Abstract
The fermentation of xylose is essential for the bioconversion of lignocellulose to fuels and chemicals, but wild-type strains of Saccharomyces cerevisiae do not metabolize xylose, so researchers have engineered xylose metabolism in this yeast. Glucose transporters mediate xylose uptake, but no transporter specific for xylose has yet been identified. Over-expressing genes for aldose (xylose) reductase, xylitol dehydrogenase and moderate levels of xylulokinase enable xylose assimilation and fermentation, but a balanced supply of NAD(P) and NAD(P)H must be maintained to avoid xylitol production. Reducing production of NADPH by blocking the oxidative pentose phosphate cycle can reduce xylitol formation, but this occurs at the expense of xylose assimilation. Respiration is critical for growth on xylose by both native xylose-fermenting yeasts and recombinant S, cerevisiae. Anaerobic growth by recombinant mutants has been reported. Reducing the respiration capacity of xylose-metabolizing yeasts increases ethanol production. Recently, two routes for arabinose metabolism have been engineered in S. cerevisiae and adapted strains of Pichia stipitis have been shown to ferment hydrolysates with ethanol yields of 0.45 g g−1 sugar consumed, so commercialization seems feasible for some applications.
Similar content being viewed by others
References
Abbi M, Kuhad RC, Singh A (1996) Fermentation of xylose and rice straw hydrolysate to ethanol by Candida shehatae NCL-3501. J Ind Microbiol 17:20–23
Aguilar R, Ramirez JA, Garrote G, Vazquez M (2002) Kinetic study of the acid hydrolysis of sugar cane bagasse. J Food Eng 55:309–318
Amore R, Kötter P, Kuster C, Ciriacy M, Hollenberg CP (1991) Cloning and expression in Saccharomyces cerevisiae of the NAD(P)H-dependent xylose reductase-encoding gene (XYL1) from the xylose-assimilating yeast Pichia stipitis. Gene 109:89–97
Aristidou A, Penttilä M (2000) Metabolic engineering applications to renewable resource utilization. Curr Opin Biotechnol 11:187–198
Bao X, Gao D, Qu Y, Wang Z, Walfridssion M, Hahn-Hägerdal B (1997) Effect on product formation in recombinant Saccharomyces cerevisiae strains expressing different levels of xylose metabolic genes. Chin J Biotechnol 13:225–231
Basaran P, Basaran N, Hang YD (2000) Isolation and characterization of Pichia stipitis mutants with enhanced xylanase activity. World J Microbiol Biotechnol 16:545–550
Becker J, Boles E (2003) A modified Saccharomyces cerevisiae strain that consumes l-arabinose and produces ethanol. Appl Environ Microbiol 69:4144–4150
Billard P, Menart S, Fleer R, Bolotin-Fukuhara M (1995) Isolation and characterization of the gene encoding xylose reductase from Kluyveromyces lactis. Gene 162:93–97
Boles E, Hollenberg CP (1997) The molecular genetics of hexose transport in yeasts. FEMS Microbiol Rev 21:85–111
Bruinenberg PM (1986) The NADP(H) redox couple in yeast metabolism. Antonie Van Leeuwenhoek 52:411–429
Bruinenberg PM, Debot PHM, Dijken JP van, Scheffers WA (1983a) The role of redox balances in the anaerobic fermentation of xylose by yeasts. Eur J Appl Microbiol Biotechnol 18:287–292
Bruinenberg PM, Dijken JP van, Scheffers WA (1983b) A theoretical analysis of NADPH production and consumption in yeasts. J Gen Microbiol 129:953–964
Bruinenberg PM, Debot PHM, Dijken JP van, Scheffers WA (1984) NADH-linked aldose reductase—the key to anaerobic alcoholic fermentation of xylose by yeasts. Appl Microbiol Biotechnol 19:256–260
