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Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status

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Abstract

Fuel ethanol production from plant biomass hydrolysates by Saccharomyces cerevisiae is of great economic and environmental significance. This paper reviews the current status with respect to alcoholic fermentation of the main plant biomass-derived monosaccharides by this yeast. Wild-type S. cerevisiae strains readily ferment glucose, mannose and fructose via the Embden–Meyerhof pathway of glycolysis, while galactose is fermented via the Leloir pathway. Construction of yeast strains that efficiently convert other potentially fermentable substrates in plant biomass hydrolysates into ethanol is a major challenge in metabolic engineering. The most abundant of these compounds is xylose. Recent metabolic and evolutionary engineering studies on S. cerevisiae strains that express a fungal xylose isomerase have enabled the rapid and efficient␣anaerobic fermentation of this pentose. l-Arabinose fermentation, based on the expression of a prokaryotic pathway in S. cerevisiae, has also been established, but needs further optimization before it can be considered for industrial implementation. In addition to these already investigated strategies, possible approaches for metabolic engineering of galacturonic acid and rhamnose fermentation by S. cerevisiae are discussed. An emerging and major challenge is to achieve the rapid transition from proof-of-principle experiments under ‘academic’ conditions (synthetic media, single substrates or simple substrate mixtures, absence of toxic inhibitors) towards efficient conversion of complex industrial substrate mixtures that contain synergistically acting inhibitors.

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References

  • Aarnio TH, Suihko ML, Kauppinen VS (1991) Isolation of acetic acid-tolerant bakers-yeast variants in a turbidostat. Appl Biochem Biotechnol 27:55–63

    Google Scholar 

  • Albers E, Larsson C, Lidén G, Niklasson C, Gustafsson L (1996) Influence of the nitrogen source on Saccharomyces cerevisiae anaerobic growth and product formation. Appl Environ Microbiol 62:3187–3195

    PubMed  CAS  Google Scholar 

  • Andreasen AA, Stier TJ (1953) Anaerobic nutrition of Saccharomyces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J Cell Physiol 41:23–36

    Google Scholar 

  • Andreasen AA, Stier TJ (1954) Anaerobic nutrition of Saccharomyces cerevisiae. II. Unsaturated fatty acid requirement for growth in a defined medium. J Cell Physiol 43:271–281

    Google Scholar 

  • Aristidou A, Penttilä M (2000) Metabolic engineering applications to renewable resource utilization. Curr Opin Biotechnol 11:187–198

    PubMed  CAS  Google Scholar 

  • Baciu IE, Jördening HJ (2004) Kinetics of galacturonic acid release from sugar-beet pulp. Enzyme Microb Technol 34:505–512

    CAS  Google Scholar 

  • Bakker BM, Bro C, Kötter P, Luttik MAH, van Dijken JP, Pronk JT (2000) The mitochondrial alcohol dehydrogenase Adh3p is involved in a redox shuttle in Saccharomyces cerevisiae. J Bacteriol 182:4730–4737

    PubMed  CAS  Google Scholar 

  • Bakker BM, Overkamp KM, van Maris AJ, Kötter P, Luttik MA, van Dijken JP, Pronk JT (2001) Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiol Rev 25:15–37

    PubMed  CAS  Google Scholar 

  • Baldoma L, Aguilar J (1988) Metabolism of l-fucose and l-rhamnose in Escherichia coli: aerobic-anaerobic regulation of l-lactaldehyde dissimilation. J Bacteriol 170:416–421

    PubMed  CAS  Google Scholar 

  • Baldomá L, Badia J, Sweet G, Aguilar J (1990). Cloning, mapping and gene-product identification of rha T from Escherichia coli K12. FEMS Microbiol Lett 72:103–108

    Google Scholar 

  • Barnett JA, Payne RW, Yarrow D (1990) Yeasts; Characteristics and identification. Cambridge University Press, Cambridge, UK. ISBN 0-521-35056-5

    Google Scholar 

  • Becker J, Boles E (2003) A modified Saccharomyces cerevisiae strain that consumes l-arabinose and produces ethanol. Appl Environ Microbiol 69:4144–4150

    PubMed  CAS  Google Scholar 

  • Bigg GR, Jickells TD, Liss PS, Osborn TJ (2003) The role of the oceans in climate. Int J Climatol 23:1127–1159

    Google Scholar 

  • Blanco P, Sieiro C, Díaz A, Villa TG (1994) Production and partial characterization of an endopolygalacturonase from Saccharomyces cerevisiae. Can J Microbiol 40:974–977

    PubMed  CAS  Google Scholar 

  • Blank LM, Lehmbeck F, Sauer U (2005) Metabolic-flux and network analysis in fourteen hemiascomycetous yeasts. FEMS Yeast Res 5:545–558

    PubMed  CAS  Google Scholar 

  • Blow DM, Hartley BS, Henrick K (1990) Xylose isomerase mutants. Pat. no. WO 9000196. Appl. no. 89-GB748

  • Boles E, Hollenberg CP (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21:85–111

    PubMed  CAS  Google Scholar 

  • Brandberg T, Sanandaji N, Gustafsson L, Franzén CJ (2005) Continuous fermentation of undetoxified dilute acid lignocellulose hydrolysate by Saccharomyces cerevisiae ATCC 96581 using cell recirculation. Biotechnol Prog 21:1093–1101

    PubMed  CAS  Google Scholar 

  • Bro C, Knudsen S, Regenberg B, Olsson L, Nielsen J (2005) Improvement of galactose uptake in Saccharomyces cerevisiae through overexpression of phosphoglucomutase: example of transcript analysis as a tool in inverse metabolic engineering. Appl Environ Microbiol 71:6465–6472

