Thermotolerant yeasts selected by adaptive evolution express heat stress response at 30 °c

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Caspeta, Luis ^a,b   Chen, Yun ^b   Nielsen, Jens ^b,c,d  

^a UNIVERSIDAD AUTÓNOMA DEL ESTADO DE MORELOS   (Mexico)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c Chalmers University of Technology   (Denmark)

^d ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TRANSCRIPTION; EXPOSURE; FUNGAL CELL CULTURE; GLOBAL CHANGE; GROWTH RATE; HEAT STRESS; HIGH TEMPERATURE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EID: 84971247513     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep27003     Document Type: Article

References (42)

1. Kültz, D. Molecular and evolutionary basis of the cellular stress response. Annu. Rev. Physiol. 67, 225-257 (2005).
2. Lopez-Maury, L., Marguerat, S. & Bahler, J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat. Rev. Genet. 10, 68-68 (2009).
3. Tagkopoulos, I., Liu, Y. C. & Tavazoie, S. Predictive behavior within microbial genetic networks. Science 320, 1313-1317 (2008).
4. Berry, D. B. & Gasch, A. P. Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol. Biol. Cell. 19, 4580-4587 (2008).
5. Gasch, A. P. et al. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell. 11, 4241-4257 (2000).
6. Postmus, J. et al. Dynamic regulation of mitochondrial respiratory chain efficiency in Saccharomyces cerevisiae. Microbiol. 157, 3500-3511 (2011).
7. Postmus, J. et al. Isoenzyme expression changes in response to high temperature determine the metabolic regulation of increased glycolytic flux in yeast. FEMS Yeast Res. 12, 571-581 (2012).
8. Postmus, J. et al. Quantitative analysis of the high temperature-induced glycolytic flux increase in Saccharomyces cerevisiae reveals dominant metabolic regulation. J. Biol. Chem. 283, 23524-23532 (2008).
9. Gasch, A. & Werner-Washburne, M. The genomics of yeast responses to environmental stress and starvation. Funct. Integr. Genom. 2, 181-192 (2002).
10. Hottiger, T., Schmutz, P. & Wiemken, A. Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae. J. Bacteriol. 169, 5518-5522 (1987).
11. Yost, H. J. & Lindquist, S. Heat shock proteins affect RNA processing during the heat shock response of Saccharomyces cerevisiae. Mol. Cell. Biol. 11, 1062-1068 (1991).
12. Piper, P. W., Ortiz-Calderon, C., Holyoak, C., Coote, P. & Cole, M. Hsp30, the integral plasma membrane heat shock protein of Saccharomyces cerevisiae, is a stress-inducible regulator of plasma membrane H+-ATPase. Cell Stress Chaperones 2, 12-24 (1997).
13. Hottiger, T., Boller, T. & Wiemken, A. Correlation of trenalose content and heat resistance in yeast mutants altered in the RAS/adenylate cyclase pathway: is trehalose a thermoprotectant? FEBS Let. 255, 431-434 (1989).
14. Piper, P. W. Molecular events associated with acquisition of heat tolerance by the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 11, 339-355 (1993).
15. Caspeta, L. & Nielsen, J. Thermotolerant yeast strains adapted by laboratory evolution show trade-off at ancestral temperatures and preadaptation to other stresses. mBio 6(4), doi: 10.1128/mBio.00431-15 (2015).
16. Carmona-Gutierrez, D. et al. Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ. 17, 763-773 (2010).
17. Lindquist, S. The heat-shock response. Annu. Rev. Biochem. 55, 1151-1191 (1986).
18. Caspeta, L. et al. Altered sterol composition renders yeast thermotolerant. Science 346, 75-78 (2014).
19. Lingwood, D. & Simons, K. Lipid rafts as a membrane-organizing principle. Science 327, 46-50 (2010).
20. Dufourc, E. Sterols and membrane dynamics. J. Chem. Biol. 1, 63-77 (2008).
21. Vigh, L., Maresca, B. & Harwood, J. L. Does the membrane's physical state control the expression of heat shock and other genes? Trends. Biochem. Sci. 23, 369-374 (1998).
