DOI QR코드

DOI QR Code

Advanced Technologies and Mechanisms for Yeast Evolutionary Engineering

  • Ryu, Hong-Yeoul (School of Life Sciences, BK21 Plus KNU Creative BioResearch Group, College of National Sciences, Kyungpook National University)
  • Received : 2020.09.07
  • Accepted : 2020.10.11
  • Published : 2020.12.28

Abstract

In vitro evolution is a powerful technique for the engineering of yeast strains to study cellular mechanisms associated with evolutionary adaptation; strains with desirable traits for industrial processes can also be generated. There are two distinct approaches to generate evolved strains in vitro: the sequential transfer of cells in the stationary phase into fresh medium or the continuous growth of cells in a chemostat bioreactor via the constant supply of fresh medium. In culture, evolutionary forces drive diverse adaptive mechanisms within the cell to overcome environmental or intracellular stressors. Especially, this engineering strategy has expanded to the field of human cell lines; the understanding of such adaptive mechanisms provides promising targets for the treatment of human genetic diseases and cancer. Therefore, this technology has the potential to generate numerous industrial, medical, and academic applications.

Keywords

References

  1. Borodina I, Nielsen J. 2014. Advances in metabolic engineering of yeast Saccharomyces cerevisiae for production of chemicals. Biotechnol. J. 9: 609-620. https://doi.org/10.1002/biot.201300445
  2. Padkina MV, Sambuk EV. 2018. Prospects for the application of yeast display in biotechnology and cell biology (Review). Appl. Biochem. Microbiol. 54: 337-351. https://doi.org/10.1134/S0003683818040105
  3. Mans R, Daran JMG, Pronk JT. 2018. Under pressure: evolutionary engineering of yeast strains for improved performance in fuels and chemicals production. Curr. Opin. Biotechnol. 50: 47-56. https://doi.org/10.1016/j.copbio.2017.10.011
  4. Portnoy VA, Bezdan D, Zengler K. 2011. Adaptive laboratory evolution - harnessing the power of biology for metabolic engineering. Curr. Opin. Biotechnol. 22: 590-594. https://doi.org/10.1016/j.copbio.2011.03.007
  5. Fulda S, Gorman AM, Hori O, Samali A. 2010. Cellular stress responses: cell survival and cell death. Int. J. Cell Biol. 2010: 214074. https://doi.org/10.1155/2010/214074
  6. Ryu HY, Ahn SH, Hochstrasser M. 2020. SUMO and cellular adaptive mechanisms. Exp. Mol. Med. 52: 931-939. https://doi.org/10.1038/s12276-020-0457-2
  7. Dragosits M, Mattanovich D. 2013. Adaptive laboratory evolution - principles and applications for biotechnology. Microb. Cell Fact. 12: 64. https://doi.org/10.1186/1475-2859-12-64
  8. Lang GI, Botstein D, Desai MM. 2011. Genetic variation and the fate of beneficial mutations in asexual populations. Genetics 188: 647-661. https://doi.org/10.1534/genetics.111.128942
  9. Gonzalez A, Bell G. 2013. Evolutionary rescue and adaptation to abrupt environmental change depends upon the history of stress. Philos Trans. R Soc. Lond B Biol. Sci. 368: 20120079. https://doi.org/10.1098/rstb.2012.0079
  10. Sonderegger M, Sauer U. 2003. Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl. Environ. Microbiol. 69: 1990-1998. https://doi.org/10.1128/AEM.69.4.1990-1998.2003
  11. Kuyper M, Toirkens MJ, Diderich JA, Winkler AA, van Dijken JP, Pronk JT. 2005. Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain. FEMS Yeast Res. 5: 925-934. https://doi.org/10.1016/j.femsyr.2005.04.004
  12. Wisselink HW, Toirkens MJ, Wu Q, Pronk JT, van Maris AJA. 2009. Novel Evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl. Environ. Microbiol. 75: 907-914. https://doi.org/10.1128/AEM.02268-08
  13. Daran-Lapujade P, Daran JM, van Maris AJA, de Winde JH, Pronk JT. 2009. Chemostat-based micro-array analysis in baker's yeast. Adv. Microb. Physiol. 54: 257-311. https://doi.org/10.1016/S0065-2911(08)00004-0
  14. Novick A, Szilard L. 1950. Description of the chemostat. Science 112: 715-716. https://doi.org/10.1126/science.112.2920.715
  15. Selmecki AM, Maruvka YE, Richmond PA, Guillet M, Shoresh N, Sorenson AL, et al. 2015. Polyploidy can drive rapid adaptation in yeast. Nature 519: 349-352. https://doi.org/10.1038/nature14187
