Absence of Rtt109p, a fungal-specific histone acetyltransferase, results in improved acetic acid tolerance of Saccharomyces cerevisiae

FEMS Yeast Research

Volumn 16, Issue 2, 2016, Pages

  Cheng, Cheng ^a   Zhao, Xinqing ^b,c   Zhang, Mingming ^a   Bai, Fengwu ^a,b,c  

^a DALIAN UNIVERSITY OF TECHNOLOGY   (China)

^b Shanghai Jiao Tong University   (China)

^c SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Acetic acid tolerance; Ethanol production; Histone modification; Oxidative stress; RTT109; Saccharomyces cerevisiae

Indexed keywords

ACETIC ACID; HISTONE ACETYLTRANSFERASE; HISTONE H3; RTT109 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONTROLLED STUDY; FLOCCULATION; FUNGAL STRAIN; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; NONHUMAN; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; DEFICIENCY; DRUG EFFECTS; DRUG TOLERANCE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ACETIC ACID; DRUG TOLERANCE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HISTONE ACETYLTRANSFERASES; OXIDATIVE STRESS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84963596182     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1093/femsyr/fow010     Document Type: Article

References (48)

1. Abbott DA, Suir E, Duong GH et al. Catalase overexpression reduces lactic acid-induced oxidative stress in Saccharomyces cerevisiae. Appl Environ Microbiol 2009;75:2320-5.
2. An J, Kwon H, Kim E et al. Tolerance to acetic acid is improved by mutations of the TATA-binding protein gene. Environ Microbiol 2015;17:656-69.
3. Ask M, Mapelli V, Höck H et al. Engineering glutathione biosynthesis of Saccharomyces cerevisiae increases robustness to inhibitors in pretreated lignocellulosic materials. Microb Cell Fact 2013;12:87.
4. Cecarini V, Gee J, Fioretti E et al. Protein oxidation and cellular homeostasis: emphasis on metabolism. BBA-Mol Cell Res 2007;1773:93-104.
5. Chen CC, Carson JJ, Feser J et al. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 2008;134:231-43.
6. Cheng C, Zhao XQ, Bai FW. Effect of cell flocculation and supplementation of zinc sulfate on enhancement of ethanol production in the presence of acetic acid. Chinese J Appl Environ Biol 2016;22:1136-42.
7. Costa V, Amorim MA, Reis E et al. Mitochondrial superoxide dismutase is essential for ethanol tolerance of Saccharomyces cerevisiae in the post-diauxic phase. Microbiology 1997;143:1649-56.
8. Dahlin JL, Chen X, WaltersMAet al. Histone-modifying enzymes, histone modifications and histone chaperones in nucleosome assembly: Lessons learned from Rtt109 histone acetyltransferases. Crit Rev Biochem Mol 2015;50:31-53.
9. D'Arcy S, Luger K. Understanding histone acetyltransferase Rtt109 structure and function: how many chaperones does it take? Curr Opin Struc Biol 2011;21:728-34.
10. Ding J, Holzwarth G, Bradford CS et al. PEP3 overexpression shortens lag phase but does not alter growth rate in Saccharomyces cerevisiae exposed to acetic acid stress. Appl Microbiol Biot 2015a;99:8667-80.
11. Ding J, Holzwarth G, Penner MH et al. Overexpression of acetyl-CoA synthetase in Saccharomyces cerevisiae increases acetic acid tolerance. FEMS Microbiol Lett 2015b;362:1-7.
12. Driscoll R, Hudson A, Jackson SP. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 2007;315:649-52.
13. Du X, Takagi H. N-Acetyltransferase Mpr1 confers ethanol tolerance on Saccharomyces cerevisiae by reducing reactive oxygen species. Appl Microbiol Biot 2007;75:1343-51.
14. Fierro-Risco J, Rincón AM, Benítez T et al. Overexpression of stress-related genes enhances cell viability and velum formation in Sherry wine yeasts. Appl Microbiol Biotl 2013;97:6867-81.
15. Giannattasio S, Guaragnella N, Zdralevic M et al. Molecular mechanisms of Saccharomyces cerevisiae stress adaptation and programmed cell death in response to acetic acid. Front Microbiol 2013;4:33.
16. Grant CM, MacIver FH, Dawes IW. Glutathione synthetase is dispensable for growth under both normal and oxidative stress conditions in the yeast Saccharomyces cerevisiae due to an accumulation of the dipeptide gamma-glutamylcysteine. Mol Biol Cell 1997;8:1699-707.
17. Guaragnella N, Antonacci L, Giannattasio S et al. Catalase T and Cu, Zn-superoxide dismutase in the acetic acid-induced programmed cell death in Saccharomyces cerevisiae. FEBS Lett 2008;582:210-4.
18. Inoue Y, Matsuda T, Sugiyama K et al. Genetic analysis of glutathione peroxidase in oxidative stress response of Saccharomyces cerevisiae. J Biol Chem 1999;274:27002-9.
19. Jamieson DJ. Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 1998;14:1511-27.
20. Jönsson LJ, Alriksson B, Nilvebrant NO. Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuel 2013;6:16.
