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The yeast Kluyveromyces marxianus and its biotechnological potential

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Abstract

Strains belonging to the yeast species Kluyveromyces marxianus have been isolated from a great variety of habitats, which results in a high metabolic diversity and a substantial degree of intraspecific polymorphism. As a consequence, several different biotechnological applications have been investigated with this yeast: production of enzymes (β-galactosidase, β-glucosidase, inulinase, and polygalacturonases, among others), of single-cell protein, of aroma compounds, and of ethanol (including high-temperature and simultaneous saccharification-fermentation processes); reduction of lactose content in food products; production of bioingredients from cheese-whey; bioremediation; as an anticholesterolemic agent; and as a host for heterologous protein production. Compared to its congener and model organism, Kluyveromyces lactis, the accumulated knowledge on K. marxianus is much smaller and spread over a number of different strains. Although there is no publicly available genome sequence for this species, 20% of the CBS 712 strain genome was randomly sequenced (Llorente et al. in FEBS Lett 487:71–75, 2000). In spite of these facts, K. marxianus can envisage a great biotechnological future because of some of its qualities, such as a broad substrate spectrum, thermotolerance, high growth rates, and less tendency to ferment when exposed to sugar excess, when compared to K. lactis. To increase our knowledge on the biology of this species and to enable the potential applications to be converted into industrial practice, a more systematic approach, including the careful choice of (a) reference strain(s) by the scientific community, would certainly be of great value.

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References

  • Abranches J, Morais PB, Rosa CA, Mendonça-Hagler LC, Hagler AN (1997) The incidence of killer activity and extracellular proteases in tropical yeast communities. Can J Microbiol 43:328–336

    Article  CAS  PubMed  Google Scholar 

  • Aksu Z, Dönmez G (2000) The use of molasses in copper (II) containing wastewaters: effects on growth and copper (II) bioaccumulation properties of Kluyveromyces marxianus. Proc Biochem 36:451–458

    Article  CAS  Google Scholar 

  • Aktas N, Boyacı IH, Mutlu M, Tanyolac A (2005) Optimization of lactose utilization in deproteinated whey by Kluyveromyces marxianus using response surface methodology (RSM). Biores Technol 97:2252–2259

    Article  CAS  Google Scholar 

  • Almeida C, Branyik T, Moradas-Ferreira P, Teixeira J (2003a) Continuous production of pectinase by immobilized yeast cells on spent grains. J Biosci Bioeng 96:513–518

    Article  CAS  PubMed  Google Scholar 

  • Amrane A, Prigent Y (1996) Behaviour of the yeast Kluyveromyces marxianus var. marxianus during its autolysis. Antonie van Leeuwenhoek 69:267–272

    Article  CAS  PubMed  Google Scholar 

  • Anderson PJ, McNeil K, Watson K (1986) High-efficiency carboidrate fermentation to ethanol at temperatures above 40°C by Kluyveromyces marxianus var. marxianus isolated from sugar mills. Appl Environ Microbiol 51:1314–1320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacci Júnior M, Siqueira CG, Antoniazi SA, Ueta J (1996) Location of the b-galactosidase of the yeast Kluyveromyces marxianus var. marxianus ATCC 10022. Antonie van Leeuwenhoek 69:357–361

    Article  PubMed  Google Scholar 

  • Bajpai P, Margaritis A (1982) Ethanol inhibition kinetics of Kluyveromyces marxianus grown on Jerusalem artichoke juice. Appl Environ Microbiol 44:1325–1329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bajpai P, Margaritis A (1987a) Kinetics of ethanol production by immobilized Kluyveromyces marxianus cells at varying sugar concentrations of Jerusalem artichoke juice. Appl Microbiol Biotechnol 26:447–449

    Article  CAS  Google Scholar 

  • Bajpai P, Margaritis A (1987b) The effect of temperature and pH on ethanol production by free and immobilized cells of Kluyveromyces marxianus grown on Jerusalem artichoke extract. Biotechnol Bioeng 30:306–313

    Article  CAS  PubMed  Google Scholar 

  • Ball MM, Raynal A, Guerineau M, Iborra F (1999) Construction of efficient centromeric, multicopy and expression vectors for the yeast Kluyveromyces marxianus using homologous elements and the promoter of a purine-cytosine-like permease. J Mol Microbiol Biotechnol 1:347–353

    CAS  PubMed  Google Scholar 

  • Ballesteros I, Ballesteros M, Cabanas A, Carrasco J, Martin C, Negro MJ, Saez F, Saez R (1991) Selection of thermotolerant yeasts for simultaneous saccharification and fermentation (SSF) of cellulose to ethanol. Appl Biochem Biotechnol 28:307–315

    Article  PubMed  Google Scholar 

  • Ballesteros I, Oliva JM, Negro MJ, Manzanares P, Ballesteros M (2002a) Simultaneous saccharification and fermentation process for converting the cellulosic fraction of olive oil extraction residue into ethanol. Grasas y Aceites 53:282–288

    Article  CAS  Google Scholar 

  • Ballesteros M, Oliva JM, Manzanares P, Negro MJ, Ballesteros I (2002b) Ethanol production from paper material using a simultaneous saccharification and fermentation system in a fed-batch basis. World J Microbiol Biotechnol 18:559–561

    Article  CAS  Google Scholar 

  • Ballesteros M, Oliva JM, Negro MJ, Manzanares P, Ballesteros I (2004) Ethanol from lignocellulosic materials by a simultaneous saccharification and fermentation process (SFS) with Kluyveromyces marxianus CECT 10875. Proc Biochem 39:1843–1848

    Article  CAS  Google Scholar 

  • Banat IM, Nigam P, Marchant R (1992) Isolation of thermotolerant, fermentative yeasts growing at 52°C and producing ethanol at 45°C and 50°C. World J Microbiol Biotechnol 8:259–263

    Article  CAS  PubMed  Google Scholar 

  • Banat IM, Singh D, Marchant R (1996) The use of a thermotolerant fermentative Kluyveromyces marxianus IMB3 yeast strain for ethanol production. Acta Biotechnol 16:215–223

    Article  CAS  Google Scholar 

  • Banat IM, Nigam P, Singh D, Marchant R, McHale AP (1998) Ethanol production at elevated temperatures and alcohol concentrations: Part I - Yeasts in general. World J Microbiol Biotechnol 14:809–821

    Article  CAS  Google Scholar 

  • Barnby FM, Morpeth FF, Pyle DL (1990) Endopolygalacturonase production from Kluyveromyces marxianus. Resolution, purification, and partial characterisation of the enzyme. Enzyme Microb Technol 12:891–897

