Increasing proline and myo-inositol improves tolerance of Saccharomyces cerevisiae to the mixture of multiple lignocellulose-derived inhibitors

Biotechnology for Biofuels

Volumn 8, Issue 1, 2015, Pages

  Wang, Xin ^a   Bai, Xue ^a   Chen, Dong Fang ^a   Chen, Fu Zan ^a   Li, Bing Zhi ^a   Yuan, Ying Jin ^a  

^a TIANJIN UNIVERSITY   (China)

Author keywords

Lignocellulose derived inhibitors; Metabolomics; Myo inositol; Proline; Synthetic biology; Tolerance

Indexed keywords

ALCOHOLS; BACTERIA; CELLULOSE; CELLULOSIC ETHANOL; FITS AND TOLERANCES; GENES; LIGNIN; MICROORGANISMS; SUGARS; YEAST;

INHIBITION MECHANISMS; INHIBITOR TOLERANCES; METABOLOMIC ANALYSIS; METABOLOMICS; MYO-INOSITOL; PROLINE; REACTIVE OXYGEN SPECIES; SYNTHETIC BIOLOGY;

POLYOLS;

BIOLOGY; FERMENTATION; INHIBITOR; METABOLITE; PHENOL; STRAIN;

SACCHAROMYCES CEREVISIAE;

EID: 84941625375     PISSN: 17546834     EISSN: None     Source Type: Journal    
DOI: 10.1186/s13068-015-0329-5     Document Type: Article

References (45)

