Metabolomic analysis reveals key metabolites related to the rapid adaptation of saccharomyce cerevisiae to multiple inhibitors of furfural, acetic acid, and phenol

OMICS A Journal of Integrative Biology

Volumn 17, Issue 3, 2013, Pages 150-159

  Wang, Xin ^a   Li, Bing Zhi ^a   Ding, Ming Zhu ^a   Zhang, Wei Wen ^a   Yuan, Ying Jin ^a  

^a TIANJIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2 FUROIC ACID; 2,3 BUTANEDIOL; ACETIC ACID; FURFURAL; PHENOL;

ADAPTATION; ALCOHOL PRODUCTION; AMINO ACID METABOLISM; ARTICLE; BIOMASS; CITRIC ACID CYCLE; DELETION MUTANT; FERMENTATION; FUNGAL STRAIN; GENE INACTIVATION; GLUCOSE UTILIZATION; GLYCOLYSIS; METABOLIC RATE; METABOLITE; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ACETIC ACID; ADAPTATION, PHYSIOLOGICAL; BIOMASS; ETHANOL; FERMENTATION; FURALDEHYDE; GLYCOLYSIS; LIGNIN; METABOLOMICS; PHENOL; SACCHAROMYCES CEREVISIAE;

EID: 84875193397     PISSN: 15362310     EISSN: 15578100     Source Type: Journal    
DOI: 10.1089/omi.2012.0093     Document Type: Article

References (42)