    Article  CAS  Google Scholar 

  • Barnett JA, Payne RW, Yarrow D (1983) Yeasts: characteristics and identification. Cambridge University Press, Cambridge

    Google Scholar 

  • Barranco-Florido E, García-Garibay M, Gómez-Ruiz L, Azaola A (2001) Immobilization system of Kluyveromyces marxianus cells in barium alginate for inulin hydrolysis. Proc Biochem 37:513–519

    Article  Google Scholar 

  • Barron N, Marchant R, McHale L, McHale AP (1995a) Partial characterization of b-glucosidase activity produced by Kluyveromyces marxianus IMB3 during growth on cellobiose containing media at 45°C. Biotechnol Lett 17:1047–1050

    Article  CAS  Google Scholar 

  • Barron N, Marchant R, McHale L, McHale AP (1995b) Studies on the use of a thermotolerant strain of Kluyveromyces marxianus in simultaneous saccharification and ethanol formation from cellulose. Appl Microbiol Biotechnol 43:518–520

    Article  CAS  Google Scholar 

  • Barron N, Marchant R, McHale L, McHale AP (1996) Ethanol production from cellulose at 45°C using a batch-fed system containing alginate-immobilized Kluyveromyces marxianus IMB3. World J Microbiol Biotechnol 12:103–104

    Article  CAS  PubMed  Google Scholar 

  • Barron N, Mulholland H, Boyle M, McHale AP (1997) Ethanol production by Kluyveromyces marxianus IMB3 during growth on straw-supplemented whiskey distillery spentwash at 45°C. Bioproc Eng 17:383–386

    CAS  Google Scholar 

  • Bartkevičiute D, Sasnauskas K (2003) Studies of yeast Kluyveromyces lactis mutations conferring super-secretion of recombinant proteins. Yeast 20:1–11

    Article  PubMed  CAS  Google Scholar 

  • Bartkevičiūtė D, Šiekštelė R, Sasnauskas K (2000) Heterologous expression of the Kluyveromyces marxianus endopolygalacturonase gene (EPG1) using versatile autonomously replicating vector for a wide range of host. Enzyme Microb Technol 26:653–656

    Article  Google Scholar 

  • Basabe L, Cabrera N, Yong V, Menéndez J, Delgado JM, Rodríguez L (1996) Isolation and characterization of mutants as an approach to a transformation system in Kluyveromyces marxianus. Curr Genet 30:89–92

    Article  CAS  PubMed  Google Scholar 

  • Beezer AE, Newell RD, Tyrrell HJ (1979) Characterisation and metabolic studies of Saccharomyces cerevisiae and Kluyveromyces fragilis by flow microcalorimetry. Antonie van Leeuwenhoek 45:55–63

    Article  CAS  PubMed  Google Scholar 

  • Belem MAF, Lee BH (1998) Production of bioingredients from Kluyveromyces marxianus grown on whey: an alternative. Crit Rev Food Sci Nut 38:565–598

    Article  CAS  Google Scholar 

  • Belem MAF, Lee BH (1999) Fed-batch fermentation to produce ologonucleotides from Kluyveromyces marxianus grown on whey. Proc Biochem 34:501–509

    Article  CAS  Google Scholar 

  • Belem MAF, Gibbs BF, Lee BH (1997) Enzymatic production of ribonucleotides from autolysates of Kluyveromyces marxianus grown on whey. J Food Sci 62:851–857

    Article  CAS  Google Scholar 

  • Bellaver LH, de Carvalho NMB, Abrahão-Neto J, Gombert AK (2004) Ethanol formation and enzyme activities around glucose-6-phosphate in Kluyveromyces marxianus CBS 6556 exposed to glucose or lactose excess. FEMS Yeast Res 4:691–698

    Article  CAS  PubMed  Google Scholar 

  • Ben-Hassan RM, Ghaly AE (1995) Continuous production of single-cell protein from cheese whey lactose using Kluyveromyces fragilis. Trans ASAE 38:1121–1127

    Article  CAS  Google Scholar 

  • Ben-Hassan RM, Ghaly AE, Ben-Abdallah N (1992) Metabolism of cheese whey lactose by Kluyveromyces fragilis for energy and growth under batch condition. Appl Biochem Biotechnol 33:97–116

    Article  CAS  Google Scholar 

  • Bergkamp RJ, Geerse RH, Verbakel JM, Musters W, Planta RJ (1991) Cloning and disruption of the LEU2 gene of Kluyveromyces marxianus CBS 6556. Yeast 7:963–970

    Article  CAS  PubMed  Google Scholar 

  • Bergkamp RJM, Bootsmas TC, Toschka HY, Mooren ATA, Kox L, Verbakel JMA, Geerse RH, Planta RJ (1993a) Expression of an a-galactosidase gene under control of the homologous inulinase promoter in Kluyveromyces marxianus. Appl Microbiol Biotechnol 40:309–317

    Article  CAS  PubMed  Google Scholar 

  • Bergkamp RJ, Geerse RH, Verbakel JM, Planta RJ (1993b) Cloning and sequencing of the URA3 gene of Kluyveromyces marxianus CBS 6556. Yeast 9:677–681

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharjee H, Bhaduri A (1992) Distinct functional roles of two active site thiols in UDPglucose 4-epimerase from Kluyveromyces fragilis. J Biol Chem 267:11714–11720

    Article  CAS  PubMed  Google Scholar 

  • Bianchi MM, Falcone C, Re CX, Wéslowski-Louvel M, Frontali L, Fukuhara H (1987) Transformation of the yeast Kluyveromyces lactis by new vectors derived from the 1.6 mm circular plasmid pKD1. Curr Genet 12:185–192

    Article  CAS  Google Scholar 

  • Blanco P, Sieiro C, Villa TG (1999) Production of pectic enzymes in yeasts. FEMS Microbiol Lett 175:1–9

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Boyle M, Barron N, McHale AP (1997) Simultaneous saccharification and fermentation of straw to ethanol using the thermotolerant yeast strain Kluyveromyces marxianus IMB 3. Biotechnol Lett 19:49–51

    Article  CAS  Google Scholar 

  • Brady D, Marchant R, McHale L, McHale AP (1995) Isolation and partial characterization of b-galactosidase activity produced by a thermotolerant strain of Kluyveromyces marxianus during growth on lactose-containing media. Enzyme Microb Technol 17:696–699

