Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation.

Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation.
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快速生长增加了在金属限制下进化过程中反复出现的突变的选择优势。

DOI:
10.1371/journal.pgen.1000652
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发表时间:
2009-09
期刊:
影响因子:
4.5
通讯作者:
Marx, Christopher J.
Marx, Christopher J.
中科院分区:
生物学2区
文献类型:
--
作者:
Chou, Hsin-Hung;Berthet, Julia;Marx, Christopher J.

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了解生物系统的进化需要理清将遗传和环境变化与其生理后果联系起来的分子机制。从人体内的病原体到海洋中的浮游植物,许多环境中的金属限制对改进金属采集系统提出了强有力的选择。在这项研究中,我们利用在缺乏金属的生长培养基中进化的扭动甲基杆菌 AM1 实验群体,揭示了适应金属限制的遗传和生理基础。我们在 32 个使用甲醇作为碳源的独立群体中的 30 个中发现了反复出现的转座突变,但在仅使用琥珀酸的 8 个群体中没有发现。这些平行插入事件增加了新型转运系统的表达,从而增强了钴的吸收。这种能力确保了维生素 B12(一种含钴辅助因子)的产生,以维持两种维生素 B12 依赖性酶促反应,这些反应对甲醇(但不是琥珀酸)代谢至关重要。有趣的是,这种突变在允许更快生长的遗传背景或孵化温度下提供了更高的选择优势,表明生长速率依赖的上位性和基因型与环境的相互作用。我们的结果将金属限制环境中出现的有益突变与其碳代谢的生理基础联系起来,表明某些分子特征可能促进平行突变的出现,并表明某些突变的选择性优势一般取决于生长速率的变化,而生长速率的变化可能源于遗传或环境影响。突变的影响可能会在不同的遗传背景或环境因素下发生变化,也分别称为上位性和基因型与环境的相互作用(G×E)。尽管上位性和 G×E 传统上被视为不同的现象,但我们对有益突变的研究强调了它们的共性。这种突变是由于在金属限制介质中进化过程中,在 32 个独立种群中的 30 个种群中,在新型钴转运系统上游插入了相同的转座元件而导致的。由此产生的钴吸收增加提供了选择性益处,该益处取决于两个环境因素:钴限制和生长底物,其代谢需要特定的维生素 B12(含有钴)依赖性生化途径。此外,这种突变以通用方式表现出上位性和 G×E 与其他细胞过程的相互作用,因此随着细胞能够更快地生长,其选择性优势也会增加。这种生长速率依赖性符合一个简单的模型:生长所需的多种生理过程中最慢的一个对生物体的生长速率发挥最大的控制作用。这表明,由于生长是整个生理系统性能的结果,因此影响不同生理过程的基因或环境因素可能通过它们对生长表型的聚合效应相互作用。
Understanding the evolution of biological systems requires untangling the molecular mechanisms that connect genetic and environmental variations to their physiological consequences. Metal limitation across many environments, ranging from pathogens in the human body to phytoplankton in the oceans, imposes strong selection for improved metal acquisition systems. In this study, we uncovered the genetic and physiological basis of adaptation to metal limitation using experimental populations of Methylobacterium extorquens AM1 evolved in metal-deficient growth media. We identified a transposition mutation arising recurrently in 30 of 32 independent populations that utilized methanol as a carbon source, but not in any of the 8 that utilized only succinate. These parallel insertion events increased expression of a novel transporter system that enhanced cobalt uptake. Such ability ensured the production of vitamin B12, a cobalt-containing cofactor, to sustain two vitamin B12–dependent enzymatic reactions essential to methanol, but not succinate, metabolism. Interestingly, this mutation provided higher selective advantages under genetic backgrounds or incubation temperatures that permit faster growth, indicating growth-rate–dependent epistatic and genotype-by-environment interactions. Our results link beneficial mutations emerging in a metal-limiting environment to their physiological basis in carbon metabolism, suggest that certain molecular features may promote the emergence of parallel mutations, and indicate that the selective advantages of some mutations depend generically upon changes in growth rate that can stem from either genetic or environmental influences. Effects of mutations can change under different genetic backgrounds or environmental factors, also known as epistasis and genotype-by-environment interactions (G×E), respectively. Though epistasis and G×E are traditionally treated as distinct phenomena, our study of a beneficial mutation highlights their commonality. This mutation resulted from insertion of the same transposable element upstream of a novel cobalt transport system in 30 of 32 independent populations during evolution in metal-limited media. The resulting increased cobalt uptake provided a selective benefit that depended upon two environmental factors: cobalt limitation and growth substrates whose metabolism requires a particular vitamin B12 (which contains cobalt) -dependent biochemical pathway. Furthermore, this mutation exhibited epistatic and G×E interactions with other cellular processes in a generic way, such that its selective advantage increased as cells were able to grow faster. This growth-rate dependence accords with a simple model: the slowest of multiple physiological processes needed for growth exerts the greatest control over an organism's growth rate. It suggests that as growth results from the performance of the entire physiological system, genes or environmental factors that affect distinct physiological processes may thus interact through their convergent effects on growth phenotypes.
DOI: 10.1371/journal.pgen.0040002
发表时间: 2008-01-01
期刊: PLOS GENETICS
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