Bruinenberg PM, Jonker R, Dijken JP van, Scheffers WA (1985) Utilization of formate as an additional energy source by glucose-limited chemostat cultures of Candida utilis CBS-621 and Saccharomyces cerevisiae CBS-8066—evidence for the absence of transhydrogenase activity in yeasts. Arch Microbiol 142:302–306
Buziol S, et al (2002) Determination of in vivo kinetics of the starvation-induced Hxt5 glucose transporter of Saccharomyces cerevisiae. FEMS Yeast Res 2:283–291
Chang SF, Ho NW (1988) Cloning the yeast xylulokinase gene for the improvement of xylose fermentation. Appl Biochem Biotechnol 17:313–318
Chang YD, Dickson RC (1988) Primary structure of the lactose permease gene from the yeast Kluyveromyces lactis—presence of an unusual transcript structure. J Biol Chem 263:16696–16703
Chen RF, Wu ZW, Lee YY (1998) Shrinking-bed model for percolation process applied to dilute-acid pretreatment hydrolysis of cellulosic biomass. Appl Biochem Biotechnol 70/72:37–49
Cho JY, Jeffries TW (1998) Pichia stipitis genes for alcohol dehydrogenase with fermentative and respiratory functions. Appl Environ Microbiol 64:1350–1358
Cho JY, Jeffries TW (1999) Transcriptional control of ADH genes in the xylose-fermenting yeast Pichia stipitis. Appl Environ Microbiol 65:2363–2368
Christensen B, Gombert AK, Nielsen J (2002) Analysis of flux estimates based on (13)C-labelling experiments. Eur J Biochem 269:2795–2800
Claassen PAM, et al (1999) Utilisation of biomass for the supply of energy carriers. Appl Microbiol Biotechnol 52:741–755
Dahn KM, Davis BP, Pittman PE, Kenealy WR, Jeffries TW (1996) Increased xylose reductase activity in the xylose-fermenting yeast Pichia stipitis by overexpression of XYL1. Appl Biochem Biotechnol 57/58:267–276
Den Haan R, van Zyl WH (2001) Differential expression of the Trichoderma reesei beta-xylanase II (xyn2) gene in the xylose-fermenting yeast Pichia stipitis. Appl Microbiol Biotechnol 57:521–527
Deng XX, Ho NW (1990) Xylulokinase activity in various yeasts including Saccharomyces cerevisiae containing the cloned xylulokinase gene. Appl Biochem Biotechnol 24/25:193–199
Dequin S (2001) The potential of genetic engineering for improving brewing, wine making and baking yeasts. Appl Microbiol Biotechnol 56:577–588
Diderich JA, Schuurmans JM, Van Gaalen MC, Kruckeberg AL, Van Dam K (2001) Functional analysis of the hexose transporter homologue HXT5 in Saccharomyces cerevisiae. Yeast 18:1515–1524
Dien BS, Kurtzman CP, Saha BC, Bothast RJ (1996) Screening for l-arabinose fermenting yeasts. Appl Biochem Biotechnol 57/58:233–242
Does AL, Bisson LF (1989) Characterization of xylose uptake in the yeasts Pichia heedii and Pichia stipitis. Appl Environ Microbiol 55:159–164
Du Preez JC, Walt JP van der (1983) Fermentation of d-xylose to ethanol by a strain of Candida shehatae. Biotechnol Lett 5:357–362
Du Preez JC, Prior BA, Monteiro AMT (1984) The effect of aeration on xylose fermentation by Candida shehatae and Pachysolen tannophilus—a comparative study. Appl Microbiol Biotechnol 19:261–266
Du Preez JC, Bosch M, Prior BA (1986) Xylose fermentation by Candida shehatae and Pichia stipitis—effects of pH, temperature and substrate concentration. Enzyme Microb Technol 8:360–364
Eliasson A, et al (2000a) Xylulose fermentation by mutant and wild-type strains of Zygosaccharomyces and Saccharomyces cerevisiae. Appl Microbiol Biotechnol 53:376–382
Eliasson A, Christensson C, Wahlbom CF, Hahn-Hägerdal B (2000b) Anaerobic xylose fermentation by recombinant Saccharomyces cerevisiae carrying XYL1, XYL2, and XKS1 in mineral medium chemostat cultures. Appl Environ Microbiol 66:3381–3386