    Article  CAS  Google Scholar 

  • Brady D, Nigam P, Marchant R, McHale L, McHale AP (1996) Ethanol production at 45°C by Kluyveromyces marxianus IMB3 immobilized in magnetically responsive alginate matrices. Biotechnol Lett 18:1213–1216

    Article  CAS  Google Scholar 

  • Brady D, Nigam P, Marchant R, McHale AP (1997a) Ethanol production at 45°C by alginate-immobilized Kluyveromyces marxianus IMB3 during growth on lactose-containing media. Bioproc Eng 16:101–104

    Article  CAS  Google Scholar 

  • Brady D, Nigam P, Marchant R, Singh D, McHale AP (1997b) The effect of Mn2+ on ethanol production from lactose using Kluyveromyces marxianus IMB3 immobilized in magnetically responsive matrices. Bioproc Eng 17:31–34

    CAS  Google Scholar 

  • Brady D, Logan SR, McHale AP (1998) The effect of soluble alginate and calcium on b-galactosidase activity produced by the thermotolerant, ethanol-producing yeast strain Kluyveromyces marxianus IMB3. Bioproc Eng 18:101–104

    CAS  Google Scholar 

  • Breunig KD, Steensma HY (2003) Kluyveromyces lactis: genetics, physiology, and application. In: de Winde JH (ed) Functional genetics of industrial yeasts, Topics in current genetics, vol. 2. Springer-Verlag, Berlin Heidelberg New York, pp 171–205

    Chapter  Google Scholar 

  • Büschges R, Bahrenberg G, Zimmermann M, Wolf K (1994) NADH: ubiquinone oxidoreductase in obligate aerobic yeasts. Yeast 10:475–479

    Article  PubMed  Google Scholar 

  • Caballero R, Olguín P, Cruz-Guerrero A, Gallardo F, García-Garibay M, Gómez-Ruiz L (1995) Evaluation of Kluyveromyces marxianus as baker’s yeast. Food Res Int 28:37–41

    Article  CAS  Google Scholar 

  • Carvalho-Silva M, Spencer-Martins I (1990) Modes of lactose uptake in the yeast species Kluyveromyces marxianus. Antonie van Leeuwenhoek 57:77–81

    Article  CAS  PubMed  Google Scholar 

  • Cassart JP, Ostling J, Ronne H, Vandenhaute J (1997) Comparative analysis in three fungi reveals structurally and functionally conserved regions in the Mig1 repressor. Mol Gen Genet 255:9–18

    Article  CAS  PubMed  Google Scholar 

  • Castrillo JI, Ugalde UO (1993) Patterns of energy metabolism and growth kinetics of Kluyveromyces marxianus in whey chemostat culture. Appl Microbiol Biotechnol 40:386–393

    Article  CAS  Google Scholar 

  • Chassang-Douillet A, Ladet J, Boze H, Galzy P (1973) Respiratory metabolism of Kluyveromyces fragilis van der Walt. Z Allg Mikrobiol 13:193–199

    CAS  PubMed  Google Scholar 

  • Chen XJ, Saliola M, Falcone C, Bianchi MM, Fukuhara H (1986) Sequence organization of the circular plasmid pKD1 from the yeast Kluyveromyces drosophilarum. Nucleic Acids Res 14:4471–4481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen XJ, Bianchi MM, Suda K, Fukuhara H (1989) The host range of the pKD1-derived plasmids in yeast. Curr Genet 16:95–98

    Article  CAS  PubMed  Google Scholar 

  • Corpillo D, Valetti F, Giuffrida MG, Conti A, Rossi A, Finazzi-Agrò A, Giunta C (2003) Induction and characterization of a novel amine oxidase from the yeast Kluyveromyces marxianus. Yeast 20:369–379

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Guerrero A, García-Peña I, Bárzana E, García-Garibay M, Gómez-Ruiz L (1995) Kluyveromyces marxianus CDBB-L-278: a wild inulinase hyperproducing strain. J Ferm Bioeng 80:159–163

    Article  CAS  Google Scholar 

  • Cruz-Guerrero A, Bárzana E, García-Garibay M, Gómez-Ruiz L (1999) Dissolved oxygen threshold for the repression of endo-polygalacturonase production by Kluyveromyces marxianus. Proc Biochem 34:621–624

    Article  CAS  Google Scholar 

  • Das S, Kellermann E, Hollenberg CP (1984) Transformation of Kluyveromyces fragilis. J Bacteriol 158:1165–1167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Bruijne AW, Schuddemat J, van den Broek PJA, van Steveninck J (1988) Regulation of sugar transport systems of Kluyveromyces marxianus: the role of carbohydrates and their catabolism. Biochim Biophys Acta 939:569–576

    Article  PubMed  Google Scholar 

  • de Morais MA Jr (2003) The NADP+-dependent glutamate dehydrogenase of the yeast Kluyveromyces marxianus responds to nitrogen repression similarly to Saccharomyces cerevisiae. Braz J Microbiol 34:334–338

    Article  Google Scholar 

  • de Sánchez SB, Castillo FJ (1980) Effect of pH on the growth of Kluyveromyces fragilis on deproteinized whey. Acta Cient Venez 31:24–26

    PubMed  Google Scholar 

  • Donaghy JA, McKay AM (1994) The use of K1uvveromyces fragilis for the extraction of orange peel pectins. J Appl Bacteriol 76:506–510

    Article  CAS  Google Scholar 

  • Dujon B, Sherman D, Fischer G et al (2004) Genome evolution in yeasts. Nature 430:35–44

    Article  PubMed  Google Scholar 

  • Duvnjak Z, Houle C, Mok KL (1987) Production of ethanol and biomass from various carbohydrates by Kluyveromyces fragilis. Biotechnol Lett 9:343–346

    Article  CAS  Google Scholar 

  • Eraso P, Gancedo JM (1984) Catabolite repression in yeasts is not associated with low levels of cAMP. Eur J Biochem 141:195–198

    Article  CAS  PubMed  Google Scholar 

  • Etschmann MMW, Schrader J (2006) An aqueous-organic two-phase bioprocess for efficient production of the natural aroma chemicals 2-phenylethanol and 2-phenylethylacetate with yeast. Appl Microbiol Biotechnol 71:440–443

    Article  CAS  PubMed  Google Scholar 

  • Etschmann MMW, Bluemke W, Sell D, Schrader J (2002) Biotechnological production of 2-phenylethanol. Appl Microbiol Biotechnol 59:1–8

