Increased expression of the yeast multidrug resistance ABC transporter Pdr18 leads to increased ethanol tolerance and ethanol production in high gravity alcoholic fermentation

Microbial Cell Factories

Volumn 11, Issue , 2012, Pages

  Teixeira, Miguel C ^a   Godinho, Cláudia P ^a   Cabrito, Tânia R ^a   Mira, Nuno P ^a   Sá Correia, Isabel ^a  

^a Instituto de Biotecnologia e Bioengenharia Lisboa   (Portugal)

Author keywords

ABC multidrug transporters; Bio ethanol production; Ethanol tolerance; Membrane permeabilization; Saccharomyces cerevisiae

Indexed keywords

ALCOHOL; ERGOSTEROL; FUNGAL PROTEIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; PDR18 PROTEIN; UNCLASSIFIED DRUG; ABC TRANSPORTER; PDR18 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ALCOHOL PRODUCTION; ALCOHOL TOLERANCE; ARTICLE; CELL MEMBRANE; CELL PERMEABILIZATION; CONTROLLED STUDY; FERMENTATION; FUNGAL STRAIN; GROWTH INHIBITION; NONHUMAN; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; YEAST CELL; CHEMISTRY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GRAVITY; METABOLISM; MICROBIOLOGY; UPREGULATION;

SACCHAROMYCES CEREVISIAE;

ATP-BINDING CASSETTE TRANSPORTERS; ETHANOL; FERMENTATION; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; HYPERGRAVITY; INDUSTRIAL MICROBIOLOGY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UP-REGULATION;

EID: 84864190737     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/1475-2859-11-98     Document Type: Article

References (33)

