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The Repertoire and Dynamics of Evolutionary Adaptations to Controlled Nutrient-Limited Environments in Yeast

Authors: Gresham D.; Desai M.M.; Tucker C.M.; Jenq H.T.; Pai D.A.; Ward A.; DeSevo C.G.; +2 Authors

The Repertoire and Dynamics of Evolutionary Adaptations to Controlled Nutrient-Limited Environments in Yeast

Abstract

The experimental evolution of laboratory populations of microbes provides an opportunity to observe the evolutionary dynamics of adaptation in real time. Until very recently, however, such studies have been limited by our inability to systematically find mutations in evolved organisms. We overcome this limitation by using a variety of DNA microarray-based techniques to characterize genetic changes -- including point mutations, structural changes, and insertion variation -- that resulted from the experimental adaptation of 24 haploid and diploid cultures of Saccharomyces cerevisiae to growth in either glucose, sulfate, or phosphate-limited chemostats for approximately 200 generations. We identified frequent genomic amplifications and rearrangements as well as novel retrotransposition events associated with adaptation. Global nucleotide variation detection in ten clonal isolates identified 32 point mutations. On the basis of mutation frequencies, we infer that these mutations and the subsequent dynamics of adaptation are determined by the batch phase of growth prior to initiation of the continuous phase in the chemostat. We relate these genotypic changes to phenotypic outcomes, namely global patterns of gene expression, and to increases in fitness by 5-50%. We found that the spectrum of available mutations in glucose- or phosphate-limited environments combined with the batch phase population dynamics early in our experiments allowed several distinct genotypic and phenotypic evolutionary pathways in response to these nutrient limitations. By contrast, sulfate-limited populations were much more constrained in both genotypic and phenotypic outcomes. Thus, the reproducibility of evolution varies with specific selective pressures, reflecting the constraints inherent in the system-level organization of metabolic processes in the cell. We were able to relate some of the observed adaptive mutations (e.g., transporter gene amplifications) to known features of the relevant metabolic pathways, but many of the mutations pointed to genes not previously associated with the relevant physiology. Thus, in addition to answering basic mechanistic questions about evolutionary mechanisms, our work suggests that experimental evolution can also shed light on the function and regulation of individual metabolic pathways.

Keywords

molecular cloning, mutation rate, gene amplification, genotype, sulfate, adaptation, QH426-470, Gene Duplication, genetic variability, genetics, glucose, Oligonucleotide Array Sequence Analysis, chemostat, Sulfates, development and aging, article, nucleotide, Adaptation, Physiological, Phenotype, point mutation, gene insertion, Research Article, haploidy, 570, Saccharomyces cerevisiae Proteins, Genotype, fungal genetics, phenotype, regulatory mechanism, Evolution, growth, Physiological, Molecular Sequence Data, 610, Saccharomyces cerevisiae, Phosphates, Evolution, Molecular, Saccharomyces cerevisiae protein, gene expression profiling, Genetics, retroposon, Selection, Genetic, reproducibility, phosphate, diploidy, nutrient limitation, nonhuman, gene deletion, molecular evolution, Gene Expression Profiling, DNA microarray, gene duplication, Molecular, fungus growth, Glucose, genetic selection, molecular genetics, physiology, Mutation, evolutionary adaptation, gene expression, mutation, metabolism, Gene Deletion

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    This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
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    This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
    Top 1%
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citations
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
402
Top 1%
Top 1%
Top 1%
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