Investigating Geobiological Feedbacks During the Evolution of Acidophilic Microorganisms

微生物群落推动全球生物地球化学循环，并将影响植物、动物和环境健康的关键生态系统过程联系起来。因此，地球科学的一个中心目标是对地圈和生物圈之间的相互作用产生新的理解，这些相互作用影响了地球化学循环的演变和生命的多样化。这种相互作用中最突出的可能是含氧光养生物的出现及其代谢活动的产物--氧(O2)。越来越多的证据表明，向厌氧生物圈引入氧气对微生物生命的地球化学循环和功能多样化产生了深远的影响。虽然氧在地质时期内地圈和生物圈元素循环上的指纹日益成为焦点，但关键问题仍然是地圈和生物圈耦合演化之间的动态反馈的性质以及发生关键事件的时间尺度。新的数据表明，以酸性温泉(嗜热性酸菌)为特征的生物的共同进化和温泉栖息地本身的酸性很可能是由过去10亿年发生的一系列地球生物反馈推动的，接近被认为大气氧已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，包括确定地球化学生境的耦合演化与其微生物栖息地的代谢潜力之间的动态。通过对低复杂性酸性生态系统的研究开发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，包括那些与维持植物、动物和环境健康的地球生物反馈直接相关的生态系统和过程。这些研究的结果将由学生、博士后和该项目支持的资深科学家通过在国内和国际会议上发表演讲和提交期刊文章来传播，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所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发生的时间尺度知之甚少，特别是从生物学的角度。这在一定程度上是由于大多数当代生态系统的复杂性，以及在了解塑造这些栖息地及其居民的地质生物相互作用方面存在的困难。这种知识差距阻碍了对生物多样性产生的更全面的了解，无论是在今天还是在过去的地质历史中，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标志物联系起来的能力。新的数据表明，嗜热微生物的进化和酸性生境的大规模生成很可能是由过去10亿年来发生的一系列地质生物反馈推动的。更具体地说，数据表明，至少有两个不同的古菌谱系在进化上汇聚在类似的氧气依赖的代谢策略上，以求在酸性条件下生存，我们假设，在这样做的过程中，他们构建了高度酸性的生态位。在这项工作中，我们将通过结合现场和实验室的分析来解决这一假设，这些分析旨在定义对非生物和生物硫氧化动力学的限制，嗜热嗜酸菌的生理学，以及酸性生境和其嗜热生境的耦合演化。具体地说，我们将应用最先进的分子、生理、进化、地球化学和建模方法来测试我们的主要假设，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中依赖氧气的、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)这些谱系及其酸性生境的共同进化。该项目的完成将以嗜热性酸菌及其酸性温泉栖息地为模型，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。我们从对这些低复杂性生态系统的研究中开发的新的理解和生物信息学工具将适用于更复杂的生态系统和过程。结果将由学生、博士后和PI通过在国内和国际会议上的演讲和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，特别是代表不足的美洲原住民。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，以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，目标是从这一人群中招募学生攻读STEM学科的高级学位。该奖项反映了NSF的法定使命，并通过使用基金会的智力优势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.