The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris
Abstract Background The effects of long-term environmental adaptation and the implications of major cellular malfunctions are still poorly understood for non-model but biotechnologically relevant species. In this study we performed a large-scale laboratory evolution experiment with 48 populations of...
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| Format: | Article |
| Language: | English |
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BMC
2017-08-01
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| Series: | BMC Genomics |
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| Online Access: | http://link.springer.com/article/10.1186/s12864-017-3952-7 |
| _version_ | 1828786020542316544 |
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| author | Josef W. Moser Iain B. H. Wilson Martin Dragosits |
| author_facet | Josef W. Moser Iain B. H. Wilson Martin Dragosits |
| author_sort | Josef W. Moser |
| collection | DOAJ |
| description | Abstract Background The effects of long-term environmental adaptation and the implications of major cellular malfunctions are still poorly understood for non-model but biotechnologically relevant species. In this study we performed a large-scale laboratory evolution experiment with 48 populations of the yeast Pichia pastoris in order to establish a general adaptive landscape upon long-term selection in several glucose-based growth environments. As a model for a cellular malfunction the implications of OCH1 mannosyltransferase knockout-mediated glycosylation-deficiency were analyzed. Results In-depth growth profiling of evolved populations revealed several instances of genotype-dependent growth trade-off/cross-benefit correlations in non-evolutionary growth conditions. On the genome level a high degree of mutational convergence was observed among independent populations. Environment-dependent mutational hotspots were related to osmotic stress-, Rim - and cAMP signaling pathways. In agreement with the observed growth phenotypes, our data also suggest diverging compensatory mutations in glycosylation-deficient populations. High osmolarity glycerol (HOG) pathway loss-of-functions mutations, including genes such as SSK2 and SSK4, represented a major adaptive strategy during environmental adaptation. However, genotype-specific HOG-related mutations were predominantly observed in opposing environmental conditions. Surprisingly, such mutations emerged during salt stress adaptation in OCH1 knockout populations and led to growth trade-offs in non-adaptive conditions that were distinct from wildtype HOG-mutants. Further environment-dependent mutations were identified for a hitherto uncharacterized species-specific Gal4-like transcriptional regulator involved in environmental sensing. Conclusion We show that metabolic constraints such as glycosylation-deficiency can contribute to evolution on the molecular level, even in non-diverging growth environments. Our dataset suggests universal adaptive mechanisms involving cellular stress response and cAMP/PKA signaling but also the existence of highly species-specific strategies involving unique transcriptional regulators, improving our biological understanding of distinct Ascomycetes species. |
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| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-12-12T00:04:22Z |
| publishDate | 2017-08-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-b2cfb222d7f3484498af097810a2d40e2022-12-22T00:45:10ZengBMCBMC Genomics1471-21642017-08-0118111610.1186/s12864-017-3952-7The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastorisJosef W. Moser0Iain B. H. Wilson1Martin Dragosits2Department of Chemistry, University of Natural Resources and Life SciencesDepartment of Chemistry, University of Natural Resources and Life SciencesDepartment of Chemistry, University of Natural Resources and Life SciencesAbstract Background The effects of long-term environmental adaptation and the implications of major cellular malfunctions are still poorly understood for non-model but biotechnologically relevant species. In this study we performed a large-scale laboratory evolution experiment with 48 populations of the yeast Pichia pastoris in order to establish a general adaptive landscape upon long-term selection in several glucose-based growth environments. As a model for a cellular malfunction the implications of OCH1 mannosyltransferase knockout-mediated glycosylation-deficiency were analyzed. Results In-depth growth profiling of evolved populations revealed several instances of genotype-dependent growth trade-off/cross-benefit correlations in non-evolutionary growth conditions. On the genome level a high degree of mutational convergence was observed among independent populations. Environment-dependent mutational hotspots were related to osmotic stress-, Rim - and cAMP signaling pathways. In agreement with the observed growth phenotypes, our data also suggest diverging compensatory mutations in glycosylation-deficient populations. High osmolarity glycerol (HOG) pathway loss-of-functions mutations, including genes such as SSK2 and SSK4, represented a major adaptive strategy during environmental adaptation. However, genotype-specific HOG-related mutations were predominantly observed in opposing environmental conditions. Surprisingly, such mutations emerged during salt stress adaptation in OCH1 knockout populations and led to growth trade-offs in non-adaptive conditions that were distinct from wildtype HOG-mutants. Further environment-dependent mutations were identified for a hitherto uncharacterized species-specific Gal4-like transcriptional regulator involved in environmental sensing. Conclusion We show that metabolic constraints such as glycosylation-deficiency can contribute to evolution on the molecular level, even in non-diverging growth environments. Our dataset suggests universal adaptive mechanisms involving cellular stress response and cAMP/PKA signaling but also the existence of highly species-specific strategies involving unique transcriptional regulators, improving our biological understanding of distinct Ascomycetes species.http://link.springer.com/article/10.1186/s12864-017-3952-7Pichia PastorisExperimental evolutionGlucoseSalt stressOCH1 |
| spellingShingle | Josef W. Moser Iain B. H. Wilson Martin Dragosits The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris BMC Genomics Pichia Pastoris Experimental evolution Glucose Salt stress OCH1 |
| title | The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris |
| title_full | The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris |
| title_fullStr | The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris |
| title_full_unstemmed | The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris |
| title_short | The adaptive landscape of wildtype and glycosylation-deficient populations of the industrial yeast Pichia pastoris |
| title_sort | adaptive landscape of wildtype and glycosylation deficient populations of the industrial yeast pichia pastoris |
| topic | Pichia Pastoris Experimental evolution Glucose Salt stress OCH1 |
| url | http://link.springer.com/article/10.1186/s12864-017-3952-7 |
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