    PubMed  CAS  Google Scholar 

  • Bruinenberg PM, de Bot PHM, van Dijken JP, Scheffers WA (1983a) The role of the redox balance in the anaerobic fermentation of xylose by yeasts. Eur J Appl Microbiol Biotechnol 18:287–292

    CAS  Google Scholar 

  • Bruinenberg PM, de Bot PHM, van Dijken JP, Scheffers WA (1984) NADH-linked aldose reductase: the key to ethanolic fermentation of xylose by yeasts. Appl Microbiol Biotechnol 19:256–260

    CAS  Google Scholar 

  • Bruinenberg PM, van Dijken JP, Scheffers WA (1983b) An enzymic analysis of NADPH production and consumption in Candida utilis. J Gen Microbiol 129:965–971

    CAS  Google Scholar 

  • Buchert J, Puls J, Poutanen K (1989) The use of steamed hemicellulose as substrate in microbial conversions. Appl Biochem Biotechnol 20–1:309–318

    Google Scholar 

  • Casal M, Cardoso H, Leão C (1996) Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142:1385–1390

    PubMed  CAS  Google Scholar 

  • Chen Z, Ho NWY (1993) Cloning and improving the expression of Pichia stipitis xylose reductase gene in Saccharomyces cerevisiae. Appl Biochem Biotechnol 39–40:135–147

    Article  PubMed  Google Scholar 

  • Chiang GC, Knight SG (1960) A new pathway of pentose metabolism. Biochem Biophys Res Commun 3:554–559

    PubMed  CAS  Google Scholar 

  • Claassen PAM, van Lier JB, Lopez-Cóntreras AM, van Niel EWJ, Sijtsma L, Stams AJM, de Vries SS, Weusthuis RA (1999) Utilisation of biomass for the supply of energy carriers. Appl Microbiol Biotechnol 52:741–755

    CAS  Google Scholar 

  • Demain AL, Newcomb M, Wu JHD (2005) Cellulase, Clostridia, and ethanol. Microbiol Mol Biol Rev 69:124–154

    PubMed  CAS  Google Scholar 

  • Dien BS, Cotta MA, Jeffries TW (2003) Bacteria engineered for fuel ethanol production: current status. Appl Microbiol Biotechnol 63:258–266

    PubMed  CAS  Google Scholar 

  • Dien BS, Kurtzman CP, Saha BC, Bothast RJ (1996) Screening for l-arabinose fermenting yeasts. Appl Biochem Biotechnol 57–58:233–242

    Article  PubMed  Google Scholar 

  • Domingues L, Dantas MM, Lima N, Teixeira JA (1999a) Continuous ethanol fermentation of lactose by a recombinant flocculating Saccharomyces cerevisiae strain. Biotechnol Bioeng 64:692–697

    CAS  Google Scholar 

  • Domingues L, Teixeira JA, Lima N (1999b) Construction of a flocculent Saccharomyces cerevisiae fermenting lactose. Appl Microbiol Biotechnol 51:621–626

    CAS  Google Scholar 

  • Doran JB, Cripe J, Sutton M, Foster B (2000) Fermentations of pectin-rich biomass with recombinant bacteria to produce fuel ethanol. Appl Biochem Biotechnol 84–86:141–152

    PubMed  Google Scholar 

  • Doran JB, Foster B (2000) Ethanol production from sugar beet pulp using engineered bacteria. Int Sugar J␣102:336–340

    CAS  Google Scholar 

  • Douglas HC, Hawthorne DC (1964) Enzymatic expression and genetic linkage of genes controlling galactose utilization in Saccharomyces. Genetics 49:837–844

    PubMed  CAS  Google Scholar 

  • Eklund T (1983) The antimicrobial effect of dissociated and undissociated sorbic acid at different pH levels. J Appl Bacteriol 54:383–389

    PubMed  CAS  Google Scholar 

  • Eliasson A, Christensson C, Wahlbom CF, Hahn-Hägerdal B (2000) Anaerobic xylose fermentation by recombinant Saccharomyces cerevisiae carrying XYL1, XYL2, and XKS1 in mineral medium chemostat cultures. Appl Environ Microbiol 66:3381–3386

    PubMed  CAS  Google Scholar 

  • Fellows PJ, Worgan JT (1986) Studies on the growth of Candida utilis on d-galacturonic acid and the products of pectin hydrolysis. Enzyme Microb Technol 9:537–540

    Google Scholar 

  • Flores CL, Rodriguez C, Petit T, Gancedo C (2000) Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev 24:507–529

    PubMed  CAS  Google Scholar 

  • Fredlund E, Blank LM, Schnürer J, Sauer U, Pasoth V (2002) Oxygen- and glucose- dependent regulation of central carbon metabolism in Pichia anomala. Appl Environ Microbiol 70:5905–5911

    Google Scholar 

  • Freeman TL, San Francisco MJ (1994) Cloning of a galacturonic acid uptake gene from Erwinia chrysanthemi EC16. FEMS Microbiol Lett 118:101–106

    CAS  Google Scholar 

  • Fukazawa C (1989) Cloning of a gene encoding glucose isomerase from Streptomyces and its expression. Pat. no. JP 01137979. Appl. no. 87-295739

  • Gainvors A, Belarbi A (1995) Detection method for polygalacturonase-producing strains of Saccharomyces cerevisiae. Yeast 11:1493–1499

    PubMed  CAS  Google Scholar 

  • Galbe M, Zacchi G (2002) A review of the production of ethanol from softwood. Appl Microbiol Biotechnol 59:618–628

    PubMed  CAS  Google Scholar 

  • Gárdonyi M, Hahn-Hägerdal B (2003) The Streptomyces rubiginosus xylose isomerase is misfolded when expressed in Saccharomyces cerevisiae. Enzyme Microb Technol 32:252–259

