MIM: A thermodynamic theory of microbiome assembly, adaptation and evolution evaluated using modular microbial environments

MIM：使用模块化微生物环境评估微生物组组装、适应和进化的热力学理论

• 批准号: 2125069
• 负责人: Eoin Brodie
• 金额: $ 240万
• 依托单位: University of California-Berkeley
• 依托单位国家: 美国
• 项目类别: Standard Grant
• 财政年份: 2021
• 资助国家: 美国
• 起止时间: 2021-10-01 至 2026-09-30
• 项目状态: 未结题
• 来源: https://www.nsf.gov/awardsearch/showAward?AWD_ID=2125069&HistoricalAwards=false
• 关键词: MIM; thermodynamic; theory; microbiome; assembly

Across Earth’s ecosystems, microbes adapt and form communities (microbiomes) across gradients of energy and resource richness. Like the machines and electrical circuits we engineer, power and efficiency are key features that also determine the competitiveness of microbes in communities. Over evolutionary time, microbes have optimized their own molecular machines to convert available energy with high efficiency, minimizing the loss of waste energy as heat. Microbes have a range of strategies, reflecting the balance between the rate of new cell production (power), and its efficiency (yield), while also dealing with various costs of survival that reduce yield. This research project will test the hypothesis that microbiomes, assemble from individual members to form communities that also optimize power while increasing efficiency. This principle of power and efficiency optimization may apply generally across different levels of biological organization from proteins to ecosystems. Researchers will study microbiomes from soils and the human gut as model systems to test this idea. They will develop a new experimental platform, involving multiple compartments to control how microbiomes interact, with integrated nanotechnology sensors to measure microbial efficiency as heat output, plus advanced microscopy to measure yield as microbes grow. This work will test if information stored in microbial genomes can predict their power-yield strategies, and if aspects of microbiome diversity can be related to efficiency, developing a predictive modeling framework. If this fundamental thermodynamic theory can explain patterns in biological organization from cells to communities, it will provide an important new framework to predict how biology will respond to future conditions on Earth. Broader impacts include involving community college students in the research, in addition to graduate and postdoctoral students. Outreach activities consist of developing scientific videos for a storytelling platform, which would be available to the general public. Microbes, like all living organisms, maintain the order of life through the creation of entropy. They exist in open, non-equilibrium thermodynamic systems, across gradients of free-energy that fuel the formation and maintenance of structures (proteins, cells, communities) that enhance exergy flow, while attempting to minimize dissipation of waste heat – enhancing overall entropy production in the process. The assembly and succession of microbial communities are driven by flows of exergy, and it is the trade-off between maximum power and minimum heat dissipation that regulate yield (i.e. efficiency). This trade-off towards the production of entropy is a fundamental thermodynamic principle. As a biological optimization function, the optimization of power and yield aligns thermodynamics and evolution through natural selection, in that constraints such as resource availability or stress, modulate the fitness of an organism depending on the placement of their power:yield strategy across a Pareto optimal curve. How these trade-offs manifest at the community scale has not been empirically tested. This research will test this by (1) developing a novel integrated nanocalorimetry-microfluidics platform to control gradients of resources and stress, simultaneously quantifying power, yield and entropy production in an open system; (2) performing a series of manipulative experiments to evaluate how properties of microorganisms and microbiomes relate to power, yield and entropy production and bio(geo)chemical outputs, and (3) develop simulation tools based on the thermodynamics of power-yield trade-offs to predict the emergence of microbiome function and composition. This thermodynamic theory is applicable to all living organisms, with the outcomes being generalizable beyond microbiome sciences.Co-funding for this award was provided by the Division of Materials Research.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.

在整个地球生态系统中，微生物适应并形成了跨越能量和资源丰富度梯度的群落（微生物组）。就像我们设计的机器和电路一样，功率和效率也是决定微生物群落竞争力的关键特征。在进化过程中，微生物已经优化了它们自己的分子机器，以高效率地转换可用能量，最大限度地减少了作为热量的废能损失。微生物有一系列的策略，反映了新细胞生产速度（功率）和效率（产量）之间的平衡，同时也处理了降低产量的各种生存成本。这个研究项目将测试这样一种假设，即微生物群从个体成员聚集成一个群落，在提高效率的同时也能优化能量。从蛋白质到生态系统，这种功率和效率优化的原则通常适用于不同层次的生物组织。研究人员将研究土壤和人类肠道中的微生物组，作为模型系统来验证这一想法。他们将开发一个新的实验平台，包括多个隔间来控制微生物组如何相互作用，集成纳米技术传感器来测量微生物的效率作为热量输出，加上先进的显微镜来测量微生物生长的产量。这项工作将测试存储在微生物基因组中的信息是否可以预测它们的发电量策略，以及微生物组多样性的各个方面是否可以与效率相关，从而开发一个预测建模框架。如果这一基本热力学理论能够解释从细胞到群落的生物组织模式，它将提供一个重要的新框架来预测生物将如何应对地球上未来的条件。更广泛的影响包括社区大学生参与研究，以及研究生和博士后。外联活动包括为讲故事平台制作科学视频，供公众观看。微生物，像所有生物一样，通过创造熵来维持生命的秩序。它们存在于开放的、非平衡的热力学系统中，跨越自由能的梯度，为结构（蛋白质、细胞、群落）的形成和维持提供燃料，这些结构（蛋白质、细胞、群落）增强了能量流，同时试图最小化废热的消散，从而增强了整个过程中的熵产。微生物群落的组装和演替是由能量流驱动的，它是调节产量（即效率）的最大功率和最小散热之间的权衡。这种对产生熵的权衡是一个基本的热力学原理。作为一种生物优化函数，功率和产量的优化通过自然选择与热力学和进化相一致，因为资源可用性或压力等约束条件根据其功率：产量策略在帕累托最优曲线上的位置来调节生物体的适合度。这些权衡如何在社区规模上表现出来还没有经过经验检验。本研究将通过(1)开发一种新型集成纳米量热-微流体平台来控制资源和应力梯度，同时量化开放系统中的功率、产量和熵产；(2)进行一系列操作实验，以评估微生物和微生物组的特性与功率、产量和熵产以及生物（地球）化学输出之间的关系；(3)开发基于功率产率权衡热力学的模拟工具，以预测微生物组功能和组成的出现。这种热力学理论适用于所有生物体，其结果可推广到微生物组科学之外。该奖项的共同资助由材料研究部提供。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。