Prolonged Maltose-Limited Cultivation of Saccharomyces cerevisiae Selects for Cells with Improved Maltose Affinity and Hypersensitivity
Open accessAbstract
Prolonged cultivation (>25 generations) of Saccharomyces cerevisiae in aerobic, maltose-limited chemostat cultures led to profound physiological changes. Maltose hypersensitivity was observed when cells from prolonged cultivations were suddenly exposed to excess maltose. This substrate hypersensitivity was evident from massive cell lysis and loss of viability. During prolonged cultivation at a fixed specific growth rate, the affinity for the growth-limiting nutrient (i.e., maltose) increased, as evident from a decreasing residual maltose concentration. Furthermore, the capacity of maltose-dependent proton uptake increased up to 2.5-fold during prolonged cultivation. Genome-wide transcriptome analysis showed that the increased maltose transport capacity was not primarily due to increased transcript levels of maltose-permease genes upon prolonged cultivation. We propose that selection for improved substrate affinity (ratio of maximum substrate consumption rate and substrate saturation constant) in maltose-limited cultures leads to selection for cells with an increased capacity for maltose uptake. At the same time, the accumulative nature of maltose-proton symport in S. cerevisiae leads to unrestricted uptake when maltose-adapted cells are exposed to a substrate excess. These changes were retained after isolation of individual cell lines from the chemostat cultures and nonselective cultivation, indicating that mutations were involved. The observed trade-off between substrate affinity and substrate tolerance may be relevant for metabolic engineering and strain selection for utilization of substrates that are taken up by proton symport.
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Self-citation
- Authors
- Jansen, M. L. A., Daran-Lapujade, P., de Winde, J. H., Piper, M. D. W., & Pronk, J. T.
- Affiliations
- Delft University of Technology (NL)
- Department of Biotechnology, Delft University of Technology, 2628 BC Delft
- University College London (GB)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2004-04
- Volume
- 70
- Issue
- 4
- Pages
- 1956-1963
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC383169
- OpenAlex
- W2118625346
- Cited by
- 62
- References
- 71
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 3 · 2019: 4 · 2018: 4 · 2017: 2 · 2016: 2 · 2013: 2 · 2012: 1
- FWCI
- 1.42
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Repository (Delft University of Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Saccharomyces cerevisiae, maltose, substrate affinity, maltose uptake, maltose permease, chemostat cultivation, long-term selection, cell lysis, genome-wide transcriptome, metabolic engineering, strain selection, substrate tolerance
- MeSH terms
- alpha-Glucosidases, Biological Transport, Active, Culture Media, Genes, Fungal, Hydrogen-Ion Concentration, Kinetics, Maltose, Monosaccharide Transport Proteins, Mutation, Phenotype, Saccharomyces cerevisiae, Transcription, Genetic, Membrane Transport Proteins
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