    Google Scholar 

  • Gong CS, Chen LF, Flickinger MC, Chiang LC, Tsao GT (1981a). Production of ethanol from d-xylose by using d-xylose isomerase and yeasts. Appl Environ Microbiol 41:430–436

    CAS  Google Scholar 

  • Gong CS, McCracken LD, Tsao GT (1981b). Direct fermentation of d-xylose to ethanol by a xylose-fermentating yeast mutant, Candida sp Xf217. Biotechnol Lett 3:245–250

    CAS  Google Scholar 

  • Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD (2005) Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 1–11

  • Greene DL, Hopson JL, Li J (2002) Running into and out of oil: scenarios of global oil use and resource depletion to 2050. 1–65. 2002. U.S. Dept. of Energy. Tennessee, Knoxville, DE-AC05-00OR22725

  • Grohmann K, Bothast RJ (1994). Pectin rich residues generated by processing of citrus fruits, apples, and sugar beets. Enzymatic hydrolysis and biological conversion to value-added products. Enzymatic Conversion of Biomass for Fuels Production, Oxford University Press, Oxford, UK pp 372–390

  • Grohmann K, Manthey JA, Cameron RG, Buslig BS (1998) Fermentation of galacturonic acid and pectin-rich materials to ethanol by genetically modified strains of Erwinia. Biotechnol Lett 20:195–200

    CAS  Google Scholar 

  • Gunsalus IC, Horecker BL, Wood WA (1955) Pathways of carbohydrate metabolism in microorganisms. Bacteriol Rev 19:79–128

    PubMed  CAS  Google Scholar 

  • Hahn-Hägerdal B, Linden T, Senac T, Skoog K (1991) Ethanolic fermentation of pentoses in lignocellulose hydrolyzates. Appl Biochem Biotechnol 28–29:131–144

    PubMed  Google Scholar 

  • Harhangi HR, Akhmanova AS, Emmens R, van der Drift C, de Laat WT, van Dijken JP, Jetten MS, Pronk JT, Op den Camp HJ, (2003) Xylose metabolism in the anaerobic fungus Piromyces sp. E2 follows the bacterial pathway. Arch Microbiol 180:134–141

    PubMed  CAS  Google Scholar 

  • Hazan R, Levine A, Abeliovich H (2004) Benzoic acid, a weak organic acid food preservative, exerts specific effects on intracellular membrane trafficking pathways in Saccharomyces cerevisiae. Appl Environ Microbiol 70:4449–4457

    PubMed  CAS  Google Scholar 

  • Heipieper HJ, Weber F, Sikkema J, Keweloh H, de Bont JAM (1994) Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol 12:409–415

    CAS  Google Scholar 

  • Heredia CF, Sols A, DelaFuente G (1968) Specificity of the constitutive hexose transport in yeast. Eur J Biochem 5:321–329

    PubMed  CAS  Google Scholar 

  • Ho NWY, Chen Z, Brainard AP (1998) Genetically engineered Saccharomyces yeast capable of effective cofermentation of glucose and xylose. Appl Environ Microbiol 64:1852–1859

    PubMed  CAS  Google Scholar 

  • Ho NWY, Stevis P, Rosenfeld S, Huang JJ, Tsao GT (1984) Expression of the E. coli xylose isomerase gene by a yeast promoter. Biotechnol Bioeng Symp 13:245–250

    Google Scholar 

  • Holden H, Cooper-Key D, Carlill P, Hinchcliff H, Heath W, Black W, Ormandy DHM (1919) Petroleum executive: report of the inter- departmental committee on various matters concerning the production and utilization of alcohol for power and traction purposes. (117–124). HMSO. Cd.218

  • Holyoak CD, Stratford M, McMullin Z, Cole MB, Crimmins K, Brown AJ, Coote PJ (1996) Activity of the plasma membrane H(+)-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl Environ Microbiol 62:3158–3164

    PubMed  CAS  Google Scholar 

  • Horak J, Wolf DH (1997) Catabolite inactivation of the galactose transporter in the yeast Saccharomyces cerevisiae: ubiquitination, endocytosis, and degradation in the vacuole. J Bacteriol 179:1541–1549

    PubMed  CAS  Google Scholar 

  • Howard RL, Abotsi E, Jansen van Rensburg E, Howard S (2003) Lignocellulose biotechnology: issues of bioconversion and enzyme production. African J Biotech 2:602–619

    CAS  Google Scholar 

  • Hsiao HY, Chiang LC, Chen LF, Tsao GT (1982) Effects of borate on isomerization and yeast fermentation of high xylulose solution and acid hydrolysate of hemicellulose. Enzyme Microb Technol 4:25–31

    Google Scholar 

  • Imai T, Ohno T (1995) The relationship between viability and intracellular pH in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 61:3604–3608

    PubMed  CAS  Google Scholar 

  • Ingram LO, Aldrich HC, Borges AC, Causey TB, Martinez A, Morales F, Saleh A, Underwood SA, Yomano LP, York SW, Zaldivar J, Zhou S (1999) Enteric bacterial catalysts for fuel ethanol production. Biotechnol Prog 15:855–866

    PubMed  CAS  Google Scholar 

  • Iogen Corporation (2005) Cellulose ethanol: clean fuel for today and tomorrow. Iogen Corporation, Ottawa, Canada

    Google Scholar 

  • Jeffries TW, Jin YS (2004). Metabolic engineering for improved fermentation of pentoses by yeasts. Appl Microbiol Biotechnol 63:495–509

    PubMed  CAS  Google Scholar 

  • Jeppsson M, Johansson B, Hahn-Hägerdal B, Gorwa-Grauslund MF (2002) Reduced oxidative pentose phosphate pathway flux in recombinant xylose-utilizing Saccharomyces cerevisiae strains improves the ethanol yield from xylose. Appl Environ Microbiol 68:1604–1609