    Article  CAS  PubMed  Google Scholar 

  • Etschmann MMW, Sell D, Schrader J (2004) Medium optimization for the production of the aroma compound 2-phenylethanol using a genetic algorithm. J Mol Catal B: Enzym 29:187–193

    Article  CAS  Google Scholar 

  • Fabre CE, Duviau VJ, Blanc PJ, Goma G (1995) Identification of volatile flavour compounds obtained in culture of Kluyveromyces marxianus. Biotechnol Lett 17:1207–1212

    Article  CAS  Google Scholar 

  • Fabre CE, Blanc PJ, Goma G (1998) Production of 2-phenylethyl alcohol by Kluyveromyces marxianus. Biotechnol Prog 14:270–274

    Article  CAS  PubMed  Google Scholar 

  • Falcone C, Saliola M, Chen XJ, Frontali L, Fukuhara H (1986) Analysis of a 1.6-micron circular plasmid from the yeast Kluyveromyces drosophilarum: structure and molecular dimorphism. Plasmid 15:248–252

    Article  CAS  PubMed  Google Scholar 

  • Ferguson P, Mulholland H, Barron N, Brady D, McHale AP (1998) Sucrose-supplemented distillery spent-wash as a medium for production of ethanol at 45°C by free and alginate-immobilized preparations of Kluyveromyces marxianus IMB3. Bioproc Eng 18:257–259

    CAS  Google Scholar 

  • Fernanda R, Sa-Correia I (1992) Ethanol tolerance and activity of plasma membrane ATPase in Kluyveromyces marxianus and Saccharomyces cerevisiae. Enzyme Microb Technol 14:23–27

    Article  Google Scholar 

  • Fernandes PA, Keen JN, Findlay JBC, Moradas-Ferreira PA (1992) Protein homologous to glyceraldehyde-3-phosphate dehydrogenase is induced in the cell wall of a flocculant Kluyveromyces marxianus. Biochim Biophys Acta 1159:67–73

    Article  CAS  PubMed  Google Scholar 

  • Fernandes PA, Sousa M, Moradas-Ferreira P (1993) Flocculation of Kluyveromyces marxianus is induced by a temperature upshift. Yeast 9:859–866

    Article  CAS  PubMed  Google Scholar 

  • Fernandes PA, Sena-Esteves M, Moradas-Ferreira P (1995) Characterization of the glyceraldehyde-3-phosphate dehydrogenase gene family from Kluyveromyces marxianus - polymerase chain reaction single-strand conformation polymorphism as a tool for the study of multigenic families. Yeast 11:725–733

    Article  CAS  PubMed  Google Scholar 

  • Ferrari MD, Loperena L, Varela H (1994) Ethanol production from concentrated whey permeate using a fed-batch culture of Kluyveromyces fragilis. Biotechnol Lett 16:205–210

    Article  CAS  Google Scholar 

  • Fiedurek J, Szczodrak J (1994) Selection of strain, culture conditions and extraction procedures for optimum production of b-galactosidase from Kluyveromyces fragilis. Acta Microbiol Pol 43:57–65

    CAS  PubMed  Google Scholar 

  • Fonseca A, Spencer-Martins I, van Uden N (1991) Transport of lactic acid in Kluyveromyces marxianus: evidence for a monocarboxylate uniport. Yeast 7:775–780

    Article  CAS  PubMed  Google Scholar 

  • Fonseca GG, Gombert AK, Heinzle E, Wittmann C (2007) Physiology of the yeast Kluyveromyces marxianus during batch and chemostat cultures with glucose as the sole carbon source. FEMS Yeast Res 7:422–435

    Article  CAS  PubMed  Google Scholar 

  • Fukuhara H (2006) Kluyveromyces lactis - A retrospective. FEMS Yeast Res 6:323–324

    Article  CAS  PubMed  Google Scholar 

  • Furlan SA, Schneider ALS, Merkle R, Carvalho-Jonas MD, Jonas R (2000) Formulation of a lactose-free, low-cost culture medium for the production of b-D-galactosidase by Kluyveromyces marxianus. Biotechnol Lett 22:589–593

    Article  CAS  Google Scholar 

  • Garcia-Garibay M, Gómez-Ruiz L, Bárzana E (1987a) Studies on the simultaneous production of single-cell protein and endo-polygalacturonase from Kluyveromyces fragilis. Biotechnol Lett 9:411–416

    Article  CAS  Google Scholar 

  • Garcia-Garibay M, Torres J, López-Munguía-Canales A, Casas LT (1987b) Influence of oxygen transfer rate on b-galactosidase production from Kluyveromyces marxianus. Biotechnol Lett 9:417–420

    Article  CAS  Google Scholar 

  • Gasnier B (1987) Characterization of low- and high-affinity glucose transports in the yeast Kluyveromyces marxianus. Biochim Biophys Acta 903:425–433

    Article  CAS  PubMed  Google Scholar 

  • Gellissen G, Hollenberg CP (1997) Application of yeasts in gene expression studies: A comparison of Saccharomyces cerevisiae, Hansenula polymorpha and Kluyveromyces lactis—a review. Gene 190:87–97

    Article  CAS  PubMed  Google Scholar 

  • Ghaly AE, Singh RK (1989) Pollution potential reduction of cheese whey through yeast fermentation. Appl Biochem Biotechnol 22:181–203

    Article  CAS  PubMed  Google Scholar 

  • Ghaly AE, Kamal M (2004) Submerged yeast fermentation of acid cheese whey for protein production and pollution potential reduction. Water Res 38:631–644

    Article  CAS  PubMed  Google Scholar 

  • Giec A, Kosikowski FV (1992) Activity of lactose fermenting yeasts in producing biomass from concentrated whey permeates. J Food Sci 47:1892–1894

    Article  Google Scholar 

  • Gonçalves JA, Castillo FJ (1982) Partial Purification and characterization of b-D-galactosidase from Kluyverornyces rnarxianus. J Dairy Sci 65:2088–2094

    Article  Google Scholar 

  • Gough S, McHale AP (1998) Continuous ethanol production from molasses at 45°C using alginate-immobilized Kluyveromyces marxianus IMB3 in a continuous-flow bioreactor. Bioproc Eng 19:33–36

    CAS  Google Scholar 

  • Gough S, Flynn O, Hack CJ, Marchant R (1996) Fermentation of molasses using a thermotolerant yeast, Kluyveromyces marxianus IMB3: simplex optimization of media supplements. Appl Microbiol Biotechnol 46:187–190

