Genomic structural variations contribute to trait improvement during whole-genome shuffling of yeast

Applied Microbiology and Biotechnology

Volumn 98, Issue 7, 2014, Pages 3059-3070

  Zheng, Dao Qiong ^a   Chen, Jie ^a   Zhang, Ke ^a   Gao, Ke Hui ^a   Li, Ou ^a   Wang, Pin Mei ^a   Zhang, Xiao Yang ^b   Du, Feng Guang ^b   Sun, Pei Yong ^b   Qu, Ai Min ^b   Wu, Shuang ^b   Wu, Xue Chang ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b State Key Laboratory of Motor Vehicle Biofuel Technology   (China)

Author keywords

Ethanol fermentation; Genomic structural variation; Stress tolerance; Whole genome shuffling; Yeast

Indexed keywords

ETHANOL; INDUSTRIAL APPLICATIONS; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TRANSCRIPTION; YEAST;

CHROMOSOMAL REARRANGEMENT; COPY NUMBER VARIATIONS; ETHANOL FERMENTATION; PHYSIOLOGICAL STATUS; SACCHAROMYCES CEREVISIAE STRAINS; STRESS TOLERANCE; STRUCTURAL VARIATIONS; WHOLE-GENOME SHUFFLING;

GENES;

ALCOHOL; REACTIVE OXYGEN METABOLITE;

BIOFUEL; CHROMOSOME; ETHANOL; FERMENTATION; GENETIC ENGINEERING; GENOME; GENOMICS; INDUSTRIAL PRODUCTION; KARYOTYPE; MOLECULAR ANALYSIS; PHYSIOLOGY; TOLERANCE; YEAST;

ARTICLE; CHROMOSOME REARRANGEMENT; CONTROLLED STUDY; COPY NUMBER VARIATION; FUNGAL CELL CULTURE; FUNGAL GENE; FUNGAL GENOME; FUNGAL STRAIN; GENE EXPRESSION; GENE TECHNOLOGY; GENETIC VARIABILITY; KARYOTYPING; NONHUMAN; PLOIDY; SACCHAROMYCES CEREVISIAE; SKN7 GENE; STRESS; WHOLE GENOME SHUFFLING; YEAST CELL; YFL052W GENE;

DNA SHUFFLING; GENOMIC STRUCTURAL VARIATION; KARYOTYPING; METABOLIC ENGINEERING; REAL-TIME POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE;

EID: 84898604795     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5423-7     Document Type: Article

References (51)