22. Vigh, L., Los, D. A., Horváth, I. & Murata, N. The primary signal in the biological perception of temperature: Pd-catalyzed hydrogenation of membrane lipids stimulated the expression of the desA gene in Synechocystis PCC6803. Proc. Natl. Acad. Sci. USA 90, 9090-9094 (1993).
23. Horváth, I. et al. Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: Identification of hsp17 as a "fluidity gene". Proc. Natl. Acad. Sci. USA 95, 3513-3518 (1998).
24. Carratù, L. et al. Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc. Natl. Acad. Sci. USA 93, 3870-3875 (1996).
25. Chatterjee, M. T., Khalawan, S. A. & Curran, B. P. G. Cellular lipid composition influences stress activation of the yeast general stress response element (STRE). Microbiology 146, 877-884 (2000).
26. Jenkins, G. M. et al. Involvement of yeast sphingolipids in the heat stress response of Saccharomyces cerevisiae. J. Biol. Chem. 272, 32566-32572 (1997).
27. Meyer, P. et al. Structural basis for recruitment of the ATPase activator Aha1 to the Hsp90 chaperone machinery. EMBO J. 23, 511-519 (2004).
28. Lotz, G. P., Lin, H., Harst, A. & Obermann, W. M. J. Aha1 binds to the middle domain of Hsp90, contributes to client protein activation, and stimulates the ATPase activity of the molecular chaperone. J. Biol. Chem. 278, 17228-17235 (2003).
29. Rigoulet, M. et al. Organization and regulation of the cytosolic NADH metabolism in the yeast Saccharomyces cerevisiae. Mol. Cell Biochem. 256-257, 73-81 (2004).
30. Overkamp, K. M. et al. In vivo analysis of the mechanisms for oxidation of cytosolic NADH by Saccharomyces cerevisiae mitochondria. J. Bacteriol. 182, 2823-2830 (2000).
31. Horng, Y. C., Cobine, P. A., Maxfield, A. B., Carr, H. S. & Winge, D. R. Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J. Biol. Chem. 279, 35334-35340 (2004).
32. Bolesm, E., Göhlmann, H. W. H. & Zimmermann, F. K. Cloning of a second gene encoding 6-phosphofructo-2-kinase in yeast, and characterization of mutant strains without fructose-2,6-bisphosphate. Mol. Microbiol. 20, 65-76 (1996).
33. Heinisch, J. J., Boles, E. & Timpel, C. A yeast phosphofructokinase insensitive to the allosteric activator fructose 2,6-Bisphosphate: Glycolysis/metabolic regulation/allosteric control. J. Biol. Chem. 271, 15928-15933 (1996).
34. Gibney, P. A., Lu, C., Caudy, A. A., Hess, D. C. & Botstein, D. Yeast metabolic and signaling genes are required for heat-shock survival and have little overlap with the heat-induced genes. Proc. Natl. Acad. Sci. USA 110, 4393-4402 (2013).
35. Yi, T. M., Huang, Y., Simon, M. I. & Doyle, J. Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc. Natl. Acad. Sci. USA 97, 4649-4653 (2000).
36. Mitchell, A. et al. Adaptive prediction of environmental changes by microorganisms. Nature 460, 220-224 (2009).
37. Gentleman, R. C. et al. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
38. Affymetrix Technical report, Guide to probe logarithmic intensity error (plier) estimation (Affymetrix, Inc.; Santa Clara, CA, 2005).
39. Benjamini, Y. H. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Statist. Soc. B 57, 289-300 (1995).
40. Väremo, L., Nielsen, J. & Nookaew, I. Enriching the gene set analysis of genome-wide data by incorporating directionality of gene expression and combining statistical hypotheses and methods. Nucleic Acids Res. 41, 4378-4391 (2013).
41. Agren, R. et al. The RAVEN toolbox and its use for generating a genome-scale metabolic model for Penicillium chrysogenum. PLOS Comput. Biol. 9, e1002980 (2013).
42. Bordel, S., Agren, R. & Nielsen, J. Sampling the solution space in genome-scale metabolic networks reveals transcriptional regulation in key enzymes. PLOS Comput. Biol. 6, e1000859 (2010).