    PubMed  CAS  Google Scholar 

  • Jin YS, Ni H, Laplaza JM, Jeffries TW (2003) Optimal growth and ethanol production from xylose by recombinant Saccharomyces cerevisiae require moderate d-xylulokinase activity. Appl Environ Microbiol 69:495–503

    PubMed  CAS  Google Scholar 

  • Johnston M, Flick JS, Pexton T (1994) Multiple mechanisms provide rapid and stringent glucose repression of GAL gene expression in Saccharomyces cerevisiae. Mol Cell Biol 14:3834–3841

    PubMed  CAS  Google Scholar 

  • Johnston SA, Salmeron JM, Dincher SS (1987) Interaction of positive and negative regulatory proteins in the galactose regulon of yeast. Cell 50:143–146

    PubMed  CAS  Google Scholar 

  • Jönsson LJ, Palmqvist E, Nilvebrant NO, Hahn-Hägerdal B (1998) Detoxification of wood hydrolyzates with laccase and peroxidase from the white-rot fungus Trametes versicolor. Appl Microbiol Biotechnol 49:691–697

    Google Scholar 

  • Kamp AF, La Rivière JWM, Verhoeven W (1959) Albert Jan Kluyver his life and his work; biographical memoranda, selected papers, bibliography and addenda. NHPC, Amsterdam

    Google Scholar 

  • Karhumaa K, Hahn-Hägerdal B, Gorwa-Grauslund MF (2005) Investigation of limiting metabolic steps in the utilization of xylose by recombinant Saccharomyces cerevisiae using metabolic engineering. Yeast 22:359–368

    PubMed  CAS  Google Scholar 

  • Kastner JR, Jones WJ, Roberts RS (1999) Oxygen starvation induces cell death in Candida shehatae fermentations of d-xylose, but not d-glucose. Appl Microbiol Biotechnol 51:780–785

    PubMed  CAS  Google Scholar 

  • Keating JD, Robinson J, Cotta MA, Saddler JN, Mansfield SD (2004) An ethanologenic yeast exhibiting unusual metabolism in the fermentation of lignocellulosic hexose sugars. J Ind Microbiol Biotechnol 31:235–244

    Article  PubMed  CAS  Google Scholar 

  • Khandekar ML, Murty TS, Chittibabu P (2005) The global warming debate: a review of the state of science. Pure Appl Geophys 162:1557–1586

    Google Scholar 

  • Kilgore WW, Starr MP (1959) Catabolism of galacturonic and glucuronic acids by Erwinia carotovoro. J Biol Chem 234:2227–2235

    PubMed  CAS  Google Scholar 

  • Klare MT (2001) The new geography of conflict. Foreign Aff 80:49

    Google Scholar 

  • Klinke HB, Ahring BK, Schmidt AS, Thomsen AB (2002) Characterization of degradation products from alkaline wet oxidation of wheat straw. Bioresour Technol 82:15–26

    PubMed  CAS  Google Scholar 

  • Klinke HB, Thomsen AB, 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

    PubMed  CAS  Google Scholar 

  • Kluyver AJ (1914) Thesis: Biochemische suikerbepalingen. Delft University of Technology

  • Kluyver AJ, Schnellen Ch (1937) Über die Vergärung von Rhamnose. Enzymologia 4:7–12

    CAS  Google Scholar 

  • Kötter P, Amore R, Hollenberg CP, Ciriacy M (1990) Isolation and characterization of the Pichia stipitis xylitol dehydrogenase gene, XYL2, and construction of a xylose-utilizing Saccharomyces cerevisiae transformant. Curr Genet 18:493–500

    PubMed  Google Scholar 

  • Kötter P, Ciriacy M (1993) Xylose fermentation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 38:776–783

    Google Scholar 

  • Kou SC, Christensen MS, Cirillo VP (1970) Galactose transport in Saccharomyces cerevisiae. 2. Characteristics of galactose uptake and exchange in galacktokinaseless cells. J Bacteriol 103:671–678

    PubMed  CAS  Google Scholar 

  • Kressmann FW (1922) The manufacture of ethyl alcohol from wood waste. U.S. Dep. Agric. Bull. 983

  • Kruckeberg AL (1996) The hexose transporter family of Saccharomyces cerevisiae. Arch Microbiol 166:283–292

    PubMed  CAS  Google Scholar 

  • Kuorelahti S, Kalkkinen N, Penttilä M, Londesborough J, Richard P (2005) Identification in the mold Hypocrea jecorina of the first fungal d-galacturonic acid reductase. Biochemistry 44:11234–11240

    PubMed  CAS  Google Scholar 

  • Kurtzman CP, Dien BS (1998) Candida arabinofermentans, a new l-arabinose fermenting yeast. Antonie van Leeuwenhoek 74:237–243

    PubMed  CAS  Google Scholar 

  • Kuyper M, Harhangi HR, Stave AK, Winkler AA, Jetten MS, de Laat WT, de Ridder JJ, Op den Camp HJ, van Dijken JP, Pronk JT (2003) High-level functional expression of a fungal xylose isomerase: the key to efficient ethanolic fermentation of xylose by Saccharomyces cerevisiae? FEMS Yeast Res 4:69–78

    PubMed  CAS  Google Scholar 

  • Kuyper M, Hartog MM, Toirkens MJ, Almering MJ, Winkler AA, van Dijken JP, Pronk JT (2005a) Metabolic engineering of a xylose-isomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation. FEMS Yeast Res 5:399–409

