Abstract
Adaptation under similar selective pressure often leads to comparable phenotypes. A longstanding question is whether such phenotypic repeatability entails similar (parallelism) or different genotypic changes (convergence). To better understand this, we characterized mutations that optimized expression of a plasmid-borne metabolic pathway during laboratory evolution of a bacterium. Expressing these pathway genes was essential for growth but came with substantial costs. Starting from overexpression, replicate populations founded by this bacterium all evolved to reduce expression. Despite this phenotypic repetitiveness, the underlying mutational spectrum was highly diverse. Analysis of these plasmid mutations identified three distinct means to modulate gene expression: (1) reducing the gene copy number, (2) lowering transcript stability, and (3) integration of the pathway-bearing plasmid into the host genome. Our study revealed diverse molecular changes beneath convergence to a simple phenotype. This complex genotype-phenotype mapping presents a challenge to inferring genetic evolution based solely on phenotypic changes.
Highlights
Gene expression is the fundamental process through which proteins and RNAs are synthesized to sustain, protect, and replicate biological systems
The lack of mechanistic mapping between genotypes and phenotypes in many similar studies renders a longstanding question unaddressed: How repeatable is evolution at genotypic versus phenotypic levels (Stern, 2011)?. We explored this question by examining the mechanism of gene expression optimization during adaptation of an engineered strain of Methylobacterium extorquens AM1 (EM) (Chou et al, 2011)
The results revealed the prevalence of particular types of mutational events, such as integration of pCM410 into the host genome, which occurred across many replicate populations despite smaller selective advantages
Summary
Gene expression is the fundamental process through which proteins and RNAs are synthesized to sustain, protect, and replicate biological systems. Controlling gene expression is crucial as expressing a gene at the incorrect level or under the wrong conditions can compromise its innate function and may disturb other physiological processes. This could result in a fitness disadvantage or even lethality (Brand and Perrimon, 1993; Saint-Dic et al, 2008). Natural selection should operate strongly on gene expression to optimize its phenotypic outcomes (Monod and Jacob, 1961) This supposition has gained increasing support from recent transcriptome analyses comparing closely related species and genetic analyses that give insight into morphological evolution
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