    Article  CAS  PubMed  Google Scholar 

  • Gough S, Brady D, Nigam P, Marchant R, McHale AP (1997) Production of ethanol from molasses at 45°C using alginate-immobilized Kluyveromyces marxianus IMB3. Bioproc Eng 16:389–392

    CAS  Google Scholar 

  • Gough S, Barron N, Zubov AL, Lozinsky VI, McHale AP (1998) Production of ethanol from molasses at 45°C using Kluyveromyces marxianus IMB3 immobilized in calcium alginate gels and poly(vinyl alcohol) cryogel. Bioproc Eng 19:87–90

    CAS  Google Scholar 

  • Grootwassink JWD, Hewitt GM (1983) Inducible and constitutive formation of b-fructofuranosidase (inulase) in batch and continuous cultures of the yeast Kluyveromyces marxianus. J Gen Microbiol 129:31–41

    CAS  Google Scholar 

  • Grubb CF, Mawson AJ (1993) Effects of elevated solute concentrations on the fermentation of lactose by Kluyveromyces marxianus Y-113. Biotechnol Lett 15:621–626

    Article  CAS  Google Scholar 

  • Goldstein AL, McCusker JH (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541–1553

    Article  CAS  PubMed  Google Scholar 

  • Güldener U, Heck S, Fielder T, Beinhauer J, Hegemann JH (1996) A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res 24:2519–2524

    Article  PubMed  PubMed Central  Google Scholar 

  • Hack CJ, Banat IM, Singh D, Marchant R (1994) Ethanol production by a strain of Kluyveromyces marxianus at elevated temperatures in various bioreactor configurations. In: Proceedings of Conference on Fermentation Physiology, Pub. Institution of Chemical Engineers, Brighton, pp 7–9

  • Hacking AJ, Taylor IWF, Hanas CM (1984) Selection of yeasts able to produce ethanol from glucose at 40°C. Appl Microbiol Biotechnol 19:361–363

    Article  CAS  Google Scholar 

  • Hahn-Hägerdal B (1985) Comparison between immobilized Kluyveromyces fragilis and Saccharomyces cerevisiae coimmobilized with b-galactosidase, with respect to continuous ethanol production from concentrated whey permeate. Biotechnol Bioeng 27:914–916

    Article  PubMed  Google Scholar 

  • Harden TJ (1996) The reduction of BOD and production of biomass from acid whey by Kluyveromyces marxianus. Food Aust 48:456–457

    Google Scholar 

  • Harsa S, Zaror CA, Pyle DL (1993) Production of polygalacturonases from Kluyveromyces marxianus fermentation—preliminary process design and economics. Proc Biochem 28:187–195

    Article  CAS  Google Scholar 

  • Hashida-Okado T, Ogawa A, Kato I, Takesako K (1998) Transformation system for prototrophic industrial yeasts using the AUR1 gene as a dominant selection marker. FEBS Lett 425:117–122

    Article  CAS  PubMed  Google Scholar 

  • Hensing M, Vrouwenvelder H, Hellinga C, Baartmans R, van Dijken JP (1994) Production of extracellular inulinase in high-cell-density fed-batch cultures of Kluyveromyces marxianus. Appl Microbiol Biotechnol 42:516–521

    Article  CAS  Google Scholar 

  • Hensing MC, Rouwenhorst RJ, Heijnen JJ, van Dijken JP, Pronk JT (1995) Physiological and technological aspects of large-scale heterologous-protein production with yeasts. Antonie van Leeuwenhoek 67:261–279

    Article  CAS  PubMed  Google Scholar 

  • Holloway P, Subden RE (1993) The isolation and nucleotide sequence of the pyruvate decarboxylase gene from Kluyveromyces marxianus. Curr Genet 24:274–277

    Article  CAS  PubMed  Google Scholar 

  • Hong J, Wang Y, Kumagai H, Tamaki H (2007) Construction of thermotolerant yeast expressing thermostable cellulase genes. J Biotechnol 130:114–123

    Article  CAS  PubMed  Google Scholar 

  • Hughes DB, Tudrosaen NJ, Moye CJ (1984) The effect of temperature on the kinectics of ethanol production by a thermotolerant strain of Kluyveromyces marxianus. Biotechnol Lett 6:1–6

    Article  CAS  Google Scholar 

  • Huo K, Li Y (1995) Cloning and expression of Kluyveromyces fragilis LAC4 gene. Sci China B 38:1332–1340

    CAS  PubMed  Google Scholar 

  • Iborra F (1993) High efficiency transformation of Kluyveromyces marxianus by a replicative plasmid. Curr Genet 24:181–183

    Article  CAS  PubMed  Google Scholar 

  • Iborra F, Ball MM (1994) Kluyveromyces marxianus small DNA fragments contain both autonomous replicative and centromeric elements that also function in Kluyveromyces lactis. Yeast 10:1621–1629

    Article  CAS  PubMed  Google Scholar 

  • Isenschmid A, Marison IW, von Stockar U (1995) The influence of pressure and temperature of compressed CO2 on the survival of yeast cells. J Biotechnol 39:229–237

    Article  CAS  PubMed  Google Scholar 

  • Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153:163–168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh T, Susuki M, Adachi S (1982) Production of b-galactosidase from lactose-fermenting yeasts. Agric Biol Chem 46:899–904

    CAS  Google Scholar 

  • Jia J, Wheals A (2000) Endopolygalacturonase genes and enzymes from Saccharomyces cerevisiae and Kluyveromyces marxianus. Curr Genet 38:264–270

    Article  CAS  PubMed  Google Scholar 

  • Jolivet P, Bergeron E, Benyair H, Meunier JC (2001) Characterization of major protein phosphatases from selected species of Kluyveromyces. Comparison with protein phosphatases from Yarrowia lipolytica. Can J Microbiol 47:861–870

    Article  CAS  PubMed  Google Scholar 

  • Jones TD, Havard JM, Daugulis AJ (1993) Ethanol production from lactose by extractive fermentation. Biotechnol Lett 15:871–876

    Article  CAS  Google Scholar 

  • Kádár ZS, Szengyel ZS, Réczey K (2004) Simultaneous saccharification and fermentation (SSF) of industrial wastes for the production of ethanol. Ind Crops Prod 20:103–110

    Article  CAS  Google Scholar 

  • Kataoka M, Kotaka A, Thiwthong R, Wada M, Nakamori S, Shimizu S (2004) Cloning and overexpression of the old yellow enzyme gene of Candida macedoniensis, and its application to the production of a chiral compound. J Biotechnol 114:1–9

