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Nutrient colimitation is a quantitative, dynamic property of microbial populations
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.4 ) Pub Date : 2024-12-18 , DOI: 10.1073/pnas.2400304121 Noelle A. Held, Aswin Krishna, Donat Crippa, Rachana Rao Battaje, Alexander J. Devaux, Anastasia Dragan, Michael Manhart
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.4 ) Pub Date : 2024-12-18 , DOI: 10.1073/pnas.2400304121 Noelle A. Held, Aswin Krishna, Donat Crippa, Rachana Rao Battaje, Alexander J. Devaux, Anastasia Dragan, Michael Manhart
Resource availability dictates how fast and how much microbial populations grow. Quantifying the relationship between microbial growth and resource concentrations makes it possible to promote, inhibit, and predict microbial activity. Microbes require many resources, including macronutrients (e.g., carbon and nitrogen), micronutrients (e.g., metals), and complex nutrients like vitamins and amino acids. When multiple resources are scarce, as frequently occurs in nature, microbes may experience resource colimitation in which more than one resource simultaneously limits growth. Despite growing evidence for colimitation, the data are difficult to interpret and compare due to a lack of quantitative measures of colimitation and systematic tests of resource conditions. We hypothesize that microbes experience a continuum of nutrient limitation states and that nutrient colimitation is common in the laboratory and in nature. To address this, we develop a quantitative theory of resource colimitation that captures the range of possible limitation states and describes how they can change dynamically with resource conditions. We apply this approach to clonal populations of Escherichia coli to show that colimitation occurs in common laboratory conditions. We also show that growth rate and growth yield are colimited differently, reflecting the different underlying biology of these traits. Finally, we analyze environmental data to provide intuition for the continuum of limitation and colimitation conditions in nature. Altogether our results provide a quantitative framework for understanding and quantifying colimitation of microbes in biogeochemical, biotechnology, and human health contexts.
中文翻译:
营养共限是微生物种群的一种定量、动态特性
资源可用性决定了微生物种群的增长速度和数量。量化微生物生长与资源浓度之间的关系可以促进、抑制和预测微生物活动。微生物需要许多资源,包括常量营养素(例如碳和氮)、微量营养素(例如金属)以及维生素和氨基酸等复合营养素。当多种资源稀缺时,就像自然界中经常发生的那样,微生物可能会经历资源协同限制,其中不止一种资源同时限制生长。尽管共限度的证据越来越多,但由于缺乏共限度的定量测量和资源条件的系统测试,这些数据难以解释和比较。我们假设微生物会经历一系列营养限制状态,并且营养共限制在实验室和自然界中很常见。为了解决这个问题,我们开发了一种资源共限的定量理论,该理论捕获了可能的限制状态的范围,并描述了它们如何随资源条件动态变化。我们将这种方法应用于大肠杆菌的克隆种群,以表明共限制发生在常见的实验室条件下。我们还表明,生长速率和生长产量的共限度不同,反映了这些性状的不同潜在生物学。最后,我们分析环境数据,为自然界中的限制和共限制条件的连续体提供直觉。总而言之,我们的结果为理解和量化生物地球化学、生物技术和人类健康背景下微生物的共限度提供了一个定量框架。
更新日期:2024-12-18
中文翻译:
营养共限是微生物种群的一种定量、动态特性
资源可用性决定了微生物种群的增长速度和数量。量化微生物生长与资源浓度之间的关系可以促进、抑制和预测微生物活动。微生物需要许多资源,包括常量营养素(例如碳和氮)、微量营养素(例如金属)以及维生素和氨基酸等复合营养素。当多种资源稀缺时,就像自然界中经常发生的那样,微生物可能会经历资源协同限制,其中不止一种资源同时限制生长。尽管共限度的证据越来越多,但由于缺乏共限度的定量测量和资源条件的系统测试,这些数据难以解释和比较。我们假设微生物会经历一系列营养限制状态,并且营养共限制在实验室和自然界中很常见。为了解决这个问题,我们开发了一种资源共限的定量理论,该理论捕获了可能的限制状态的范围,并描述了它们如何随资源条件动态变化。我们将这种方法应用于大肠杆菌的克隆种群,以表明共限制发生在常见的实验室条件下。我们还表明,生长速率和生长产量的共限度不同,反映了这些性状的不同潜在生物学。最后,我们分析环境数据,为自然界中的限制和共限制条件的连续体提供直觉。总而言之,我们的结果为理解和量化生物地球化学、生物技术和人类健康背景下微生物的共限度提供了一个定量框架。