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- Title
Paths to adaptation under fluctuating nitrogen starvation: The spectrum of adaptive mutations in Saccharomyces cerevisiae is shaped by retrotransposons and microhomology-mediated recombination.
- Authors
Hays, Michelle; Schwartz, Katja; Schmidtke, Danica T.; Aggeli, Dimitra; Sherlock, Gavin
- Abstract
There are many mechanisms that give rise to genomic change: while point mutations are often emphasized in genomic analyses, evolution acts upon many other types of genetic changes that can result in less subtle perturbations. Changes in chromosome structure, DNA copy number, and novel transposon insertions all create large genomic changes, which can have correspondingly large impacts on phenotypes and fitness. In this study we investigate the spectrum of adaptive mutations that arise in a population under consistently fluctuating nitrogen conditions. We specifically contrast these adaptive alleles and the mutational mechanisms that create them, with mechanisms of adaptation under batch glucose limitation and constant selection in low, non-fluctuating nitrogen conditions to address if and how selection dynamics influence the molecular mechanisms of evolutionary adaptation. We observe that retrotransposon activity accounts for a substantial number of adaptive events, along with microhomology-mediated mechanisms of insertion, deletion, and gene conversion. In addition to loss of function alleles, which are often exploited in genetic screens, we identify putative gain of function alleles and alleles acting through as-of-yet unclear mechanisms. Taken together, our findings emphasize that how selection (fluctuating vs. non-fluctuating) is applied also shapes adaptation, just as the selective pressure (nitrogen vs. glucose) does itself. Fluctuating environments can activate different mutational mechanisms, shaping adaptive events accordingly. Experimental evolution, which allows a wider array of adaptive events to be assessed, is thus a complementary approach to both classical genetic screens and natural variation studies to characterize the genotype-to-phenotype-to-fitness map. Author summary: A major driver of evolution is the occurrence and subsequent selection of adaptive mutations, which make an organism more fit in a given environment. While adaptive mutations are often point mutations, such as missense or nonsense mutations, there are many other types of mutation. Here we find that retrotransposition events, whereby a retrotransposon makes a new copy of itself elsewhere in the genome, are frequent when yeast are propagated by serial batch transfer in media with limiting nitrogen. Furthermore, we find many such events are adaptive, and show that the rate of retrotransposition is increased in nitrogen limited media compared to glucose limited media specifically when cells are propagated by serial batch transfer. However, we see no evidence of beneficial retrotransposition events when cells are propagated in nitrogen limited media in continuous culture. Our findings emphasize that how selection (fluctuating vs. non-fluctuating) is applied also shapes adaptation, just as the selective pressure (nitrogen vs. glucose) does itself.
- Subjects
GENE conversion; SACCHAROMYCES cerevisiae; RETROTRANSPOSONS; GENETIC testing; NONSENSE mutation
- Publication
PLoS Genetics, 2023, Vol 19, Issue 5, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010747