    Article  CAS  PubMed  Google Scholar 

  • Kiers J, Zeeman AM, Luttik M, Thiele C, Castrillo JI, Steensma HY, van Dijken JP, Pronk JT (1998) Regulation of alcoholic fermentation in batch and chemostat cultures of Kluyveromyces lactis CBS 2359. Yeast 14:459–469

    Article  CAS  PubMed  Google Scholar 

  • Kim WH, Chung JH, Back JH, Choi J, Cha JH, Koh HY, Han YS (2003) Molecular cloning and characterization of an NADPH quinone oxidoreductase from Kluyveromyces marxianus. J Biochem Mol Biol 36:442–449

    CAS  PubMed  Google Scholar 

  • Kreger-van Rij NJW (1984) The yeasts: a taxonomic study, 3rd edn. Elsevier, Amsterdam

    Google Scholar 

  • Künkel W, May R (1976) Alcohol dehydrogenase (ADH) in yeast cells. I. Cytoplasmic, mitochondrial and nuclear ADH in Saccharomyces carlsbergensis and Kluyveromyces fragilis. Z Allg Mikrobiol 16:529–536

    Article  PubMed  Google Scholar 

  • Kurtzman CP (2003) Phylogenetic circumscription of Saccharomyces, Kluyveromyces and other members of the Saccharomycetaceae, and the proposal of the new genera Lachancea, Nakaseomyces, Naumovia, Vanderwaltozyma and Zygotorulaspora. FEMS Yeast Res 4:233–245

    Article  CAS  PubMed  Google Scholar 

  • Kurtzman CP, Fell JW (eds) (1998) The yeasts: a taxonomic study, 4th edn. Elsevier, Amsterdam

    Google Scholar 

  • Kurtzman CP, Robnett CJ (2003) Phylogenetic relationships among yeasts of the ‘Saccharomyces complex’ determined from multigene sequence analyses. FEMS Yeast Res 3:417–432

    Article  CAS  PubMed  Google Scholar 

  • Lachance MA (1998) Kluyveromyces van der Walt emend. van der Walt. In: Kurtzman CP, Fell JW (eds) The yeasts: a taxonomic study, 4th edn. Elsevier, Amsterdam, pp 227–247

    Chapter  Google Scholar 

  • Lachance MA (2007) Current status of Kluyveromyces systematics. FEMS Yeast Res 7:642–645

    Article  CAS  PubMed  Google Scholar 

  • Ladrière JM, Delcour J, Vandenhaute J (1993) Sequence of a gene coding for a cytoplasmic alcohol dehydrogenase from Kluyveromyces marxianus ATCC 12424. Biochim Biophys Acta 1173:99–101

    Article  PubMed  Google Scholar 

  • Ladrière JM, Georis I, Guerineau M, Vandenhaute J (2000) Kluyveromyces marxianus exhibits an ancestral Saccharomyces cerevisiae genome organization downstream of ADH2. Gene 255:83–91

    Article  PubMed  Google Scholar 

  • Laloux O, Cassart JP, Delcour J, van Beeumen J, Vandenhaute J (1991) Cloning and sequencing of the inulinase gene of Kluyveromyces marxianus var. marxianus ATCC 12424. FEBS Lett 289:64–68

    Article  CAS  PubMed  Google Scholar 

  • Leclerc M, Chemardin P, Arnaud A, Ratomahenina R, Galzy P, Gerbaud C, Raynal A, Guérineau M (1987) Comparison of the properties of the purified beta-glucosidase from the transformed strain of Saccharomyces cerevisiae TYKF2 with that of the donor strain Kluyveromyces fragilis Y610. Biotechnol Appl Biochem 9:410–422

    CAS  PubMed  Google Scholar 

  • Leclercq-Perlat MN, Corrieu G, Spinnler HE (2004) Comparison of volatile compounds produced in model cheese medium deacidified by Debaryomyces hansenii or Kluyveromyces marxianus. J Dairy Sci 87:1545–1550

    Article  CAS  PubMed  Google Scholar 

  • Lim J, Yamasaki Y, Suzuki Y, Ozawa J (1980) Multiple forms of endo-polygalacturonase from Saccharomyces fragilis. Agric Biol Chem 44:473–480

    CAS  Google Scholar 

  • Llorente B, Malpertuy A, Blandin G, Artiguenave F, Wincker P, Dujon B (2000) Genomic exploration of the hemiascomycetous yeasts: 12. Kluyveromyces marxianus var. marxianus. FEBS Lett 487:71–75

    Article  CAS  PubMed  Google Scholar 

  • Lodder J (1970) The yeasts: a taxonomic study, 2nd edn. NHPC, Amsterdam

    Google Scholar 

  • Lodder J, Kreger-van Rij NJW (1952) The yeasts: a taxonomic study. NHPC, Amsterdam

    Google Scholar 

  • Love G, Nigam P, Barron N, Singh D, Marchant R, McHale AP (1996) Ethanol production at 45°C using preparations of Kluyveromyces marxianus IMB3 immobilized in calcium alginate and kissiris. Bioproc Eng 15:275–277

    Article  CAS  Google Scholar 

  • Love G, Gough S, Brady D, Barron N, Nigam P, Singh D, Marchant R, McHale AP (1998) Continuous ethanol fermentation at 45°C using Kluyveromyces marxianus IMB3. Immobilized in calcium alginate and kissiris. Bioproc Eng 18:187–189

    CAS  Google Scholar 

  • Lukondeh T, Ashbolt NJ, Rogers PL (2003a) Evaluation of Kluyveromyces marxianus as a source of yeast autolysates. J Ind Microbiol Biotechnol 30:52–56

    Article  CAS  PubMed  Google Scholar 

  • Lukondeh T, Ashbolt NJ, Rogers PL (2003b) Evaluation of Kluyveromyces marxianus FII 510700 grown on a lactose-based medium as a source of a natural bioemulsifier. J Ind Microbiol Biotechnol 30:715–720

    Article  CAS  PubMed  Google Scholar 

  • Lukondeh T, Ashbolt NJ, Rogers PL (2003c) Confirmation of an alkali-insoluble glucans from Kluyveromyces marxianus cultivated on a lactose-based medium. World J Microbiol Biotechnol 19:349–355

    Article  CAS  Google Scholar 

  • Mahoney RR, Nickerson TA, Whitaker JR (1975) Selection of strain, growth conditions and extraction procedures for optimum production of lactase from Kluyveromyces fragilis. J Dairy Sci 58:1620–1629