Fiaux J, Cakar ZP, Sonderegger M, Wuthrich K, Szyperski T, Sauer U (2003) Metabolic flux profiling of the yeasts Saccharomyces cerevisiae and Pichia stipitis. Eukaryot Cell 2:170–180
Flores CL, Rodriguez C, Petit T, Gancedo C (2000) Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev 24:507–529
Galbe M, Zacchi G (2002) A review of the production of ethanol from softwood. Appl Microbiol Biotechnol 59:618–628
Gong CS, Cao NJ, Du J, Tsao GT (1999) Ethanol production from renewable resources. Adv Biochem Eng Biotechnol 65:207–241
Gupthar AS (1992) Segregation of altered parental properties in fusions between Saccharomyces cerevisiae and the d-xylose fermenting yeasts Candida shehatae and Pichia stipitis. Can J Microbiol 38:1233–1237
Hahn-Hägerdal B, Wahlbom CF, Gardonyi M, Zyl WH van, Cordero Otero RR, Jönsson LJ (2001) Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Adv Biochem Eng Biotechnol 73:53–84
Hallborn J, et al (1991) Xylitol production by recombinant Saccharomyces cerevisiae. Biotechnology 9:1090–1095
Hallborn J, Gorwa MF, Meinander N, Penttilä M, Keranen S, Hahn-Hägerdal B (1994) The influence of cosubstrate and aeration on xylitol formation by recombinant Saccharomyces cerevisiae expressing the XYL1 gene. Appl Microbiol Biotechnol 42:326–333
Hallborn J, Walfridsson M, Penttilä M, Keranen S, Hahn-Hägerdal B (1995) A short-chain dehydrogenase gene from Pichia stipitis having d-arabinitol dehydrogenase activity. Yeast 11:839–847
Hamacher T, Becker J, Gardonyi M, Hahn-Hägerdal B, Boles E (2002) Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 148:2783–2788
Handumrongkul C, Ma DP, Silva JL (1998) Cloning and expression of Candida guilliermondii xylose reductase gene (xyl1) in Pichia pastoris. Appl Microbiol Biotechnol 49:399–404
Harhangi HR, et al (2003) Xylose metabolism in the anaerobic fungus Piromyces sp. strain E2 follows the bacterial pathway. Arch Microbiol 180:134–141
Hespell RB (1998) Extraction and characterization of hemicellulose from the corn fiber produced by corn wet-milling processes. J Agric Food Chem 46:2615–2619
Hinmann ND, Wright JD, Hoagland W, Wyman CE (1989) Xylose fermentation—an economic analysis. Appl Biochem Biotechnol 20/21:391–401
Ho NW, Tsao GT (1993) Recombinant yeasts for effective fermentation of glucose and xylose. US Patent 5789210
Ho NW, Lin FP, Huang S, Andrews PC, Tsao GT (1990) Purification, characterization, and amino terminal sequence of xylose reductase from Candida shehatae. Enzyme Microb Technol 12:33–39
Ho NW, Chen Z, Brainard AP (1998) Genetically engineered Saccharomyces yeast capable of effective co-fermentation of glucose and xylose. Appl Environ Microbiol 64:1852–1859
Ho NW, Chen Z, Brainard AP, Sedlak M (1999) Successful design and development of genetically engineered Saccharomyces yeasts for effective co-fermentation of glucose and xylose from cellulosic biomass to fuel ethanol. Adv Biochem Eng Biotechnol 65:163–192
Hohmann S, Neves MJ, Koning W de, Alijo R, Ramos J, Thevelein JM (1993) The growth and signalling defects of the ggs1 (fdp1/byp1) deletion mutant on glucose are suppressed by a deletion of the gene encoding hexokinase PII. Curr Genet 23:281–289
Hohmann S, Bell W, Neves MJ, Valckx D, Thevelein JM (1996) Evidence for trehalose-6-phosphate-dependent and -independent mechanisms in the control of sugar influx into yeast glycolysis. Mol Microbiol 20:981–991
Jeffries T (1981) Conversion of xylose to ethanol under aerobic conditions. Biotechnol Lett 3:213–218
Jeffries TW (1982) A comparison of Candida tropicalis and Pachysolen tannophilus for conversion of xylose to ethanol. Biotechnol Bioeng Symp 12:103–110