    CAS  Google Scholar 

  • Kuyper M, Toirkens MJ, Diderich JA, Winkler AA, van Dijken JP, Pronk JT (2005b) Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain. FEMS Yeast Res 5:925–934

    CAS  Google Scholar 

  • Kuyper M, Winkler AA, van Dijken JP, Pronk JT (2004) Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: a proof of principle. FEMS Yeast Res 4:655–664

    PubMed  CAS  Google Scholar 

  • Larsson S, Cassland P, Jönsson LJ (2001a) 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

    CAS  Google Scholar 

  • Larsson S, Nilvebrant NO, Jönsson LJ (2001b). Effect of overexpression of Saccharomyces cerevisiae Pad1p on the resistance to phenylacrylic acids and lignocellulose hydrolysates under aerobic and oxygen-limited conditions. Appl Microbiol Biotechnol 57:167–174

    CAS  Google Scholar 

  • Larsson S, Palmqvist E, Hahn-Hägerdal B, Tengborg C, Stenberg K, Zacchi G, Nilvebrant NO (1999) The generation of fermentation inhibitors during dilute acid hydrolysis of softwood. Enzyme Microb Technol 24:151–159

    CAS  Google Scholar 

  • Leão C, Van Uden N (1984) Effects of ethanol and other alkanols on passive proton influx in the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 774:43–48

    PubMed  Google Scholar 

  • Lee N, Gielow W, Martin R, Hamilton E, Fowler A (1986) The organization of the araBAD operon of Escherichia coli. Gene 47:231–244

    PubMed  CAS  Google Scholar 

  • Lee RL (1997) Overview and evaluation of fuel ethanol from cellulosic biomass: technology, economics, the environment and policy. Annu Rev Energy Environ 21:403–465

    Google Scholar 

  • Leloir LF (1951) The enzymatic transformation of uridine diphosphate glucose into a galactose derivative. Arch Biochem Biophys 33:186–190

    CAS  Google Scholar 

  • Leuther KK, Johnston SA (1992) Nondissociation of GAL4 and GAL80 in vivo after galactose induction. Science 256:1333–1335

    PubMed  CAS  Google Scholar 

  • Liu ZL, Slininger PJ, Dien BS, Berhow MA, Kurtzman CP, Gorsich SW (2004) Adaptive response of yeasts to furfural and 5-hydroxymethylfurfural and new chemical evidence for HMF conversion to 2,5-bis-hydroxymethylfuran. J Ind Microbiol Biotechnol 31:345–352

    PubMed  CAS  Google Scholar 

  • Liu ZL, Slininger PJ, Gorsich SW (2005) Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 121–124:451–460

    PubMed  Google Scholar 

  • López MJ, Nichols NN, Dien BS, Moreno J, Bothast RJ (2004) Isolation of microorganisms for biological detoxification of lignocellulosic hydrolysates. Appl Microbiol Biotechnol 64:125–131

    PubMed  Google Scholar 

  • Ludovico P, Sousa MJ, Silva MT, Leão C, Côrte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147:2409–2415

    PubMed  CAS  Google Scholar 

  • Lugar R, Woolsey RJ (1999) The new petroleum. Foreign Aff 78:88–102

    Google Scholar 

  • Lynd LR (1996) Overview and evaluation of fuel ethanol from cellulosic biomass: technology, economics, the environment, and policy. Annu Rev Energy Environ 21:403–465

    Google Scholar 

  • Lynd LR, van Zyl WH, McBride JE, Laser M (2005) Consolidated bioprocessing of cellulosic biomass: an update. Curr Opin Biotechnol 16:577–583

    PubMed  CAS  Google Scholar 

  • Lynd LR, Weimer PJ, van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577

    PubMed  CAS  Google Scholar 

  • Melcher K (1997) Galactose metabolism in Saccharomyces cerevisiae: a paradigm for eukaryotic gene regulation. Yeast sugar metabolism. Technomic Publishing Inc., Lancaster PA, pp 235–269

    Google Scholar 

  • Micard V, Renard CMGC, Thibault JF (1996) Enzymatic saccharification of sugar-beet pulp. Enzyme Microb Technol 19:162–170

    CAS  Google Scholar 

  • Moes CJ, Pretorius IS, van Zyl WH (1996) Cloning and expression of the Clostridium thermosulfurogenes d-xylose isomerase gene (xylA) in Saccharomyces cerevisiae. Biotechnol Lett 18:269–274

    CAS  Google Scholar 

  • Mussatto SI, Roberto IC (2004) Alternatives for detoxification of diluted-acid lignocellulosic hydrolyzates for use in fermentative processes: a review. Bioresour Technol 93:1–10

    PubMed  CAS  Google Scholar 

  • Navarro AR (1994) Effects of furfural on ethanol fermentation by Saccharomyces cerevisiae: mathematical models. Curr Microbiol 29:87–90

    CAS  Google Scholar 

  • Nehlin JO, Carlberg M, Ronne H (1991) Control of yeast GAL genes by MIG1 repressor: a transcriptional cascade in the glucose response. EMBO J 10:3373–3377

    PubMed  CAS  Google Scholar 

  • Nichols NN, Dien BS, Guisado GM, López MJ (2005) Bioabatement to remove inhibitors from biomass-derived sugar hydrolysates. Appl Biochem Biotechnol 121:379–390

    PubMed  Google Scholar 

  • Nigam JN (2001) Ethanol production from wheat straw hemicellulose hydrolysate by Pichia stipitis. J Biotechnol 87:17–27

    PubMed  CAS  Google Scholar 

  • Nilsson A, Modig T, Gorwa-Grauslund MF, Hahn-Hägerdal B, Lidén G (2005) Furan reduction capacity of Saccharomyces cerevisiae strains in fermentation of dilute-acid hydrolysates. J Biotechnol Abstracts 118S1:S1–S189