1. Akache B, Wu K, Turcotte B (2001) Phenotypic analysis of genes encoding yeast zinc cluster proteins. Nucleic Acids Res 29:2181-2190
2. Argueso JL, Carazzolle MF, Mieczkowski PA, Duarte FM, Netto OV, Missawa SK, Galzerani F, Costa GG, Vidal RO, Noronha MF, Dominska M, Andrietta MG, Andrietta SR, Cunha AF, Gomes LH, Tavares FC, Alcarde AR, Dietrich FS, McCusker JH, Petes TD, Pereira GA (2009) Genome structure of a Saccharomyces cerevisiae strain widely used in bioethanol production. Genome Res 19:2258-2270
3. Bajwa PK, Pinel D, Martin VJ, Trevors JT, Lee H (2010) Strain improvement of the pentose-fermenting yeast Pichia stipitis by genome shuffling. J Microbiol Methods 81:179-186
4. Bajwa PK, Ho CY, Chan CK, Martin VJ, Trevors JT, Lee H (2013) Transcriptional profiling of Saccharomyces cerevisiae T2 cells upon exposure to hardwood spent sulphite liquor: comparison to acetic acid, furfural and hydroxymethylfurfural. Antonie Van Leeuwenhoek 103:1-15
5. Borneman AR, Desany BA, Riches D, Affourtit JP, Forgan AH, Pretorius IS, Egholm M, Chambers PJ (2011) Whole-genome comparison reveals novel genetic elements that characterize the genome of industrial strains of Saccharomyces cerevisiae. PLoS Genet 7:e1001287
6. Brown NA, de Castro PA, Castro Pimentel Figueiredo B, Savoldi M, Buckeridge MS, Lopes ML, Lima Paullilo SC, Borges EP, Amorim HV, Goldman MH (2013) Transcriptional profiling of Brazilian Saccharomyces cerevisiae strains selected for semi-continuous fermentation of sugarcane must. FEMS Yeast Res 13:277-290
7. Chang SL, Lai HY, Tung SY, Leu JY (2013) Dynamic large-scale chromosomal rearrangements fuel rapid adaptation in yeast populations. PLoS Genet 9:e1003232
8. Dinh TN, Nagahisa K, Yoshikawa K, Hirasawa T, Furusawa C, Shimizu H (2009) Analysis of adaptation to high ethanol concentration in Saccharomyces cerevisiae using DNA microarray. Bioprocess Biosyst Eng 32:681-688
9. Dwight SS, Harris MA, Dolinski K, Ball CA, Binkley G, Christie KR, Fisk DG, Issel-Tarver L, Schroeder M, Sherlock G (2002) Saccharomyces Genome Database (SGD) provides secondary gene annotation using the Gene Ontology (GO). Nucleic Acids Res 30:69-72
10. Estruch F (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiol Rev 24:469-486
11. Gasch AP, Werner-Washburne M (2002) The genomics of yeast responses to environmental stress and starvation. Funct Integr Genomics 2:181-192
12. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241
13. Gong JX, Zheng HJ, Wu ZJ, Chen T, Zhao XM (2009) Genome shuffling: progress and applications for phenotype improvement. Biotechnol Adv 27:996-1005
14. Graves T, Narendranath NV, Dawson K, Power R (2006) Effect of pH and lactic or acetic acid on ethanol productivity by Saccharomyces cerevisiae in corn mash. J Ind Microbiol Biotechnol 33:469-474
15. Graves T, Narendranath NV, Dawson K, Power R (2007) Interaction effects of lactic acid and acetic acid at different temperatures on ethanol production by Saccharomyces cerevisiae in corn mash. Appl Microbiol Biotechnol 73:1190-1196
16. Guan N, Liu L, Shin H-D, Chen RR, Zhang J, Li J, Du G, Shi Z, Chen J (2013) Systems-level understanding how Propionibacterium acidipropionici respond to propionic acid stress at the microenvironment levels: mechanism and application. J Biotechnol 167:56-63
17. Gueldener U, Heinisch J, Koehler G, Voss D, Hegemann J (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30:e23-e23
18. Herrero E, Ros J, Bellí G, Cabiscol E (2008) Redox control and oxidative stress in yeast cells. Biochim Biophys Acta 1780:1217-1235
19. Hirasawa T, Nakakura Y, Yoshikawa K, Ashitani K, Nagahisa K, Furusawa C, Katakura Y, Shimizu H, Shioya S (2006) Comparative analysis of transcriptional responses to saline stress in the laboratory and brewing strains of Saccharomyces cerevisiae with DNA microarray. Appl Microbiol Biotechnol 70:346-357
20. Kim NR, Yang J, Kwon H, An J, Choi W, Kim W (2013) Mutations of the TATA-binding protein confer enhanced tolerance to hyperosmotic stress in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 97:8227-8238
21. Laopaiboon L, Nuanpeng S, Srinophakun P, Klanrit P, Laopaiboon P (2009) Ethanol production from sweet sorghum juice using very high gravity technology: effects of carbon and nitrogen supplementations. Bioresour Technol 100:4176-4182
22. Lewis JA, Elkon IM, McGee MA, Higbee AJ, Gasch AP (2010) Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics 186:1197-1205
23. Li RQ, Yu C, Li YR, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966-1967
24. Lucena BT, Silva-Filho EA, Coimbra MR, Morais JO, Simões DA, Morais MA Jr (2007) Chromosome instability in industrial strains of Saccharomyces cerevisiae batch cultivated under laboratory conditions. Genet Mol Res 6:1072-1084
25. Lv XA, Jin YY, Li YD, Zhang H, Liang XL (2013) Genome shuffling of Streptomyces viridochromogenes for improved production of avilamycin. Appl Microbiol Biotechnol 97:641-648