Jeffries T (1983) Utilization of xylose by bacteria yeasts and fungi. Adv Biochem Eng Biotechnol 27:1–32
Jeffries TW (1985) Emerging technology for fermenting d-xylose. Trends Biotechnol 3:208–212
Jeffries TW, Jin YS (2000) Ethanol and thermotolerance in the bioconversion of xylose by yeasts. Adv Appl Microbiol 2000:221–268
Jeffries TW, Kurtzman CP (1994) Strain selection, taxonomy, and genetics of xylose fermenting yeasts. Enzyme Microb Technol 16:922–932
Jeffries TW, Shi NQ (1999) Genetic engineering for improved xylose fermentation by yeasts. Adv Biochem Eng Biotechnol 65:117–161
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
Jin YS (2002) Metabolic engineering of xylose fermentation in Saccharomyces cerevisiae. PhD thesis, University of Wisconsin, Madison
Jin YS, Jeffries TW (2003) Changing flux of xylose metabolites by altering expression of xylose reductase and xylitol dehydrogenase in recombinant Saccharomyces cerevisiae. Appl Biochem Biotechnol 105/108:277–285
Jin YS, Jones S, Shi NQ, Jeffries TW (2002) Molecular cloning of XYL3 (d-xylulokinase) from Pichia stipitis and characterization of its physiological function. Appl Environ Microbiol 68:1232–1239
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
Johansson B, Christensson C, Hobley T, Hahn-Hägerdal B (2001) Xylulokinase overexpression in two strains of Saccharomyces cerevisiae also expressing xylose reductase and xylitol dehydrogenase and its effect on fermentation of xylose and lignocellulosic hydrolysate. Appl Environ Microbiol 67:4249–4255
Jönsson LJ, Palmqvist E, Nilvebrant NO, Hahn-Hägerdal B (1998) Detoxification of wood hydrolysates with laccase and peroxidase from the white-rot fungus Trametes versicolor. Appl Microbiol Biotechnol 49:691–697
Kastner JR, Jones WJ, Roberts RS (1998) Simultaneous utilization of glucose and d-xylose by Candida shehatae in a chemostat. J Ind Microbiol Biotechnol 20:339–343
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
Kheshgi HS, Prince RC, Marland G (2000) The potential of biomass fuels in the context of global climate change: focus on transportation fuels. Annu Rev Energy Environ 25:199–244
Kilian SG, Uden N van (1988) Transport of xylose and glucose in the xylose-fermenting yeast Pichia stipitis. Appl Microbiol Biotechnol 27:545–548
Kim KH, Tucker MP, Keller FA, Aden A, Nguyen QA (2001) Continuous countercurrent extraction of hemicellulose from pretreated wood residues. Appl Biochem Biotechnol 91/93:253–267
Kim YS, Kim SY, Kim JH, Kim SC (1999) Xylitol production using recombinant Saccharomyces cerevisiae containing multiple xylose reductase genes at chromosomal delta-sequences. J Biotechnol 67:159–171
Kordowska-Wiater M, Targonski Z (2001) Application of Saccharomyces cerevisiae and Pichia stipitis karyoductants to the production of ethanol from xylose. Acta Microbiol Pol 50:291–299
Kötter P, Ciriacy M (1993) Xylose fermentation by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 38:776–783
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
Kou SC, Christensen MS, Cirillo VP (1970) Galactose transport in Saccharomyces cerevisiae. II. Characteristics of galactose uptake and exchange in galactokinaseless cells. J Bacteriol 103:671–678
Krishnan MS, Ho NWY, Tsao GT (1999) Fermentation kinetics of ethanol production from glucose and xylose by recombinant Saccharomyces 1400 (pLNH33). Appl Biochem Biotechnol 77/79:373–388
Kruckeberg AL (1996) The hexose transporter family of Saccharomyces cerevisiae. Arch Microbiol 166:283–292
