Investigating Geobiological Feedbacks During the Evolution of Acidophilic Microorganisms

微生物群落驱动全球生物地球化学循环，连接影响植物、动物和环境健康的关键生态系统过程。因此，地球科学的一个中心目标是发展对影响地球化学循环演变和生命多样化的地圈和生物圈之间相互作用的新认识。也许这种相互作用中最突出的是含氧光养生物及其代谢活动的产物氧（O2）的出现。越来越多的证据表明，向厌氧生物圈引入氧气对地球化学循环和微生物生命的功能多样化产生了深远的影响。虽然氧在地质时期内对地圈和生物圈元素循环的影响日益成为人们关注的焦点，但地圈和生物圈耦合演化之间动态反馈的性质以及关键事件发生的时间尺度仍然是关键问题。新的数据表明，栖息在酸性温泉中的生物（嗜热嗜酸菌）和温泉栖息地本身的酸性可能是由过去10亿年间发生的一系列地球生物学反馈所驱动的，这一过程接近于大气氧气被认为达到接近当今水平的时间。这些独特的低复杂性酸性生态系统为测试和进一步发展地球科学中的综合概念提供了机会，包括确定地球化学栖息地的耦合演化与其微生物居民的代谢潜力之间的动力学。从低复杂性酸性生态系统的研究中发展出来的新的理解和分析工具将适用于更复杂的生态系统和过程，包括那些直接影响维持植物、动物和环境健康的地球生物学反馈的生态系统和过程。这些研究的成果将由学生、博士后和受资助的资深科学家通过在国内和国际会议上发表报告和提交期刊文章的方式传播，从而促进专业发展。人们普遍认识到生物和地质过程之间的反馈在环境景观及其支持的生物多样性的共同进化中的作用。然而，人们对这些反馈的性质和它们发生的时间尺度知之甚少，特别是从生物学的角度来看。这在一定程度上是由于大多数当代生态系统的复杂性，以及在解开形成这些栖息地及其居民的地理生物相互作用方面所呈现的困难。这种知识差距阻碍了对生物多样性产生的更全面理解的发展，无论是在今天还是在地质历史上，也许更重要的是，限制了我们将岩石记录中的地球化学和生物生物标志物联系起来的能力。新的数据表明，嗜热酸微生物的进化和酸性栖息地的大规模产生可能是由过去10亿年来发生的一系列地球生物学反馈所驱动的。更具体地说，数据表明，至少有两种不同的古细菌谱系在进化上趋同于相似的、依赖氧的代谢策略，以在酸性条件下生存，我们假设，在这样做的过程中，它们构建了高酸性的生态位。在这项工作中，我们将通过结合基于现场和实验室的分析来解决这一假设，旨在定义非生物和生物硫氧化动力学的限制，嗜热嗜酸菌的生理，以及酸性栖息地及其嗜热嗜酸菌的耦合进化。具体来说，我们将运用最先进的分子、生理、进化、地球化学和建模方法来验证我们的主要假设，即酸性温泉环境中微生物的分类和功能多样性是与这些环境的氧依赖性、生物诱导的酸化相一致的。在这项工作中，我们将评估氧对(i)在pH和温度连续体上硫氧化动力学的影响，（ii）促进沿该连续体居住的适应性，以及（iii）这些谱系及其酸性栖息地的共同进化。该项目的完成将使我们更全面地了解微生物与其环境之间的相互作用如何导致生物多样性和地质变化，并以嗜热嗜酸菌及其酸性温泉栖息地为模型。我们从这些低复杂性生态系统的研究中发展出来的新的认识和生物信息学工具将适用于更复杂的生态系统和过程。研究结果将由学生、博士后和PI在国内和国际会议上发表报告，并通过提交期刊文章来传播，从而促进专业发展。通过这项工作，我们将继续招募并为有动力的本科生和研究生提供研究机会，特别是代表性不足的印第安人。为了实现这一目标，我们将继续与萨利什库特奈学院建立合作伙伴关系，吸引本科生在蒙大拿州立大学完成为期六周的暑期研究实习，目标是招募来自这一人口统计的学生，以寻求STEM学科的高级学位。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

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. 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.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.