  16. Yona AH, Manor YS, Herbst RH, Romano GH, Mitchell A, Kupiec M, et al. 2012. Chromosomal duplication is a transient evolutionary solution to stress. Proc. Natl. Acad. Sci. USA 109: 21010-21015. https://doi.org/10.1073/pnas.1211150109
  17. Serero A, Jubin C, Loeillet S, Legoix-Ne P, Nicolas AG. 2014. Mutational landscape of yeast mutator strains. Proc. Natl. Acad. Sci. USA 111: 1897-1902. https://doi.org/10.1073/pnas.1314423111
  18. Solis-Escalante D, van den Broek M, Kuijpers NGA, Pronk JT, Boles E, Daran JM, et al. 2015. The genome sequence of the popular hexose-transport-deficient Saccharomyces cerevisiae strain EBY.VW4000 reveals LoxP/Cre-induced translocations and gene loss. FEMS Yeast Res. 15: fou004.
  19. Shen Y, Stracquadanio G, Wang Y, Yang K, Mitchell LA, Xue YX, et al. 2016. SCRaMbLE generates designed combinatorial stochastic diversity in synthetic chromosomes. Genome Res. 26: 36-49. https://doi.org/10.1101/gr.193433.115
  20. Finney-Manchester SP, Maheshri N. 2013. Harnessing mutagenic homologous recombination for targeted mutagenesis in vivo by TaGTEAM. Nucleic Acids Res. 41: e99. https://doi.org/10.1093/nar/gkt150
  21. Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M, Tabata M, et al. 2016. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science 353: aaf8729. https://doi.org/10.1126/science.aaf8729
  22. Attfield PV. 1997. Stress tolerance: The key to effective strains of industrial baker's yeast. Nat. Biotechnol. 15: 1351-1357. https://doi.org/10.1038/nbt1297-1351
  23. Randez-Gil F, Sanz P, Prieto JA. 1999. Engineering baker's yeast: room for improvement. Trends Biotechnol. 17: 237-244. https://doi.org/10.1016/S0167-7799(99)01318-9
  24. Schulze U, Liden G, Nielsen J, Villadsen J. 1996. Physiological effects of nitrogen starvation in an anaerobic batch culture of Saccharomyces cerevisiae. Microbiology 142: 2299-2310. https://doi.org/10.1099/13500872-142-8-2299
  25. Sillje HHW, Paalman JWG, ter Schure EG, Olsthoorn SQB, Verkleij AJ, Boonstra J, et al. 1999. Function of trehalose and glycogen in cell cycle progression and cell viability in Saccharomyces cerevisiae. J. Bacteriol. 181: 396-400. https://doi.org/10.1128/jb.181.2.396-400.1999
  26. Mager WH, Ferreira PM. 1993. Stress response of yeast. Biochem. J. 290: 1-13. https://doi.org/10.1042/bj2900001
  27. Singer MA, Lindquist S. 1998. Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose. Trends Biotechnol. 16: 460-468. https://doi.org/10.1016/S0167-7799(98)01251-7
  28. Mensonides FI, Schuurmans JM, Teixeira de Mattos MJ, Hellingwerf KJ, Brul S. 2002. The metabolic response of Saccharomyces cerevisiae to continuous heat stress. Mol. Biol. Rep. 29: 103-106. https://doi.org/10.1023/A:1020392805411
  29. Parada G, Acevedo F. 1983. On the relation of temperature and RNA content to the specific growth rate in Saccharomyces cerevisiae. Biotechnol. Bioeng. 25: 2785-2788. https://doi.org/10.1002/bit.260251120
  30. Teunissen A, Dumortier F, Gorwa MF, Bauer M, Tanghe A, Loiez A, et al. 2002. Isolation and characterization of a freeze-tolerant diploid derivative of an industrial baker's yeast strain and its use in frozen doughs. Appl. Environ. Microbiol. 68: 4780-4787. https://doi.org/10.1128/AEM.68.10.4780-4787.2002
  31. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G. 2006. Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314: 1565-1568. https://doi.org/10.1126/science.1131969
  32. Cipponi A, Thomas DM. 2014. Stress-induced cellular adaptive strategies: ancient evolutionarily conserved programs as new anticancer therapeutic targets. Bioessays 36: 552-560. https://doi.org/10.1002/bies.201300170
  33. Rosenberg SM, Thulin C, Harris RS. 1998. Transient and heritable mutators in adaptive evolution in the lab and in nature. Genetics 148: 1559-1566. https://doi.org/10.1093/genetics/148.4.1559
  34. Oud B, van Maris AJA, Daran JM, Pronk JT. 2012. Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast. FEMS Yeast Res. 12: 183-196. https://doi.org/10.1111/j.1567-1364.2011.00776.x
  35. Fabrizio P, Garvis S, Palladino F. 2019. Histone methylation and memory of environmental stress. Cells. 8: 339. https://doi.org/10.3390/cells8040339