Kuyper M, et al (2003) High-level functional expression of a fungal xylose isomerase: the key to efficient ethanolic fermentation of xylose by Saccharomyces cerevisiae? FEMS Yeast Res (in press)
La Grange DC, Pretorius IS, Claeyssens M, Zyl WH van (2001) Degradation of xylan to d-xylose by recombinant Saccharomyces cerevisiae coexpressing the Aspergillus niger beta-xylosidase (xlnD) and the Trichoderma reesei xylanase II (xyn2) genes. Appl Environ Microbiol 67:5512–5519
Lagunas R (1993) Sugar transport in Saccharomyces cerevisiae. FEMS Microbiol Rev 104:229–242
Larsson S, Cassland P, Jönsson 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
Lawford HG, Rousseau JD (1993) Production of ethanol from pulp-mill hardwood and softwood spent sulfite liquors by genetically engineered Escherichia coli. Appl Biochem Biotechnol 39:667–685
Lee H, Biely P, Latta RK, Barbosa MFS, Schneider H (1986) Utilization of xylan by yeasts and Its conversion to ethanol by Pichia stipitis strains. Appl Environ Microbiol 52:320–324
Lee WJ, Kim MD, Ryu YW, Bisson LF, Seo JH (2002) Kinetic studies on glucose and xylose transport in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 60:186–191
Ligthelm ME, Prior BA, Du Preez JC (1988) The induction of d-xylose catabolizing enzymes in Pachysolen tannophilus and the relationship to anaerobic d-xylose fermentation. Biotechnol Lett 10:207–212
Lönn A, Gardonyi M, Zyl W van, Hahn-Hägerdal B, Otero RC (2002) Cold adaptation of xylose isomerase from Thermus thermophilus through random PCR mutagenesis. Gene cloning and protein characterization. Eur J Biochem 269:157–163
Lucas C, Uden N van (1986) Transport of hemicellulose monomers in the xylose-fermenting yeast Candida shehatae. Appl Microbiol Biotechnol 23:491–495
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
Maier A, Volker B, Boles E, Fuhrmann GF (2002) Characterisation of glucose transport in Saccharomyces cerevisiae with plasma membrane vesicles (countertransport) and intact cells (initial uptake) with single Hxt1, Hxt2, Hxt3, Hxt4, Hxt6, Hxt7 or Gal2 transporters. FEMS Yeast Res 2:539–550
Maleszka R, Schneider H (1982) Fermentation of d-xylose, xylitol, and d-xylulose by yeasts. Can J Microbiol 28:360–363
Maleszka R, Schneider H (1984) Involvement of oxygen and mitochondrial function in the metabolism of d-xylulose by Saccharomyces cerevisiae. Arch Biochem Biophys 228. 228:22–30
McMillan JD (1997) Bioethanol production: status and prospects. Renewable Energy 10:295–302
Meinander NQ, Hahn-Hägerdal B (1997) Influence of cosubstrate concentration on xylose conversion by recombinant, XYL1-expressing Saccharomyces cerevisiae: a comparison of different sugars and ethanol as cosubstrates. Appl Environ Microbiol 63:1959–1964
Meinander NQ, Boels I, Hahn-Hägerdal B (1999) Fermentation of xylose/glucose mixtures by metabolically engineered Saccharomyces cerevisiae strains expressing XYL1 and XYL2 from Pichia stipitis with and without overexpression of TAL1. Bioresour Technol 68:79–87
Metzger MH, Hollenberg CP (1994) Isolation and characterization of the Pichia stipitis transketolase gene and expression in a xylose-utilising Saccharomyces cerevisiae transformant. Appl Microbiol Biotechnol 42:319–325
Michal G (1999) Biochemical pathways. Wiley, New York
Moniruzzaman M, et al (1997) Fermentation of corn fibre sugars by an engineered xylose utilizing Saccharomyces yeast strain. World J Microbiol Biotechnol 13:341–346
Morosoli R, Zalce E, Durand S (1993) Secretion of a Cryptococcus albidus xylanase in Pichia stipitis resulting in a xylan fermenting transformant. Curr Genet 24:94–99