1. Peralta-Yahya PP, Zhang F, del Cardayre SB, Keasling JD. Microbial engineering for the production of advanced biofuels. Nature. 2012;488(7411):320-8.
2. Jonsson LJ, Alriksson B, Nilvebrant NO. Bioconversion of lignocellulose: inhibitors and detoxification. Biotechnol Biofuels. 2013;6(1):16.
3. Ling H, Teo W, Chen B, Leong SS, Chang MW. Microbial tolerance engineering toward biochemical production: from lignocellulose to products. Curr Opin Biotechnol. 2014;29:99-106.
4. Lo TM, Teo WS, Ling H, Chen B, Kang A, Chang MW. Microbial engineering strategies to improve cell viability for biochemical production. Biotechnol Adv. 2013;31(6):903-14.
5. Liu ZL, Moon J, Andersh BJ, Slininger PJ, Weber S. Multiple gene-mediated NAD(P)H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and 5-hydroxymethylfurfural by Saccharomyces cerevisiae. Appl Microbiol Biotechnol. 2008;81(4):743-53.
6. Heer D, Heine D, Sauer U. Resistance of Saccharomyces cerevisiae to high concentrations of furfural is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol. 2009;75(24):7631-8.
7. Ishii J, Yoshimura K, Hasunuma T, Kondo A. Reduction of furan derivatives by overexpressing NADH-dependent Adh1 improves ethanol fermentation using xylose as sole carbon source with Saccharomyces cerevisiae harboring XR-XDH pathway. Appl Microbiol Biotechnol. 2013;97(6):2597-607.
8. Giannattasio S, Guaragnella N, Zdralevic M, Marra E. Molecular mechanisms of Saccharomyces cerevisiae stress adaptation and programmed cell death in response to acetic acid. Front Microbiol. 2013;4:33.
9. Tanaka K, Ishii Y, Ogawa J, Shima J. Enhancement of acetic acid tolerance in Saccharomyces cerevisiae by overexpression of the HAA1 gene, encoding a transcriptional activator. Appl Environ Microbiol. 2012;78(22):8161-3.
10. Mollapour M, Piper PW. Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid. Mol Cell Biol. 2007;27(18):6446-56.
11. Larsson S, Cassland P, Jonsson LJ. Development of a Saccharomyces cerevisiae strain with enhanced resistance to phenolic fermentation inhibitors in lignocellulose hydrolysates by heterologous expression of laccase. Appl Environ Microbiol. 2001;67(3):1163-70.
12. Oldiges M, Lutz S, Pflug S, Schroer K, Stein N, Wiendahl C. Metabolomics: current state and evolving methodologies and tools. Appl Microbiol Biotechnol. 2007;76(3):495-511.
13. Lu S, Wang J, Niu Y, Yang J, Zhou J, Yuan Y. Metabolic profiling reveals growth related FAME productivity and quality of Chlorella sorokiniana with different inoculum sizes. Biotechnol Bioeng. 2012;109(7):1651-62.
14. Hasunuma T, Sanda T, Yamada R, Yoshimura K, Ishii J, Kondo A. Metabolic pathway engineering based on metabolomics confers acetic and formic acid tolerance to a recombinant xylose-fermenting strain of Saccharomyces cerevisiae. Microb Cell Fact. 2011;10(1):1475-2859.
15. Liang X, Dickman MB, Becker DF. Proline biosynthesis is required for endoplasmic reticulum stress tolerance in Saccharomyces cerevisiae. J Biol Chem. 2014;289(40):27794-806.
16. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant Signal Behav. 2012;7(11):1456-66.
17. Hong ME, Lee KS, Yu BJ, Sung YJ, Park SM, Koo HM, et al. Identification of gene targets eliciting improved alcohol tolerance in Saccharomyces cerevisiae through inverse metabolic engineering. J Biotechnol. 2010;149(1-2):52-9.
18. Kildegaard KR, Hallstrom BM, Blicher TH, Sonnenschein N, Jensen NB, Sherstyk S, et al. Evolution reveals a glutathione-dependent mechanism of 3-hydroxypropionic acid tolerance. Metab Eng. 2014;26c:57-66.
19. Lv YJ, Wang X, Ma Q, Bai X, Li BZ, Zhang W, et al. Proteomic analysis reveals complex metabolic regulation in Saccharomyces cerevisiae cells against multiple inhibitors stress. Appl Microbiol Biotechnol. 2014;98(5):2207-21.
20. Liu ZL. Genomic adaptation of ethanologenic yeast to biomass conversion inhibitors. Appl Microbiol Biotechnol. 2006;73(1):27-36.
21. Kim SK, Jin YS, Choi IG, Park YC, Seo JH. Enhanced tolerance of Saccharomyces cerevisiae to multiple lignocellulose-derived inhibitors through modulation of spermidine contents. Metab Eng. 2015;29:46-55.
22. Wang X, Yang B, Zhang A, Sun H, Yan G. Potential drug targets on insomnia and intervention effects of Jujuboside A through metabolic pathway analysis as revealed by UPLC/ESI-SYNAPT-HDMS coupled with pattern recognition approach. J Proteom. 2012;75(4):1411-27.
23. Wang X, Li BZ, Ding M-Z, Zhang WW, Yuan YJ. Metabolomic analysis reveals key metabolites related to the rapid adaptation of Saccharomyces cerevisiae to multiple inhibitors of furfural, acetic acid, and phenol. Omics-a J Integr Biol. 2013;17(3):150-9.
24. Horvath IS, Franzen CJ, Taherzadeh MJ, Niklasson C, Liden G. Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in glucose-limited chemostats. Appl Environ Microbiol. 2003;69(7):4076-86.
25. Lin FM, Qiao B, Yuan YJ. Comparative proteomic analysis of tolerance and adaptation of ethanologenic Saccharomyces cerevisiae to furfural, a lignocellulosic inhibitory compound. Appl Environ Microbiol. 2009;75(11):3765-76.
26. Yang J, Ding MZ, Li BZ, Liu ZL, Wang X, Yuan YJ. Integrated phospholipidomics and transcriptomics analysis of Saccharomyces cerevisiae with enhanced tolerance to a mixture of acetic acid, furfural, and phenol. Omics-a J Integr Biol. 2012;16(7-8):374-86.
27. Smith CJ, Deutch AH, Rushlow KE. Purification and characteristics of a gamma-glutamyl kinase involved in Escherichia coli proline biosynthesis. J Bacteriol. 1984;157(2):545-51.
28. Sekine T, Kawaguchi A, Hamano Y, Takagi H. Desensitization of feedback inhibition of the Saccharomyces cerevisiae gamma-glutamyl kinase enhances proline accumulation and freezing tolerance. Appl Environ Microbiol. 2007;73(12):4011-9.
29. Kaino T, Takagi H. Proline as a stress protectant in the yeast Saccharomyces cerevisiae: effects of trehalose and PRO1 gene expression on stress tolerance. Biosci Biotechnol Biochem. 2009;73(9):2131-5.
30. Sasano Y, Haitani Y, Hashida K, Ohtsu I, Shima J, Takagi H. Enhancement of the proline and nitric oxide synthetic pathway improves fermentation ability under multiple baking-associated stress conditions in industrial baker's yeast. Microb Cell Fact. 2012;11(40):1475-2859.
31. Sasano Y, Haitani Y, Ohtsu I, Shima J, Takagi H. Proline accumulation in baker's yeast enhances high-sucrose stress tolerance and fermentation ability in sweet dough. Int J Food Microbiol. 2012;152(1-2):40-3.
32. Takagi H, Takaoka M, Kawaguchi A, Kubo Y. Effect of l-proline on sake brewing and ethanol stress in Saccharomyces cerevisiae. Appl Environ Microbiol. 2005;71(12):8656-62.
33. Takagi H. Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Appl Microbiol Biotechnol. 2008;81(2):211-23.
34. Allen SA, Clark W, McCaffery JM, Cai Z, Lanctot A, Slininger PJ, et al. Furfural induces reactive oxygen species accumulation and cellular damage in Saccharomyces cerevisiae. Biotechnol Biofuels. 2010;3:2.
35. Ludovico P, Sousa MJ, Silva MT, Leao C, Corte-Real M. Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology. 2001;147:2409-15.
36. Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Frohlich KU. Apoptosis in yeast. Curr Opin Microbiol. 2004;7(6):655-60.
37. Chen CB, Dickman MB. Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci USA. 2005;102(9):3459-64.
38. Monserrate JP, York JD. Inositol phosphate synthesis and the nuclear processes they affect. Curr Opin Cell Biol. 2010;22(3):365-73.
39. Carman GM, Han GS. Regulation of phospholipid synthesis in the yeast Saccharomyces cerevisiae. Annu Rev Biochem. 2011;80:859-83.
40. Zha J, Li BZ, Shen MH, Hu ML, Song H, Yuan YJ. Optimization of CDT-1 and XYL1 expression for balanced co-production of ethanol and xylitol from cellobiose and xylose by engineered Saccharomyces cerevisiae. PLoS One. 2013;8(7):e68317.
41. Gietz RD, Schiestl RH, Willems AR, Woods RA. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast. 1995;11(4):355-60.
42. Peng HC, Long FH, Ding C. Feature selection based on mutual information: criteria of max-dependency, max-relevance, and min-redundancy. IEEE Trans Pattern Anal Mach Intell. 2005;27(8):1226-38.
43. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. MetaboAnalyst 2.0 - a comprehensive server for metabolomic data analysis. Nucleic Acids Res. 2012;40:W127-33.
44. Xia J, Wishart DS. MetPA: a web-based metabolomics tool for pathway analysis and visualization. Bioinformatics. 2010;26(18):2342-4.
45. Sikorski RS, Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989;122(1):19-27.