1. Almeida JRM, Modig T, Petersson A, Hahn-Hagerdal B, Liden G, and Gorwa-Grauslund MF. (2007). Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82, 340-349.
2. Ansell R, Granath K, Hohmann S, Thevelein JM, and Adler L. (1997). The two isoenzymes for yeast NAD(+)-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16, 2179-2187.
3. Bach B, Meudec E, Lepoutre JP, et al. (2009). New insights into {gamma}-aminobutyric acid catabolism: Evidence for {gamma}-hydroxybutyric acid and polyhydroxybutyrate synthesis in Saccharomyces cerevisiae. Appl Environ Microbiol 75, 4231-4239.
4. Banerjee N, Bhatnagar R, and Viswanathan L., (1981). Inhibition of glycolysis by furfural in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 11, 226-228.
5. Blomberg A. (2000). Metabolic surprises in Saccharomyces cerevisiae during adaptation to saline conditions: Questions, some answers and a model. Fems Microbiol Lett 182, 1-8.
6. Bouche N, Fait A, Bouchez D, Moller SG, and Fromm H. (2003). Mitochondrial succinic-semialdehyde dehydrogenase of the gamma-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Natl Acad Sci USA 100, 6843-6848.
7. Bro C, Regenberg B, Forster J, and Nielsen J. (2006). In silico aided metabolic engineering of Saccharomyces cerevisiae for improved bioethanol production. Metabol Eng 8, 102-111.
8. Devantier R, Scheithauer B, Villas-Boas SG, Pedersen S, and Olsson l. (2005). Metabolite profiling for analysis of yeast stress response during very high gravity ethanol fermentations. Biotechnol Bioeng 90, 703-714.
9. Ding MZ, Zhou X, and Yuan YJ. (2010). Metabolome profiling reveals adaptive evolution of Saccharomyces cerevisiae during repeated vacuum fermentations. Metabolomics 6, 42-55.
10. Dinh TN, Nagahisa K, Hirasawa T, Furusawa C, and Shimizu H. (2008). Adaptation of Saccharomyces cerevisiae cells to high ethanol concentration and changes in fatty acid composition of membrane and cell size. Plos One 3, e2623.
11. Fiehn O. (2002). Metabolomics: The link between genotypes and phenotypes. Plant Mol Biol 48, 155-171.
12. Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, and Willmitzer L. (2000). Metabolite profiling for plant functional genomics. Nature Biotechnol 18, 1157-1161.
13. Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, and Skory CD. (2006). Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 71, 339-349.
14. Heer D, Heine E, and Sauer U. (2009). Resistance of Saccharomyces cerevisiae to high concentrations of furfural is based on NADPH-dependent reduction by at least two oxireductases. Appl Environ Microbiol 75, 7631-7638.
15. Heer D, and Sauer U. (2008). Identification of furfural as a key toxin in lignocellulosic hydrolysates and evolution of a tolerant yeast strain. Microb Biotechnol 1, 497-506.
16. Horvath IS, Franzen CJ, Taherzadeh MJ, Niklasson C, and Liden G. (2003). Effects of furfural on the respiratory metabolism of Saccharomyces cerevisiae in glucose-limited chemostats. Appl Environ Microbiol 69, 4076-4086.
17. Klinke HB, Thomsen AB, and Ahring BK. (2004). Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 66, 10-26.
18. Kresnowati MTAP, Van Winden WA, Van Gulik WM, and Heijnen JJ. (2008). Dynamic in vivo metabolome response of Saccharomyces cerevisiae to a stepwise perturbation of the ATP requirement for benzoate export. Biotechnol Bioeng 99, 421-441.
19. Larsson S, Cassland P, and Jonsson LJ. (2001). Development of a Saccharomyces cerevisiae strain with enhanced resistance to phenolic fermentation inhibitors in lignocellulose hydrolysates by heterologous expression of laccase. Appl Environ Microbiol 67, 1163-1170.
20. Li BZ, and Yuan YJ. (2010). Transcriptome shifts in response to furfural and acetic acid in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 86, 1915-1924.
21. Lin FM, Qiao B, and Yuan YJ. (2009). Comparative proteomic analysis of tolerance and adaptation of ethanologenic Saccharomyces cerevisiae to furfural, a lignocellulosic inhibitory compound. Appl EnvironMicrobiol 75, 3765-3776.
22. Liu ZL, Moon J, Andersh BJ, Slininger PJ, and Weber S. (2008). 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 81, 743-753.
23. Liu ZL, Slininger PJ, and Gorsich SW. (2005). Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 121, 451-460.
24. Lourenc AB, Ascenso JR, and Sa-Correia I. (2011). Metabolic insights into the yeast response to propionic acid based on high resolution H-1 NMR spectroscopy. Metabolomics 7, 457-468.
25. Martinez A, Rodriguez ME, Wells ML, York SW, Preston JF, and Ingram LO. (2001). Detoxification of dilute acid hydrolysates of lignocellulose with lime. Biotechnol Prog 17, 287-293.
26. Palmqvist E, Almeida JS, and Hahn-Hagerdal B. (1999a). Influence of furfural on anaerobic glycolytic kinetics of Saccharomyces cerevisiae in batch culture. Biotechnol Bioengin 62, 447-454.
27. Palmqvist E, Grage H, Meinander NQ, and Hahn-Hagerdal B. (1999b). Main and interaction effects of acetic acid, furfural, and p-hydroxybenzoic acid on growth and ethanol productivity of yeasts. Biotechnol Bioeng 63, 46-55.
28. Palmqvist E, and Hahn-Hagerdal B. (2000a). Fermentation of lignocellulosic hydrolysates. I: Inhibition and detoxification. Bioresource Technol 74, 17-24.
29. Palmqvist E, and Hahn-Hagerdal B. (2000b). Fermentation of lignocellulosic hydrolysates. II: Inhibitors and mechanisms of inhibition. Bioresource Technol 74, 25-33.
30. Pampulha ME, and Loureiro-Dias MC. (1989). Combined effect of acetic acid, pH and ethanol on intracellular pH of fermenting yeast. Appl Microbiol Biotechnol 31, 547-550.
31. Pampulha ME, and Loureiro-Dias MC. (1990). Activity of glycolytic enzymes of Saccharomyces cerevisiae in the presence of acetic acid. Appl Microbiol Biotechnol 34, 375-380.
32. Panagiotou G, Pachidou F, Petroutsos D, Olsson L, and Christakopoulos P. (2008). Fermentation characteristics of Fusarium oxysporum grown on acetate. Bioresource Technol 99, 7397-7401.
33. Pears MR, Codlin S, Haines RL, et al. (2010). Deletion of btn1, an orthologue of CLN3, increases glycolysis and perturbs amino acid metabolism in the fission yeast model of Batten disease. Mol Biosystems 6, 1093-1102.
34. Petersson A, Almeida JR, Modig T, et al. (2006). A 5-hydroxymethyl furfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 23, 455-464.
35. Romano P, Granchi L, Caruso M, et al. (2003). The speciesspecific ratios of 2,3-butanediol and acetoin isomers as a tool to evaluate wine yeast performance. Intl J Food Microbiol 86, 163-168.
36. Siderius M, and Mager WH. (2003). Conditional response to stress in yeast. Monatshefte Chem 134, 1433-1444.
37. Slininger PJ, Gorsich SW, and Liu ZL. (2009). Culture nutrition and physiology impact the inhibitor tolerance of the yeast Pichia stipitis NRRL Y-7124. Biotechnol Bioeng 102, 778-790.
38. Taherzadeh MJ, Gustafsson L, Niklasson C, and Liden G. (1999). Conversion of furfural in aerobic and anaerobic batch fermentation of glucose by Saccharomyces cerevisiae. J Biosci Bioeng 87, 169-174.
39. Xia JM, and Yuan YJ. (2009). Comparative lipidomics of four strains of Saccharomyces cerevisiae reveals different responses to furfural, phenol, and acetic acid. J Agric Food Chem 57, 99-108.
40. Yang J, Ding MZ, Li BZ, Liu ZL, Wang X, and Yuan YJ. (2012). Integrated phospholipidomics and transcriptomics analysis of Saccharomyces cerevisiae with enhanced tolerance to a mxture of acetic acid, furfural, and phenol. Omics J Integ Biol 16, 374-386.
41. Zhang Q, Lambert G, Liao D, et al. (2011). Acceleration of emergence of bacterial antibiotic resistance in connected microenvironments. Science 333, 1764-1767.
42. Zhong C, Cao YX, Li BZ, and Yuan YJ. (2010). Biofuels in China: Past, present and future. Biofuels Bioprod Bioref-Biofpr 4, 326-342.