    Article  CAS  PubMed  Google Scholar 

  • Majumdar S, Bhattacharjee H, Bhattacharyya D, Bhaduri A (1998) UDP-galactose 4-epimerase from Kluyveromyces fragilis: reconstitution of holoenzyme structure after dissociation with parachloromercuribenzoate. Eur J Biochem 257:427–433

    Article  CAS  PubMed  Google Scholar 

  • Margaritis A, Bajpai P (1982) Direct fermentation of D-xylose to ethanol by Kluyveromyces marxianus strains. Appl Environ Microbiol 44:1039–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margaritis A, Bajpai P (1983) Effect of sugar concentration in Jerusalem artichoke extract on Kluyveromyces marxianus growth and ethanol production. Appl Environ Microbiol 45:723–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martins DB, de Souza CG Jr, Simões DA, de Morais MA Jr (2002) The b-galactosidase activity in Kluyveromyces marxianus CBS6556 decreases by high concentrations of galactose. Curr Microbiol 44:379–382

    Article  CAS  PubMed  Google Scholar 

  • Marwaha SS, Kennedy JF, Sehgal VK (1988) Simulation of process conditions of continuous ethanol fermentation of whey permeate using alginate entrapped Kluyveromyces marxianus NCYC-179 cells in a packed-bed reactor system. Proc Biochem 23:17–22

    CAS  Google Scholar 

  • Medeiros ABP, Pandey A, Freitas RJS, Christen P, Soccol CR (2000) Optimization of the production of aroma compounds by Kluyveromyces marxianus in solid-state fermentation using factorial design and response surface methodology. Biochem Eng J 6:33–39

    Article  CAS  PubMed  Google Scholar 

  • Medeiros ABP, Pandey A, Christen P, Fontoura PSG, de Freitas RJS, Soccol CR (2001) Aroma compounds produced by Kluyveromyces marxianus in solid state fermentation on a packed bed column bioreactor. World J Microbiol Biotechnol 17:767–771

    Article  CAS  Google Scholar 

  • Meilhoc E, Masson JM, Teissié J (1990) High efficiency transformation of intact yeast cells by electric field pulses. J Biotechnol 8:223–227

    CAS  Google Scholar 

  • Molnár O, Prillinger H, Lopandic K, Weigang F, Staudacher E (1996) Analysis of coenzyme Q systems, monosaccharide patterns of purified cell walls, and RAPD-PCR patterns in the genus Kluyveromyces. Antonie van Leeuwenhoek 70:67–78

    Article  PubMed  Google Scholar 

  • Mukherji S, Bhaduri A (1992) An essential histidine residue for the activity of UDPglucose 4-epimerase from Kluyveromyces fragilis. J Biol Chem 267:11709–11713

    Article  CAS  PubMed  Google Scholar 

  • Neves L, Oliveira R, Lucas C (2004) Yeast orthologues associated with glycerol transport and metabolism. FEMS Yeast Res 5:51–62

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TH, Fleet GH, Rogers PL (1998) Composition of the cell walls of several yeast species. Appl Microbiol Biotechnol 50:206–212

    Article  CAS  PubMed  Google Scholar 

  • Nigam P, Banat IM, Singh D, McHale AP, Marchant R (1997) Continuous ethanol production by thermotolerant Kluyveromyces marxianus IMB3 yeast immobilized on mineral kissiris at 45°C. World J Microbiol Biotechnol 13:283–288

    Article  CAS  Google Scholar 

  • Nilsson U, Barron N, McHale L, McHale AP (1995) The effects of phosphoric and pretreatment on conversion of cellulose to ethanol at 45°C using the thermotolerant yeast Kluyveromyces marxianus IMB3. Biotechnol Lett 17:985–988

    Article  CAS  Google Scholar 

  • Nolan AM, Barron N, Brady D, McAree T, Smith D, McHale L, McHale AP (1994) Ethanol production at 45°C by an alginate-immobilized strain of Kluyveromyces marxianus following growth on glucose-containing media. Biotechnol Lett 16:849–852

    Article  CAS  Google Scholar 

  • Nunes MFA, Massaguer S, Alegre RM (1993) Produção e propriedades de b-galactosidase de Kluyveromyces marxianus NRRL Y-2415. Rev Farm Bioquim Univ S Paulo 29:25–30

    CAS  Google Scholar 

  • Oberyé EH, Maurer K, Mager WH, Planta RJ (1993) Structure of the ABF1-homologue from Kluyveromyces marxianus. Biochim Biophys Acta 1173:233–236

    Article  PubMed  Google Scholar 

  • O’Shea DG, Walsh PK (2000) The effect of culture conditions on the morphology of the dimorphic yeast Kluyveromyces marxianus var. marxianus NRRLy 2415: a study incorporating image analysis. Appl Microbiol Biotechnol 53:316–322

    Article  PubMed  Google Scholar 

  • Panuwatsuk W, da Silva NA (2002) Evaluation of pKD1-based plasmid systems for heterologous protein production in Kluyveromyces lactis. Appl Microbiol Biotechnol 58:195–201

    Article  CAS  PubMed  Google Scholar 

  • Parekh S, Margaritis A (1985) Inulinase (b-fructofuranosidase) production by Kluyveromyces marxianus in batch culture. Appl Microbiol Biotechnol 22:446–448

    Article  CAS  Google Scholar 

  • Pecota DC, da Silva NA (2005) Evaluation of the tetracycline promoter system for regulated gene expression in Kluyveromyces marxianus. Biotechnol Bioeng 92:117–123

    Article  CAS  PubMed  Google Scholar 

  • Pecota DC, Rajgarhia V, da Silva NA (2007) Sequential gene integration for the engineering of Kluyveromyces marxianus. J Biotechnol 127:408–416

    Article  CAS  PubMed  Google Scholar 

  • Penman CS, Duffus JH (1974) Ergosterol is the only sterol in Kluyveromyces fragilis. Antonie van Leeuwenhoek 40:529–531

    Article  CAS  PubMed  Google Scholar 

  • Pessoa Jr A, Vitolo M (1999) Inulinase from Kluyveromyces marxianus: culture medium composition and enzyme extraction. Braz J Chem Eng 16:237–245

    Article  CAS  Google Scholar 

  • Pinheiro R, Belo I, Mota M (2000) Air pressure effects on biomass yield of two different Kluyveromyces strains. Enzyme Microb Technol 26:756–762

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro R, Belo I, Mota M (2002) Oxidative stress response of Kluyveromyces marxianus to hydrogen peroxide, paraquat and pressure. Appl Microbiol Biotechnol 58:842–847