  36. Westergard L, True HL. 2014. Wild yeast harbour a variety of distinct amyloid structures with strong prion-inducing capabilities. Mol. Microbiol. 92: 183-193. https://doi.org/10.1111/mmi.12543
  37. Datta A, Jinks-Robertson S. 1995. Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268: 1616-1619. https://doi.org/10.1126/science.7777859
  38. Shor E, Fox CA, Broach JR. 2013. The yeast environmental stress response regulates mutagenesis induced by proteotoxic stress. PLoS Genet. 9: e1003680. https://doi.org/10.1371/journal.pgen.1003680
  39. Sheltzer JM, Blank HM, Pfau SJ, Tange Y, George BM, Humpton TJ, et al. 2011. Aneuploidy drives genomic instability in yeast. Science 333: 1026-1030. https://doi.org/10.1126/science.1206412
  40. Heidenreich E, Novotny R, Kneidinger B, Holzmann V, Wintersberger U. 2003. Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells. EMBO J. 22: 2274-2283. https://doi.org/10.1093/emboj/cdg203
  41. Hickey CM, Wilson NR, Hochstrasser M. 2012. Function and regulation of SUMO proteases. Nat. Rev. Mol. Cell Biol. 13: 755-766. https://doi.org/10.1038/nrm3478
  42. Ryu HY, Su D, Wilson-Eisele NR, Zhao DJ, Lopez-Giraldez F, Hochstrasser M. 2019. The Ulp2 SUMO protease promotes transcription elongation through regulation of histone sumoylation. EMBO J. 38: e102003.
  43. Stephens AD, Snider CE, Bloom K. 2015. The SUMO deconjugating peptidase Smt4 contributes to the mechanism required for transition from sister chromatid arm cohesion to sister chromatid pericentromere separation. Cell Cycle 14: 2206-2218. https://doi.org/10.1080/15384101.2015.1046656
  44. Ryu HY, Wilson NR, Mehta S, Hwang SS, Hochstrasser M. 2016. Loss of the SUMO protease Ulp2 triggers a specific multichromosome aneuploidy. Genes Dev. 30: 1881-1894. https://doi.org/10.1101/gad.282194.116
  45. Ryu HY, Lopez-Giraldez F, Knight J, Hwang SS, Renner C, Kreft SG, et al. 2018. Distinct adaptive mechanisms drive recovery from aneuploidy caused by loss of the Ulp2 SUMO protease. Nat. Commun. 9: 5417. https://doi.org/10.1038/s41467-018-07836-0
  46. Ryu HY, Hochstrasser M. 2017. Adaptive aneuploidy counters a dysregulated SUMO system. Cell Cycle. 16: 383-385. https://doi.org/10.1080/15384101.2016.1256154
  47. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, et al. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924. https://doi.org/10.1126/science.1142210
  48. Cakar ZP, Seker UOS, Tamerler C, Sonderegger M, Sauer U. 2005. Evolutionary engineering of multiple-stress resistant Saccharomyces cerevisiae. FEMS Yeast Res. 5: 569-578. https://doi.org/10.1016/j.femsyr.2004.10.010
  49. van Maris AJA, Geertman JMA, Vermeulen A, Groothuizen MK, Winkler AA, Piper MDW, et al. 2004. Directed evolution of pyruvate decarboxylase-negative Saccharomyces cerevisiae, yielding a C-2-independent, glucose-tolerant, and pyruvate-hyperproducing yeast. Appl. Environ. Microbiol. 70: 159-166. https://doi.org/10.1128/AEM.70.1.159-166.2004
  50. Draper JS, Moore HD, Ruban LN, Gokhale PJ, Andrews PW. 2004. Culture and characterization of human embryonic stem cells. Stem Cells Dev. 13: 325-336. https://doi.org/10.1089/1547328041797525
  51. Mitalipova MM, Rao RR, Hoyer DM, Johnson JA, Meisner LF, Jones KL, et al. 2005. Preserving the genetic integrity of human embryonic stem cells. Nat. Biotechnol. 23: 19-20. https://doi.org/10.1038/nbt0105-19
  52. Inzunza J, Sahlen S, Holmberg K, Stromberg AM, Teerijoki H, Blennow E, et al. 2004. Comparative genomic hybridization and karyotyping of human embryonic stem cells reveals the occurrence of an isodicentric X chromosome after long-term cultivation. Mol. Hum. Reprod. 10: 461-466. https://doi.org/10.1093/molehr/gah051
  53. Maitra A, Arking DE, Shivapurkar N, Ikeda M, Stastny V, Kassauei K, et al. 2005. Genomic alterations in cultured human embryonic stem cells. Nat. Genet. 37: 1099-1103. https://doi.org/10.1038/ng1631
  54. Olariu V, Harrison NJ, Coca D, Gokhale PJ, Baker D, Billings S, et al. 2010. Modeling the evolution of culture-adapted human embryonic stem cells. Stem Cell Res. 4: 50-56. https://doi.org/10.1016/j.scr.2009.09.001