Long-Term Adaptation to Galactose as a Sole Carbon Source Selects for Mutations Outside the Canonical GAL Pathway

Galactose is a secondary fermentable sugar that requires specific regulatory and structural genes for its assimilation, which are under catabolite repression by glucose. When glucose is absent, the catabolic repression is attenuated, and the structural GAL genes are fully activated. In Saccharomyces...

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Bibliographic Details
Published in:Journal of molecular evolution 2023-02, Vol.91 (1), p.46-59
Main Authors: Martínez, Artemiza A., Conboy, Andrew, Buskirk, Sean W., Marad, Daniel A., Lang, Gregory I.
Format: Article
Language:English
Subjects:
Adaptation
Animal Genetics and Genomics
Biomedical and Life Sciences
Carbon
Carbon - metabolism
Carbon sources
Catabolite repression
Cell Biology
Chromosome 8
Copy number
Diploids
DNA Copy Number Variations
Evolution
Evolutionary Biology
Fitness
Fungi
Galactose
Galactose - metabolism
Gene sequencing
Genes
Genomes
Glucose
Glucose - metabolism
Life Sciences
Microbiology
Mutation
Nucleotides
Original
Original Article
Plant Genetics and Genomics
Plant Sciences
Ploidy
Population studies
Populations
Reproductive fitness
Saccharomyces cerevisiae
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - metabolism
Whole genome sequencing
Yeast
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Summary:Galactose is a secondary fermentable sugar that requires specific regulatory and structural genes for its assimilation, which are under catabolite repression by glucose. When glucose is absent, the catabolic repression is attenuated, and the structural GAL genes are fully activated. In Saccharomyces cerevisiae , the GAL pathway is under selection in environments where galactose is present. However, it is unclear the adaptive strategies in response to long-term propagation in galactose as a sole carbon source in laboratory evolution experiments. Here, we performed a 4,000-generation evolution experiment using 48 diploid Saccharomyces cerevisiae populations to study adaptation in galactose. We show that fitness gains were greater in the galactose-evolved population than in identically evolved populations with glucose as a sole carbon source. Whole-genome sequencing of 96 evolved clones revealed recurrent de novo single nucleotide mutations in candidate targets of selection, copy number variations, and ploidy changes. We find that most mutations that improve fitness in galactose lie outside of the canonical GAL pathway. Reconstruction of specific evolved alleles in candidate target of selection, SEC23 and IRA1 , showed a significant increase in fitness in galactose compared to glucose. In addition, most of our evolved populations (28/46; 61%) fixed aneuploidies on Chromosome VIII, suggesting a parallel adaptive amplification. Finally, we show greater loss of extrachromosomal elements in our glucose-evolved lineages compared with previous glucose evolution. Broadly, these data further our understanding of the evolutionary pressures that drive adaptation to less-preferred carbon sources.
ISSN:0022-2844
1432-1432
DOI:10.1007/s00239-022-10079-9