    Google Scholar 

  • Nissen TL, Anderlund M, Nielsen J, Villadsen J, Kielland-Brandt MC (2001) Expression of a cytoplasmic transhydrogenase in Saccharomyces cerevisiae results in formation of 2-oxoglutarate due to depletion of the NADPH pool. Yeast 18:19–32

    PubMed  CAS  Google Scholar 

  • Nissen TL, Hamann CW, Kielland-Brandt MC, Nielsen J, Villadsen J (2000) Anaerobic and aerobic batch cultivations of Saccharomyces cerevisiae mutants impaired in glycerol synthesis. Yeast 16:463–474

    PubMed  CAS  Google Scholar 

  • Oh D, Hopper JE (1990) Transcription of a yeast phosphoglucomutase isozyme gene is galactose inducible and glucose repressible. Mol Cell Biol 10:1415–1422

    PubMed  CAS  Google Scholar 

  • Oosterveld A (1997) Thesis: Pectic substances from sugar beet pulp: structural features, enzymatic modification, and gel formation. Wageningen Universiteit

  • Ostergaard S, Walloe KO, Gomes SG, Olsson L, Nielsen J (2001) The impact of GAL6, GAL80, and MIG1 on glucose control of the GAL system in Saccharomyces cerevisiae. FEMS Yeast Res 1:47–55

    PubMed  CAS  Google Scholar 

  • Palmqvist E, Grage H, Meinander NQ, Hahn-Hägerdal B (1999) Main and interaction effects of acetic acid, furfural, and para-hydroxybenzoic acid on growth and ethanol productivity of yeasts. Biotechnol Bioeng 63:46–55

    PubMed  CAS  Google Scholar 

  • Palmqvist E, Hahn-Hägerdal B (2000) Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 74:25–33

    CAS  Google Scholar 

  • Palmqvist E, Hahn-Hägerdal B, Szengyel Z, Zacchi G, Rèczey K (1997) Simultaneous detoxification and enzyme production of hemicellulose hydrolysates obtained after steam pretreatment. Enzyme Microb Technol 20:286–293

    CAS  Google Scholar 

  • Pampulha ME, Loureiro-Dias MC (1989) Combined effect of acetic acid, pH and ethanol on intracellular pH of fermenting yeast. Appl Microbiol Biotechnol 31:547–550

    CAS  Google Scholar 

  • Pampulha ME, Loureiro-Dias MC (1990) Activity of glycolytic enzymes of Saccharomyces cerevisiae in the presence of acetic acid. Appl Microbiol Biotechnol 34:375–380

    CAS  Google Scholar 

  • Perez J, Munoz-Dorado J, de la Rubia T, Martinez J (2002) Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol 5:53–63

    PubMed  CAS  Google Scholar 

  • Petschacher B, Leitgeb S, Kavanagh KL, Wilson DK, Nidetzky B (2005). The coenzyme specificity of Candida tenuis xylose reductase (AKR2B5) explored by site-directed mutagenesis and X-ray crystallography. Biochem J 385:75–83

    PubMed  CAS  Google Scholar 

  • Platt A, Reece RJ (1998) The yeast galactose genetic switch is mediated by the formation of a Gal4p-Gal80p-Gal3p complex. EMBO J 17:4086–4091

    PubMed  CAS  Google Scholar 

  • Radoi F, Kishida M, Kawasaki H (2005) Characteristics of wines made by Saccharomyces mutants which produce a polygalacturonase under wine-making conditions. Biosci Biotechnol Biochem 69:2224–2226

    PubMed  CAS  Google Scholar 

  • Reifenberger E, Boles E, Ciriacy M (1997) Kinetic characterization of individual hexose transporters of Saccharomyces cerevisiae and their relation to the triggering mechanisms of glucose repression. Eur J Biochem 245:324–333

    PubMed  CAS  Google Scholar 

  • Richard P, Putkonen M, Väänänen R, Londesborough J, Penttilä M (2002) The missing link in the fungal l-arabinose catabolic pathway, identification of the l-xylulose reductase gene. Biochemistry 41:6432–6437

    PubMed  CAS  Google Scholar 

  • Richard P, Verho R, Putkonen M, Londesborough J, Penttilä M (2003) Production of ethanol from l-arabinose by Saccharomyces cerevisiae containing a fungal l-arabinose pathway. FEMS Yeast Res 3:185–189

    PubMed  CAS  Google Scholar 

  • Rigo LU, Marechal LR, Vieira MM, Veiga LA (1985) Oxidative pathway for l-rhamnose degradation in Pullularia pullulans. Can J Microbiol 31:817–822

    CAS  Google Scholar 

  • Rizzi M, Erlemann P, Buithanh NA and Dellweg H (1988) Xylose fermentation by yeasts. 4. Purification and kinetic-studies of xylose reductase from Pichia stipitis. Appl Microbiol Biotechnol 29:148–154

    Article  CAS  Google Scholar 

  • Ronnow B, Olsson L, Nielsen J, Mikkelsen JD (1999) Derepression of galactose metabolism in melibiase producing bakers’ and distillers’ yeast. J Biotechnol 72:213–228

    PubMed  CAS  Google Scholar 

  • Russell JB (1992) Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling. J Appl Bacteriol 73:363–370

    CAS  Google Scholar 

  • Sarthy AV, McConaughy BL, Lobo Z, Sundstrom JA, Furlong CE Hall BD (1987) Expression of the Escherichia coli xylose isomerase gene in Saccharomyces cerevisiae. Appl Environ Microbiol 53:1996–2000

    PubMed  CAS  Google Scholar 

  • Sauer U (2001) Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 73:129–169

    PubMed  CAS  Google Scholar 

  • Sawada H, Takagi Y (1964) The metabolism of l-rhamnose in Escherichia coli III l-rhamnulose-phosphate aldolase. Biochim Biophys Acta 92:26–32