26. Mahmud SA, Hirasawa T, Furusawa C, Yoshikawa K, Shimizu H (2010) Understanding the mechanism of heat stress tolerance caused by high trehalose accumulation in Saccharomyces cerevisiae using DNA microarray. J Biosci Bioeng 113:526-528
27. Otte B, Grunwaldt E, Mahmoud O, Jennewein S (2009) Genome shuffling in Clostridium diolis DSM 15410 for improved 1, 3-propanediol production. Appl Environ Microbiol 75:7610-7616
28. Palma M, Madeira SC, Mendes-Ferreira A, Sá-Correia I (2013) Impact of assimilable nitrogen availability in glucose uptake kinetics in Saccharomyces cerevisiae during alcoholic fermentation. Microb Cell Fact 11:99
29. Patnaik R, Louie S, Gavrilovic V, Perry K, Stemmer WP, Ryan CM, del Cardayré S (2002) Genome shuffling of Lactobacillus for improved acid tolerance. Nat Biotechnol 20:707-712
30. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L, Sanderson BW, Hattem GL, Li R (2010) Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468:321-325
31. Pinel D, D'Aoust F, del Cardayre SB, Bajwa PK, Lee H, Martin VJ (2011) Saccharomyces cerevisiae genome shuffling through recursive population mating leads to improved tolerance to spent sulfite liquor. Appl Environ Microbiol 77:4736-4743
32. Raitt DC, Johnson AL, Erkine AM, Makino K, Morgan B, Gross DS, Johnston LH (2000) The Skn7 response regulator of Saccharomyces cerevisiae interacts with Hsf1 in vivo and is required for the induction of heat shock genes by oxidative stress. Mol Biol Cell 11:2335-2347
33. Rossouw D, Olivares-Hernandes R, Nielsen J, Bauer FF (2009) Comparative transcriptomic approach to investigate differences in wine yeast physiology and metabolism during fermentation. Appl Environ Microbiol 75:6600-6612
34. Rossouw D, Jacobson D, Bauer FF (2012) Transcriptional regulation and the diversification of metabolism in wine yeast strains. Genetics 190:251-261
35. Shi DJ, Wang CL, Wang KM (2009) Genome shuffling to improve thermotolerance, ethanol tolerance and ethanol productivity of Saccharomyces cerevisiae. J Ind Microbiol Biotechnol 36:139-147
36. Stambuk BU, Dunn B, Alves SL, Duval EH, Sherlock G (2009) Industrial fuel ethanol yeasts contain adaptive copy number changes in genes involved in vitamin B1 and B6 biosynthesis. Genome Res 19:2271-2278
37. Tao XL, Zheng DQ, Liu TZ, Wang PM, Zhao WP, Zhu MY, Jiang XH, Zhao YH, Wu XC (2012) A novel strategy to construct yeast Saccharomyces cerevisiae strains for very high gravity fermentation. PLoS One 7:e31235
38. Thomas K, Ingledew W (1992) Production of 21 % (v/v) ethanol by fermentation of very high gravity (VHG) wheat mashes. J Ind Microbiol 10:61-68
39. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, Amon A (2007) Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317:916-924
40. Torres EM, Dephoure N, Panneerselvam A, Tucker CM, Whittaker CA, Gygi SP, Dunham MJ, Amon A (2010) Identification of aneuploidy-tolerating mutations. Cell 143:71-83
41. Wang PM, Zheng DQ, Liu TZ, Tao XL, Feng MG, Min H, Jiang XH, Wu XC (2012) The combination of glycerol metabolic engineering and drug resistance marker-aided genome shuffling to improve very-high-gravity fermentation performances of industrial Saccharomyces cerevisiae. Bioresour Technol 108:203-210
42. Wood JS (1982) Mitotic chromosome loss induced by methyl benzimidazole-2-yl-carbamate as a rapid mapping method in Saccharomyces cerevisiae. Mol Cell Biol 2:1080-1087
43. Wu CY, Steffen J, Eide DJ (2009) Cytosolic superoxide dismutase (SOD1) is critical for tolerating the oxidative stress of zinc deficiency in yeast. PLoS One 4:e7061
44. Yang J, Bae JY, Lee YM, Kwon H, Moon HY, Kang HA, Yee SB, Kim W, Choi W (2011) Construction of Saccharomyces cerevisiae strains with enhanced ethanol tolerance by mutagenesis of the TATA-binding protein gene and identification of novel genes associated with ethanol tolerance. Biotechnol Bioeng 108:1776-1787
45. Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T, Shimizu H (2009) Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Res 9:32-44
46. Zhang W, Geng A (2012) Improved ethanol production by a xylose-fermenting recombinant yeast strain constructed through a modified genome shuffling method. Biotechnol Biofuels 5:1-11
47. Zhang YX, Perry K, Vinci VA, Powell K, Stemmer WP, del Cardayré SB (2002) Genome shuffling leads to rapid phenotypic improvement in bacteria. Nature 415:644-646
48. Zheng DQ, Wu XC, Tao XL, Wang PM, Li P, Chi XQ, Li YD, Yan QF, Zhao YH (2011) Screening and construction of Saccharomyces cerevisiae strains with improved multi-tolerance and bioethanol fermentation performance. Bioresour Technol 102:3020-3027
49. Zheng DQ, Wang PM, Chen J, Zhang K, Liu TZ, Wu XC, Li YD, Zhao YH (2012a) Genome sequencing and genetic breeding of a bioethanol Saccharomyces cerevisiae strain YJS329. BMC Genomics 13:479
50. Zheng P, Zhang KK, Yan Q, Xu Y, Sun ZH (2012b) Enhanced succinic acid production by Actinobacillus succinogenes after genome shuffling. J Ind Microbiol Biotechnol 40:1-10
51. Zheng DQ, Liu TZ, Chen J, Zhang K, Li O, Zhu L, Zhao YH, Wu XC, Wang PM (2013) Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Appl Microbiol Biotechnol 97:2067-2076