaluate the influence of oxygen on (i) the kinetics of sulfur oxidation over a pH and temperature continuum, (ii) the adaptations that facilitate habitation along this continuum and, (iii) the co-evolution of these lineages and their acidic habitats. Completion of this project will culminate in a more complete understanding of how interactions between microorganisms and their environment can lead to biological diversification and geological change, using thermoacidophiles and their acidic hot spring habitats as a model. New understanding and bioinformatics tools that we develop from the study of these low complexity ecosystems will be applicable to more complex ecosystems and processes. Results will be disseminated by students, postdocs, and the PI through presentations at national and international conferences and through submission of journal articles, thereby boosting professional development. Through this work, we will continue to recruit and offer research opportunities to motivated undergraduate and graduate students, particularly underrepresented Native Americans. To achieve this goal, we will continue the partnership that has been forged with Salish Kootenai College to attract undergraduates to complete a six-week summer research internship at Montana State University, with the goal of recruiting students from this demographic to seek an advanced degree in a STEM discipline.<br/><br/>This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.