Nigam JN (2001a) Development of xylose-fermenting yeast Pichia stipitis for ethanol production through adaptation on hardwood hemicellulose acid prehydrolysate. J Appl Microbiol 90:208–215
Nigam JN (2001b) Ethanol production from hardwood spent sulfite liquor using an adapted strain of Pichia stipitis. J Ind Microbiol Biotechnol 26:145–150
Nissen TL, Schulze U, Nielsen J, Villadsen J (1997) Flux distributions in anaerobic, glucose-limited continuous cultures of Saccharomyces cerevisiae. Microbiology 143:203–218
Olsson L, Hahn-Hägerdal B (1996) Fermentation of lignocellulosic hydrolysates for ethanol production. Enzyme Microb Technol 18:312–331
Ostergaard S, Olsson L, Nielsen J (2000) Metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 64:34–50
Ozcan S, Kötter P, Ciriacy M (1991) Xylan-hydrolyzing enzymes of the yeast Pichia stipitis. Appl Microbiol Biotechnol 36:190–195
Park NH, Yoshida S, Takakashi A, Kawabata Y, Sun HJ, Kusakabe I (2001) A new method for the preparation of crystalline l-arabinose from arabinoxylan by enzymatic hydrolysis and selective fermentation with yeast. Biotechnol Lett 23:411–416
Passoth V, Cohn M, Schafer B, Hahn-Hagerdal B, Klinner U (2003) Analysis of the hypoxia-induced ADH2 promoter of the respiratory yeast Pichia stipitis reveals a new mechanism for sensing of oxygen limitation in yeast. Yeast 20:39–51
Pettersen RC (1984) The chemical composition of wood. Adv Chem Ser 1984:57–126
Prior BA, Kilian SG, Dupreez JC (1989) Fermentation of d-xylose by the yeasts Candida shehatae and Pichia stipitis—prospects and problems. Process Biochem 24:21–32
Rees DA (1977) Polysaccharide shapes. Wiley, New York
Richard P, Toivari MH, Penttilä M (2000) The role of xylulokinase in Saccharomyces cerevisiae xylulose catabolism. FEMS Microbiol Lett 190:39–43
Richard P, Londesborough J, Putkonen M, Kalkkinen N, Penttilä M (2001) Cloning and expression of a fungal l-arabinitol 4-dehydrogenase gene. J Biol Chem 276:40631–40637
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
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 (in press)
Rizzi M, Erlemann P, Buithanh NA, Dellweg H (1988) Xylose fermentation by yeasts 4. Purification and kinetic studies of xylose reductase from Pichia stipitis. Appl Microbiol Biotechnol 29:148–154
Roca C, Olsson L (2003) Increasing ethanol productivity during xylose fermentation by cell recycling of recombinant Saccharomyces cerevisiae. Appl Microbiol Biotechnol 60:560–563
Rodrigues DC, Da Silva SS, Almeida ESJB, Vitolo M (2002) Xylose reductase activity of Candida guilliermondii during xylitol production by fed-batch fermentation: selection of process variables. Appl Biochem Biotechnol 98/100:875–883
Rodriguez-Pena JM, Cid VJ, Arroyo J, Nombela C (1998) The YGR194c (XKS1) gene encodes the xylulokinase from the budding yeast Saccharomyces cerevisiae. FEMS Microbiol Lett 162:155–160
Saha BC, Bothast RJ (1999) Pretreatment and enzymatic saccharification of corn fiber. Appl Biochem Biotechnol 76:65–77
Saha BC, Dien BS, Bothast RJ (1998) Fuel ethanol production from corn fiber—current status and technical prospects. Appl Biochem Biotechnol 70/72:115–125
Sanchez S, Bravo V, Castro E, Moya AJ, Camacho F (1998) The production of xylitol from d-xylose by fermentation with Hansenula polymorpha. Appl Microbiol Biotechnol 50:608–611
Sanchez S, Bravo V, Castro E, Moya AJ, Camacho F (2002) The fermentation of mixtures Of d-glucose and d-xylose by Candida shehatae, Pichia stipitis or Pachysolen tannophilus to produce ethanol. J Chem Technol Biotechnol 77:641–648
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