21. Kim SR, Skerker JM, Kang W et al. Rational and evolutionary engineering approaches uncover a small set of genetic changes efficient for rapid xylose fermentation in Saccharomyces cerevisiae. PLoS One 2013;8:e57048.
22. Klopf E, Paskova L, C Solé et al. Cooperation between the INO80 complex and histone chaperones determines adaptation of stress gene transcription in the yeast Saccharomyces cerevisiae. Mol Cell Boil 2009;29:4994-5007.
23. Kobayashi O, Hayashi N, Kuroki R et al. Region of Flo1 proteins responsible for sugar recognition. J Bacteriol 1998;180: 6503-10.
24. Kouzarides T. Chromatin modifications and their function. Cell 2007;128:693-705.
25. Lee Y, Nasution O, Choi E et al. Transcriptome analysis of aceticacid-treated yeast cells identifies a large set of genes whose overexpression or deletion enhances acetic acid tolerance. Appl Microbiol Biot 2015;99:6391-403.
26. Lennartsson A, Ekwall K. Histonemodification patterns and epigenetic codes. BBA-Gen Subjects 2009;1790:863-8.
27. Lin C, Yuan YA. Structural insights into histone H3 lysine 56 acetylation by Rtt109. Structure 2008;16:1503-10.
28. Liu XY, Zhang XH, Zhang ZJ. Point mutation of H3/H4 histones affects acetic acid tolerance in Saccharomyces cerevisiae. J Biotechnol 2014;187:116-23.
29. -ΔΔCT method. Methods 2001;25:402-8.
30. Ludovico P, Sousa MJ, Silva MT et al. Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 2001;147:2409-15.
31. Ma C, Wei XW, Sun CH et al. Improvement of acetic acid tolerance of Saccharomyces cerevisiae using a zinc-finger-based artificial transcription factor and identification of novel genes involved in acetic acid tolerance. Appl Microbiol Biot 2015;99:2441-9.
32. Minard LV, Williams JS, Walker AC et al. Transcriptional regulation by Asf1: new mechanistic insights from studies of the DNA damage response to replication stress. J Biol Chem 2011;286:7082-92.
33. Moraitis C, Curran BPG. Reactive oxygen species may influence the heat shock response and stress tolerance in the yeast Saccharomyces cerevisiae. Yeast 2004;21:313-23.
34. Nishimura A, Kotani T, Sasano Y et al. An antioxidative mechanism mediated by the yeastN-acetyltransferaseMpr1: oxidative stress-induced arginine synthesis and its physiological role. FEMS Yeast Res 2010;10:687-98.
35. Okada N, Ogawa J, Shima J. Comprehensive analysis of genes involved in the oxidative stress tolerance using yeast heterozygous deletion collection. FEMS Yeast Res 2014;14: 425-34.
36. Peterson CL, LanielMA. Histones and histonemodifications. Curr Microbiol 2004;14:R546-51.
37. Rona G, Herdeiro R, Mathias CJ et al. CTT1 overexpression increases life span of calorie-restricted Saccharomyces cerevisiae deficient in Sod1. Biogerontology 2015;16:343-51.
38. Stanley D, Fraser S, Chambers PJ et al. Generation and characterisation of stable ethanol-tolerant mutants of Saccharomyces cerevisiae. J Ind Microbiol Biot 2010;37:139-49.
39. Stavropoulos P, Nagy V, Blobel G et al. Molecular basis for the autoregulation of the protein acetyl transferase Rtt109. P Natl Acad Sci USA 2008;105:12236-41.
40. Takabatake A, Kawazoe N, Izawa S. Plasma membrane proteins Yro2 and Mrh1 are required for acetic acid tolerance in Saccharomyces cerevisiae. Appl Microbiol Biot 2015;99:2805-14.
41. Thomas KC, Hynes SH, Ingledew WM. Influence of medium buffering capacity on inhibition of Saccharomyces cerevisiae growth by acetic and lactic acids. Apppl Environ Microbiol 2002;68:1616-23.
42. Wan C, Zhang MM, Fang Q et al. Impact of zinc sulfate addition on dynamic metabolic profiling of Saccharomyces cerevisiae subjected to long term acetic acid stress treatment and identification of key metabolites involved in antioxidant effect of zinc. Metallomics 2015;7:322-32.
43. Wang L, Zhao XQ, Xue C et al. Impact of osmotic stress and ethanol inhibition in yeast cells on process oscillation associated with continuous very-high-gravity ethanol fermentation. Biotechnol Biofuel 2013;6:1-10.
44. Welker S, Rudolph B, Frenzel E et al. Hsp12 is an intrinsically unstructured stress protein that folds upon membrane associationand modulates membrane function. Mol Cell 2010;39:507-20.
45. Westman JO, Mapelli V, Taherzadeh MJ et al. Flocculation causes inhibitor tolerance in Saccharomyces cerevisiae for second-generation bioethanol production. Appl Environ Microb 2014;80:6908-18.
46. Zhang MM, Zhao XQ, Cheng C et al. Improved growth and ethanol fermentation of Saccharomyces cerevisiae in the presence of acetic acid by overexpression of SET5 and PPR1. Biotechnol J 2015;10:1903-11.
47. Zhao XQ, Bai FW. Zinc and yeast stress tolerance: micronutrient plays a big role. J Biotechnol 2012;158:176-83.
48. Zheng DQ, Liu TZ, Chen J et al. Comparative functional genomics to reveal the molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Appl Microbiol Biot 2013;97:2067-76.