    PubMed  CAS  Google Scholar 

  • Schloss PD, Handelsman J (2003) Biotechnological prospects from metagenomics. Curr Opin Biotechnol 14:303–310

    PubMed  CAS  Google Scholar 

  • Sedlak M, Ho NWY (2001) Expression of E. coli araBAD operon encoding enzymes for metabolizing l-arabinose in Saccharomyces cerevisiae. Enzyme Microb Technol 28:16–24

    PubMed  CAS  Google Scholar 

  • Sedlak M, Ho NWY (2004) Production of ethanol from cellulosic biomass hydrolysates using genetically engineered Saccharomyces yeast capable of cofermenting glucose and xylose. Appl Biochem Biotechnol 114:403–416

    Google Scholar 

  • Serrat M, Bermúdez RC, Villa TG (2004) Polygalacturonase and ethanol production in Kluyveromyces marxianus: potential use of polygalacturonase in foodstuffs. Appl Biochem Biotechnol 117:49–64

    PubMed  CAS  Google Scholar 

  • Sirotek K, Slováková L, Kopecný J, Marounek M (2004) Fermentation of pectin and glucose, and activity of pectin-degrading enzymes in the rabbit caecal bacterium Bacteroides caccae. Lett Appl Microbiol 38:327–332

    PubMed  CAS  Google Scholar 

  • Sjöström E (1991) Carbohydrate degradation products from alkaline treatment of biomass. Biomass Bioenergy 1:61–64

    Google Scholar 

  • Slininger PJ, Bothast RJ, Vancauwenberge JE, Kurtzman CP (1982) Conversion of d-xylose to ethanol by the yeast Pachysolen tannophilus. Biotechnol Bioeng 24:371–384

    CAS  PubMed  Google Scholar 

  • Sonderegger M, Jeppsson M, Larsson C, Gorwa-Grauslund MF, Boles E, Olsson L, Spencer-Martins I, Hahn-Hägerdal B, Sauer U (2004) Fermentation performance of engineered and evolved xylose-fermenting Saccharomyces cerevisiae strains. Biotechnol Bioeng 87:90–98

    PubMed  CAS  Google Scholar 

  • Sonderegger M, Sauer U (2003) Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl Environ Microbiol 69:1990–1998

    PubMed  CAS  Google Scholar 

  • Taherzadeh MJ, Gustafsson L, Niklasson C, Lidén G (1999) Conversion of furfural in aerobic and anaerobic batch fermentation of glucose by Saccharomyces cerevisiae. J Biosci Bioeng 87:169–174

    PubMed  CAS  Google Scholar 

  • Taherzadeh MJ, Gustafsson L, Niklasson C, Lidén G (2000) Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 53:701–708

    PubMed  CAS  Google Scholar 

  • Taherzadeh MJ, Niklasson C, Lidén G, Eklund R, Gustafsson L (1997) Characterization and fermentation of dilute-acid hydrolyzates from wood. Ind Eng Chem Res 36:4659–4665

    CAS  Google Scholar 

  • Takagi Y, Sawada H (1964a) The metabolism of l-rhamnose in Escherichia coli I. l-rhamnose isomerase. Biochim Biophys Acta 92:10–17

    CAS  Google Scholar 

  • Takagi Y, Sawada H (1964b) The metabolism of l-rhamnose in Escherichia coli II l-rhamnulose kinase. Biochim Biophys Acta 92:18–25

    CAS  Google Scholar 

  • Thakur BR, Singh RK, Handa AK (1997) Chemistry and uses of pectin – a review. Crit Rev Food Sci Nutr 37:47–73

    Article  PubMed  CAS  Google Scholar 

  • Thomas KC, Hynes SH, Ingledew WM (2001) Effect of lactobacilli on yeast growth, viability and batch and semi-continuous alcoholic fermentation of corn mash. J Appl Microbiol 90:819–828

    PubMed  CAS  Google Scholar 

  • Toivari MH, Aristidou A, Ruohonen L, Penttilä M (2001) Conversion of xylose to ethanol by recombinant Saccharomyces cerevisiae: importance of xylulokinase (XKS1) and oxygen availability. Metab Eng 3:236–249

    PubMed  CAS  Google Scholar 

  • Toivola A, Yarrow D, Van den Bosch E, van Dijken JP, Scheffers WA (1984) Ethanolic fermentation of d-xylose by yeasts. Appl Environ Microbiol 47:1221–1223

    PubMed  CAS  Google Scholar 

  • Twerdochlib AL, Pedrosa FO, Funayama S, Rigo LU (1994) l-rhamnose metabolism in Pichia stipitis and Debaryomyces polymorphus. Can J Microbiol 40:896–902

    Article  CAS  Google Scholar 

  • van Dijken JP, Scheffers WA (1986) Redox balances in the metabolism of sugars by yeasts. FEMS Microbiol Rev 32:199–224

    Google Scholar 

  • van Rooyen R, Hahn-Hägerdal B, La Grange DC, van Zyl WH (2005) Construction of cellobiose-growing and fermenting Saccharomyces cerevisiae strains. J Biotechnol 120:284–295

    PubMed  Google Scholar 

  • Verduyn C, Postma E, Scheffers WA, van Dijken JP (1990a) Energetics of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136:405–412

    CAS  Google Scholar 

  • Verduyn C, Postma E, Scheffers WA, van Dijken JP (1990b) Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136:395–403

    CAS  Google Scholar 

  • Verduyn C, Postma E, Scheffers WA, van Dijken JP (1992) Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8:501–517