Schneider H, Wang PY, Chan YK, Maleszka R (1981) Conversion of d-xylose into ethanol by the yeast Pachysolen tannophilus. Biotechnol Lett 3:89–92
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
Shi NQ, Jeffries TW (1998) Anaerobic growth and improved fermentation of Pichia stipitis bearing a URA1 gene from Saccharomyces cerevisiae. Appl Microbiol Biotechnol 50:339–345
Shi NQ, Davis B, Sherman F, Cruz J, Jeffries TW (1999) Disruption of the cytochrome c gene in xylose-utilizing yeast Pichia stipitis leads to higher ethanol production. Yeast 15:1021–1030
Shi NQ, et al (2000) Characterization and complementation of a Pichia stipitis mutant unable to grow on d-xylose or l-arabinose. Appl Biochem Biotechnol 84-86:201–216
Shi NQ, Cruz J, Sherman F, Jeffries TW (2002) SHAM-sensitive alternative respiration in the xylose-metabolizing yeast Pichia stipitis. Yeast 19:1203–1220
Slininger PJ, Bothast RJ, Van Cauwenberge JE, Kurtzman CP (1982) Conversion of d-xylose to ethanol by the yeast Pachysolen tannophilus. Biotechnol Bioeng 24:371–384
Smil V (1999) Crop residues: agriculture′s largest harvest—crop residues incorporate more than half of the world agricultural phytomass. Bioscience 49:299–308
Smith CA, Rangarajan M, Hartley BS (1991) d-Xylose (d-glucose) isomerase from Arthrobacter strain NRRL B3728. Purification and properties. Biochem J 277:255–261
Sonderegger M, Sauer U (2003) Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl Environ Microbiol 69:1990–1998
Sreenath HK, Jeffries TW (2000) Production of ethanol from wood hydrolyzate by yeasts. Bioresour Technol 72:253–260
Sreenath HK, Koegel RG, Moldes AB, Jeffries TW, Straub RJ (1999) Enzymic saccharification of alfalfa fiber after liquid hot water pretreatment. Process Biochem 35:33–41
Sreenath HK, Koegel RG, Moldes AB, Jeffries TW, Straub RJ (2001) Ethanol production from alfalfa fiber fractions by saccharification and fermentation. Process Biochem 36:1199–1204
Takuma S, et al (1991) Isolation of xylose reductase gene of Pichia stipitis and its expression in Saccharomyces cerevisiae. Appl Biochem Biotechnol 28/29:327–340
Tantirungkij M, Nakashima N, Seki T, Yoshida T (1993) Construction of xylose-assimilating Saccharomyces cerevisiae. J Ferment Bioeng 75:83–88
Tantirungkij M, Seki T, Yoshida T (1994) Genetic improvement of Saccharomyces cerevisiae for ethanol production from xylose. Ann NY Acad Sci 721:138–147
Teusink B, Walsh MC, Dam K van, Westerhoff HV (1998) The danger of metabolic pathways with turbo design. Trends Biochem Sci 23:162–169
Thestrup HN, Hahn-Hägerdal B (1995) Xylitol formation and reduction equivalent generation during anaerobic xylose conversion with glucose as cosubstrate in recombinant Saccharomyces cerevisiae expressing the xyl1 gene. Appl Environ Microbiol 61:2043–2045
Thevelein JM, Hohmann S (1995) Trehalose synthase: guard to the gate of glycolysis in yeast? Trends Biochem Sci 20:3–10
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
Toivola A, Yarrow D, Bosch E van den, Dijken JP van, Scheffers WA (1984) Alcoholic fermentation of deuterium-xylose by yeasts. Appl Environ Microbiol 47:1221–1223
Träff KL, Otero Cordero RR, Zyl WH van, Hahn-Hägerdal B (2001) Deletion of the GRE3 aldose reductase gene and its influence on xylose metabolism in recombinant strains of Saccharomyces cerevisiae expressing the xylA and XKS1 genes. Appl Environ Microbiol 67:5668–5674
Vandeska E, Amartey S, Kuzmanova S, Jeffries TW (1996) Fed-batch culture for xylitol production by Candida boidinii. Proc Biochem 31:265–270