1. Schubert C. Can biofuels finally take center stage?. Nat Biotechnol 2006, 24(7):777-784. 10.1038/nbt0706-777, 16841058.
2. Van Uden N. Ethanol toxicity and ethanol tolerance in yeasts. Ann Rep Ferm Process 1985, 8:11-58.
3. Mira NP, Teixeira MC, Sá-Correia I. Adaptive response and tolerance to weak acids inSaccharomyces cerevisiae: a genome-wide view. OMICS 2010, 14(5):525-540. 10.1089/omi.2010.0072, 3129613, 20955006.
4. Teixeira MC, Mira NP, Sá-Correia I. A genome-wide perspective on the response and tolerance to food-relevant stresses inSaccharomyces cerevisiae. Curr Opin Biotechnol 2011, 22:150-156. 10.1016/j.copbio.2010.10.011, 21087853.
5. Gibson BR, Lawrence SJ, Leclaire JP, Powell CD, Smart KA. Yeast responses to stresses associated with industrial brewery handling. FEMS Microbiol Rev 2007, 31(5):535-569. 10.1111/j.1574-6976.2007.00076.x, 17645521.
6. Rosa MF, Sá-Correia I. In vivo activation by ethanol of plasma membrane ATPase ofSaccharomyces cerevisiae. Appl Environ Microbiol 1991, 57(3):830-835. 182802, 1645512.
7. Rosa MF, Sá-Correia I. Intracellular acidification does not account for inhibition ofSaccharomyces cerevisiaegrowth in the presence of ethanol. FEMS Microbiol Lett 1996, 135(2-3):271-274.
8. Salgueiro SP, Sá-Correia I, Novais JM. Ethanol-Induced Leakage inSaccharomyces cerevisiae: Kinetics and Relationship to Yeast Ethanol Tolerance and Alcohol Fermentation Productivity. Appl Environ Microbiol 1988, 54(4):903-909. 202571, 16347612.
9. Alexandre H, Ansanay-Galeote V, Dequin S, Blondin B. Global gene expression during short-term ethanol stress inSaccharomyces cerevisiae. FEBS Lett 2001, 498(1):98-103. 10.1016/S0014-5793(01)02503-0, 11389906.
10. Fujita K, Matsuyama A, Kobayashi Y, Iwahashi H. The genome-wide screening of yeast deletion mutants to identify the genes required for tolerance to ethanol and other alcohols. FEMS Yeast Res 2006, 6(5):744-750. 10.1111/j.1567-1364.2006.00040.x, 16879425.
11. Kubota S, Takeo I, Kume K, Kanai M, Shitamukai A, Mizunuma M, Miyakawa T, Shimoi H, Iefuji H, Hirata D. Effect of ethanol on cell growth of budding yeast: genes that are important for cell growth in the presence of ethanol. Biosci Biotechnol Biochem 2004, 68(4):968-972. 10.1271/bbb.68.968, 15118337.
12. van Voorst F, Houghton-Larsen J, Jonson L, Kielland-Brandt MC, Brandt A. Genome-wide identification of genes required for growth ofSaccharomyces cerevisiaeunder ethanol stress. Yeast 2006, 23(5):351-359. 10.1002/yea.1359, 16598687.
13. Hirasawa T, Yoshikawa K, Nakakura Y, Nagahisa K, Furusawa C, Katakura Y, Shimizu H, Shioya S. Identification of target genes conferring ethanol stress tolerance toSaccharomyces cerevisiaebased on DNA microarray data analysis. J Biotechnol 2007, 131(1):34-44. 10.1016/j.jbiotec.2007.05.010, 17604866.
14. Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T, Shimizu H. Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress inSaccharomyces cerevisiae. FEMS Yeast Res 2009, 9(1):32-44. 10.1111/j.1567-1364.2008.00456.x, 19054128.
15. Teixeira MC, Raposo LR, Mira NP, Lourenco AB, Sá-Correia I. Genome-wide identification ofSaccharomyces cerevisiaegenes required for maximal tolerance to ethanol. Appl Environ Microbiol 2009, 75(18):5761-5772. 10.1128/AEM.00845-09, 2747848, 19633105.
16. Wysocki R, Chery CC, Wawrzycka D, Van Hulle M, Cornelis R, Thevelein JM, Tamas MJ. The glycerol channel Fps1p mediates the uptake of arsenite and antimonite inSaccharomyces cerevisiae. Mol Microbiol 2001, 40(6):1391-1401. 10.1046/j.1365-2958.2001.02485.x, 11442837.
17. Hohmann S. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 2002, 66(2):300-372. 10.1128/MMBR.66.2.300-372.2002, 120784, 12040128.
18. 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):6446-6456. 10.1128/MCB.02205-06, 2099610, 17620418.
19. Nozawa A, Takano J, Kobayashi M, von Wiren N, Fujiwara T. Roles ofBOR1,DUR3, andFPS1in boron transport and tolerance inSaccharomyces cerevisiae. FEMS Microbiol Lett 2006, 262(2):216-222. 10.1111/j.1574-6968.2006.00395.x, 16923078.
20. Pettersson N, Filipsson C, Becit E, Brive L, Hohmann S. Aquaporins in yeasts and filamentous fungi. Biol Cell 2005, 97(7):487-500. 10.1042/BC20040144, 15966864.
21. Támas MJ, Luyten K, Sutherland FC, Hernandez A, Albertyn J, Valadi H, Li H, Prior BA, Kilian SG, Ramos J, et al. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol Microbiol 1999, 31(4):1087-1104. 10.1046/j.1365-2958.1999.01248.x, 10096077.
22. Toh TH, Kayingo G, van der Merwe MJ, Kilian SG, Hallsworth JE, Hohmann S, Prior BA. Implications ofFPS1deletion and membrane ergosterol content for glycerol efflux fromSaccharomyces cerevisiae. FEMS Yeast Res 2001, 1(3):205-211.
23. Jungwirth H, Kuchler K. Yeast ABC transporters- a tale of sex, stress, drugs and aging. FEBS Lett 2006, 580(4):1131-1138. 10.1016/j.febslet.2005.12.050, 16406363.
24. Sá-Correia I, Santos S, Teixeira M, Cabrito T, Mira N. Drug:H+antiporters in chemical stress response in yeast. Trends Microbiol 2009, 17:22-31. 10.1016/j.tim.2008.09.007, 19062291.
25. Paumi CM, Chuk M, Snider J, Stagljar I, Michaelis S. ABC transporters inSaccharomyces cerevisiaeand their interactors: new technology advances the biology of the ABCC (MRP) subfamily. Microbiol Mol Biol Rev 2009, 73(4):577-593. 10.1128/MMBR.00020-09, 2786581, 19946134.
26. Cabrito TR, Teixeira MC, Singh A, Prasad R, Sá-Correia I. The yeast ABC transporter Pdr18 (ORFYNR070w) controls plasma membrane sterol composition, playing a role in multidrug resistance. Biochem J 2011, 440:195-202. 10.1042/BJ20110876, 3215286, 21831043.
27. Hillenmeyer ME, Fung E, Wildenhain J, Pierce SE, Hoon S, Lee W, Proctor M, St Onge RP, Tyers M, Koller D, et al. The chemical genomic portrait of yeast: uncovering a phenotype for all genes. Science 2008, 320(5874):362-365. 10.1126/science.1150021, 2794835, 18420932.
28. Marks VD, Ho Sui SJ, Erasmus D, van der Merwe GK, Brumm J, Wasserman WW, Bryan J, van Vuuren HJ. Dynamics of the yeast transcriptome during wine fermentation reveals a novel fermentation stress response. FEMS Yeast Res 2008, 8(1):35-52. 10.1111/j.1567-1364.2007.00338.x, 18215224.
29. Pereira FB, Guimaraes PM, Gomes DG, Mira NP, Teixeira MC, Sá-Correia I, Domingues L. Identification of candidate genes for yeast engineering to improve bioethanol production in Very-High-Gravity and lignocellulosic biomass industrial fermentations. Biotechnol Biofuels 2011, 4(1):57. 10.1186/1754-6834-4-57, 3287136, 22152034.
30. D'Amore T, Panchal CJ, Stewart GG. Intracellular ethanol accumulation inSaccharomyces cerevisiaeduring fermentation. Appl Environ Microbiol 1988, 54(1):110-114. 202405, 3278685.
31. Dupont S, Beney L, Ferreira T, Gervais P. Nature of sterols affects plasma membrane behavior and yeast survival during dehydration. Biochim Biophys Acta 2011, 1808(6):1520-1528. 10.1016/j.bbamem.2010.11.012, 21081111.
32. Vanegas JM, Contreras MF, Faller R, Longo ML. Role of unsaturated lipid and ergosterol in ethanol tolerance of model yeast biomembranes. Biophys J 2012, 102(3):507-516. 10.1016/j.bpj.2011.12.038, 22325273.
33. Garcia-Gonzalez L, Geeraerd AH, Mast J, Briers Y, Elst K, Van Ginneken L, Van Impe JF, Devlieghere F. Membrane permeabilization and cellular death ofEscherichia coli,Listeria monocytogenesandSaccharomyces cerevisiaeas induced by high pressure carbon dioxide treatment. Food Microbiol 2010, 27(4):541-549. 10.1016/j.fm.2009.12.004, 20417405.