    PubMed  CAS  Google Scholar 

  • Verho R, Londesborough J, Penttilä M, Richard P (2003) Engineering redox cofactor regeneration for improved pentose fermentation in Saccharomyces cerevisiae. Appl Environ Microbiol 69:5892–5897

    PubMed  CAS  Google Scholar 

  • Verho R, Putkonen M, Londesborough J, Penttilä M, Richard P (2004) A novel NADH-linked l-xylulose reductase in the l-arabinose catabolic pathway of yeast. J Biol Chem 279:14746–14751

    PubMed  CAS  Google Scholar 

  • Vincent SF, Bell PJ, Bissinger P, Nevalainen KM (1999) Comparison of melibiose utilizing baker’s yeast strains produced by genetic engineering and classical breeding. Lett Appl Microbiol 28:148–152

    PubMed  CAS  Google Scholar 

  • Visser J, Van Rooijen R, Dijkema C, Swart K, Sealy-Lewis HM (1988) Glycerol uptake mutants of the hyphal fungus Aspergillus nidulans. J Gen Microbiol 134:655–659

    PubMed  CAS  Google Scholar 

  • Visser W, Scheffers WA, Batenburg-van der Vegte WH, van Dijken JP (1990) Oxygen requirements of yeasts. Appl Environ Microbiol 56:3785–3792

    PubMed  CAS  Google Scholar 

  • Wahlbom CF, Hahn-Hägerdal B (2002) Furfural, 5-hydroxymethyl furfural, and acetoin act as external electron acceptors during anaerobic fermentation of xylose in recombinant Saccharomyces cerevisiae. Biotechnol Bioeng 78:172–178

    PubMed  CAS  Google Scholar 

  • Walfridsson M, Bao X, Anderlund M, Lilius G, Bulow L, Hahn-Hägerdal B (1996) Ethanolic fermentation of xylose with Saccharomyces cerevisiae harboring the Thermus thermophilus xylA gene, which expresses an active xylose (glucose) isomerase. Appl Environ Microbiol 62:4648–4651

    PubMed  CAS  Google Scholar 

  • Walfridsson M, Hallborn J, Penttilä M, Keränen S, Hahn-Hägerdal B (1995) Xylose-metabolizing Saccharomyces cerevisiae strains overexpressing theTKL1 and TAL1 genes encoding the pentose phosphate pathway enzymes transketolase and transaldolase. Appl Environ Microbiol 61:4184–4190

    PubMed  CAS  Google Scholar 

  • Wang PY, Schneider H (1980) Growth of yeasts on d-xylulose. Can J Microbiol 26:1165–1168

    Article  PubMed  CAS  Google Scholar 

  • Wilson DM, Ajl S (1955) The metabolism of l-rhamnose by Escherichia coli. Biochim Biophys Acta 17:289

    PubMed  CAS  Google Scholar 

  • Wilson DM, Ajl S (1957a) Metabolism of l-rhamnose by Escherichia coli. I. l-rhamnose isomerase. J Bacteriol 73:410–414

    CAS  Google Scholar 

  • Wilson DM, Ajl S (1957b) Metabolism of l-rhamnose by Escherichia coli. II. The phosphorylation of l-rhamnulose. J Bacteriol 73:415–420

    CAS  Google Scholar 

  • Witteveen CFB, Busink R, Vandevondervoort P, Dijkema C, Swart K, Visser J (1989) l-arabinose and d-xylose catabolism in Aspergillus niger. J Gen Microbiol 135:2163–2171

    CAS  Google Scholar 

  • Witteveen CFB, Weber F, Busink R, Visser J (1994) Isolation and characterization of two xylitol dehydrogenases from Aspergillus niger. Microbiology 140:1679–1685

    Article  CAS  Google Scholar 

  • Wu YB, Reece RJ, Ptashne M (1996) Quantitation of putative activator-target affinities predicts transcriptional activating potentials. EMBO J 15:3951–3963

    PubMed  CAS  Google Scholar 

  • Yoon SH, Mukerjea R, Robyt JF (2003) Specificity of yeast (Saccharomyces cerevisiae) in removing carbohydrates by fermentation. Carbohydr Res 338:1127–1132

    PubMed  CAS  Google Scholar 

  • Zaldivar J, Nielsen J, Olsson L (2001) Fuel ethanol production from lignocellulose: a challenge for metabolic engineering and process integration. Appl Microbiol Biotechnol 56:17–34

    PubMed  CAS  Google Scholar 

  • Zandleven J, Beldman G, Bosveld M, Benen J, Voragen A (2005) Mode of action of xylogalacturonan hydrolase towards xylogalacturonan and xylogalacturonan oligosaccharides. Biochem J 387:719–725

    PubMed  CAS  Google Scholar 

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Acknowledgements

The research group of JTP is part of the Kluyver Centre for Genomics of Industrial Fermentation, which is supported by the Netherlands Genomics Initiative. HWW is supported by the B-Basic Programme, JvdB by the IOP Genomics Programme and DAA by Tate & Lyle Ingredients Americas.

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  1. Department of Biotechnology, Delft University of Technology, Julianalaan 67, 2628, BC, Delft, The Netherlands

    Antonius J. A. van Maris, Derek A. Abbott, Eleonora Bellissimi, Joost van den Brink, Marko Kuyper, Marijke A. H. Luttik, H. Wouter Wisselink, W. Alexander Scheffers, Johannes P. van Dijken & Jack T. Pronk

  2. Bird Engineering B.V., Westfrankelandsedijk 1, 3115, Schiedam, HG, The Netherlands

    Johannes P. van Dijken

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van Maris, A.J.A., Abbott, D.A., Bellissimi, E. et al. Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Antonie van Leeuwenhoek 90, 391–418 (2006). https://doi.org/10.1007/s10482-006-9085-7

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