Verduyn C, Frank J, Dijken JP van, Scheffers WA (1985a) Multiple forms of xylose reductase in Pachysolen tannophilus CBS 4044. FEMS Microbiol Lett 30:313–317
Verduyn C, Kleef R van, Frank J, Schreuder H, Dijken JP van, Scheffers WA (1985b) Properties of the NAD(P)H-dependent xylose reductase from the xylose-fermenting yeast Pichia stipitis. Biochem J 226:669–677
Verwaal R, Paalman JW, Hogenkamp A, Verkleij AJ, Verrips CT, Boonstra J (2002) HXT5 expression is determined by growth rates in Saccharomyces cerevisiae. Yeast 19:1029–1038
Wahlbom CF, Zyl WH van, Jonsson LJ, Hahn-Hagerdal B, Otero RR (2003) Generation of the improved recombinant xylose-utilizing Saccharomyces cerevisiae TMB 3400 by random mutagenesis and physiological comparison with Pichia stipitis CBS 6054. FEMS Yeast Res 3:319–326
Walfridsson M, Hallborn J, Penttilä M, Keranen S, Hahn-Hägerdal B (1995) Xylose-metabolizing Saccharomyces cerevisiae strains overexpressing the TKL1 and TAL1 genes encoding the pentose phosphate pathway enzymes transketolase and transaldolase. Appl Environ Microbiol 61:4184–4190
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
Walfridsson M, Anderlund M, Bao X, Hahn-Hägerdal B (1997) Expression of different levels of enzymes from the Pichia stipitis XYL1 and XYL2 genes in Saccharomyces cerevisiae and its effects on product formation during xylose utilisation. Appl Microbiol Biotechnol 48:218–224
Wang PY, Schneider H (1980) Growth of yeasts on d-xylulose 1. Can J Microbiol 26:1165–1168
Wang PY, Shopsis C, Schneider H (1980) Fermentation of a pentose by yeasts. Biochem Biophys Res Commun 94:248–254
Weierstall T, Hollenberg CP, Boles E (1999) Cloning and characterization of three genes (SUT1–3) encoding glucose transporters of the yeast Pichia stipitis. Mol Microbiol 31:871–883
Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, Boles E (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464:123–128
Wijsman MR, Bruinenberg PM, Dijken JP van, Scheffers WA (1985) Incapacity for anaerobic growth in xylose-fermenting yeasts. Antonie Van Leeuwenhoek 51:563–564
Winkelhausen E, Pittman P, Kuzmanova S, Jeffries TW (1996) Xylitol formation by Candida boidinii in oxygen limited chemostat culture. Biotechnol Lett 18:753–758
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
Wyman CE (1999) Biomass ethanol: technical progress, opportunities, and commercial challenges. Annu Rev Energy Environ 24:189–226
Yoon G-S, Lee T-S, Kim C, Seo J-H, Ryu Y-W (1996) Characterization of alcohol fermentation and segregation of protoplast fusant of Saccharomyces cerevisiae and Pichia stipitis. J Microbiol Biotechnol 6:286–291
Zaldivar J, et al (2002) Fermentation performance and intracellular metabolite patterns in laboratory and industrial xylose-fermenting Saccharomyces cerevisiae. Appl Microbiol Biotechnol 59:436–442
Zyl C van, Prior BA, Kilian SG, Brandt EV (1993) Role of d-ribose as a cometabolite in d-xylose metabolism by Saccharomyces cerevisiae. Appl Environ Microbiol 59:1487–1494
Zyl WH van, Eliasson A, Hobley T, Hahn-Hägerdal B (1999) Xylose utilisation by recombinant strains of Saccharomyces cerevisiae on different carbon sources. Appl Microbiol Biotechnol 52:829–833
Acknowledgements
The authors thank P. Richard, E. Boles and J. Becker for early access to reviewed manuscripts and to J. Laplaza for useful discussion.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jeffries, T.W., Jin, YS. Metabolic engineering for improved fermentation of pentoses by yeasts. Appl Microbiol Biotechnol 63, 495–509 (2004). https://doi.org/10.1007/s00253-003-1450-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-003-1450-0