    Article  CAS  PubMed  Google Scholar 

  • Porro D, Sauer M, Branduardi P, Mattanovich D (2005) Recombinant protein production in yeasts. Mol Biotechnol 31:245–259

    Article  CAS  PubMed  Google Scholar 

  • Postma E, van der Broek PJA (1990) Continuous-culture study of the regutation of glucose and fructose transport in Kluyveromyces marxianus CBS 6556. J Bacteriology 172:2871–2876

    Article  CAS  Google Scholar 

  • Prudêncio C, Sansonetty F, Sousa MJ, Côrte-Real M, Leão C (2000) Rapid detection of efflux pumps and their relation with drug resistance in yeast cells. Cytometry 39:26–35

    Article  PubMed  Google Scholar 

  • Queirós O, Casal M, Althoff S, Moradas-Ferreira P, Leão C (1998) Isolation and characterization of Kluyveromyces marxianus mutants deficient in malate transport. Yeast 14:401–407

    Article  PubMed  Google Scholar 

  • Rajoka MI, Khan S, Shahid R (2003) Kinetics and regulation studies of the production of b-galactosidase from Kluyveromyces marxianus grown on different substrates. Food Technol Biotechnol 41:315–320

    CAS  Google Scholar 

  • Rajoka MI, Latif F, Khan S, Shahid R (2004) Kinetics of improved productivity of b-galactosidase by a cycloheximide-resistant mutant of Kluyveromyces marxianus. Biotechnol Lett 26:741–746

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Zavala B, Mercado-Flores Y, Hernandez-Rodriguez C, Villa-Tanaca L (2004a) Purification and characterization of a lysine aminopeptidase from Kluyveromyces marxianus. FEMS Microbiol Lett 235:369–375

    Article  CAS  PubMed  Google Scholar 

  • Ramirez-Zavala B, Mercado-Flores Y, Hernandez-Rodriguez C, Villa-Tanaca L (2004b) Purification and characterization of a serine carboxypeptidase from Kluyveromyces marxianus. Int J Food Microbiol 91:245–252

    Article  CAS  PubMed  Google Scholar 

  • Ray S, Mukherji S, Bhaduri A (1995) Two tryptophans at the active site of UDP-glucose 4-epimerase from Kluyveromyces fragilis. J Biol Chem 270:11383–11390

    Article  CAS  PubMed  Google Scholar 

  • Raynal A, Guerineau M (1984) Cloning and expression of the structural gene for b-glucosidase of Kluyveromyces fragilis in Escherichia coli and Saccharomyces cerevisiae. Mol Gen Genet 195:108–115

    Article  CAS  PubMed  Google Scholar 

  • Raynal A, Gerbaud C, Francingues MC, Guerineau M (1987) Sequence and transcription of the b-glucosidase gene of Kluyveromyces fragilis cloned in Saccharomyces cerevisiae. Curr Genet 12:175–184

    Article  CAS  PubMed  Google Scholar 

  • Rech R, Cassini CF, Secchi AR, Ayub MAZ (1999) Utilization of protein-hydrolyzed chesse whey for the production of b-galactosidase by Kluyveromyces marxianus. J Ind Microbiol Biotechnol 23:91–96

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro O, Gombert AK, Teixeira JA, Domingues L (2007) Application of the Cre-loxP system for multiple gene disruption in the yeast Kluyveromyces marxianus. J Biotechnol 131:20–26

    Article  CAS  PubMed  Google Scholar 

  • Riordan C, Love G, Barron N, Nigam P, Marchant R, McHale L, McHale AP (1996) Production of ethanol from sucrose at 45°C by alginate-immobilized preparations of the thermotolerant yeast strain Kluyveromyces marxianus IMB3. Biores Technol 55:171–173

    Article  CAS  Google Scholar 

  • Romanos MA, Scorer CA, Clare JJ (1992) Foreign gene expression in yeast: a review. Yeast 8:423–488

    Article  CAS  PubMed  Google Scholar 

  • Rosa FM, Sa-Correia I (1992) Ethanol tolerance and activity of plasma membrane ATPase in Kluyveromyces marxianus and Saccharomyces cerevisiae. Enzyme Microb Technol 14:23–27

    Article  CAS  Google Scholar 

  • Rouwenhorst RJ, Visser LE, van der Baan AA, Scheffers WA, van Dijken JP (1988) Production, distribution, and kinetic properties of inulinase in continuous culture of Kluyveromyces marxianus CBS 6556. Appl Environ Microbiol 54:1131–1137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouwenhorst RJ, Hensing M, Verbakel J, Scheffers WA, van Dijken JP (1990a) Structure and properties of the extracellular inulinase of Kluyveromyces marxianus CBS 6556. Appl Environ Microbiol 56:3337–3345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouwenhorst RJ, Ritmeester WS, Scheffers WA, van Dijken JP (1990b) Localization of inulinase and invertase in Kluyveromyces species. Appl Environ Microbiol 56:3329–3336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakanaka K, Yan W, Kishida M, Sakai T (1996) Breeding a fermentative yeast at high temperature using protoplast fusion. J Ferment Bioeng 81:104–108

    Article  CAS  Google Scholar 

  • Schaffrath R, Breunig KD (2000) Genetics and molecular physiology of the yeast Kluyveromyces lactis. Fung Genet Biol 30:173–190

    Article  CAS  Google Scholar 

  • Scharpf LG, Seitz EW, Morris JA, Farbood MI (1986) Generation of flavor and odor compounds through fermentation processes. In: Parliament TH, Croteau R (eds) Biogeneration of aroma, American Chemical Society, Washington, DC, vol. 317, pp 323–346

    Google Scholar 

  • Schultz N, Chang L, Hauck A, Reuss M, Syldatk C (2006) Microbial production of single-cell protein from deproteinized whey concentrates. Appl Microbiol Biotechnol 69:515–520

    Article  CAS  PubMed  Google Scholar 

  • Schwan RF, Rose AH (1994) Polygalacturonase production by Kluyveromyces marxianus: effect of medium composition. J Appl Bacteriol 76:62–67

    Article  CAS  Google Scholar 

  • Schwan RF, Cooper RM, Wheals AE (1997) Endopolygalacturonase secretion by Kluyveromyces marxianus and other cocoa pulp-degrading yeasts. Enzyme Microb Technol 21:234–244

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Šiekštelė R, Bartkevičiūtė D, Sasnauskas K (1999) Cloning, targeted disruption and heterologous expression of the Kluyveromyces marxianus endopolygalacturonase gene (EPG1). Yeast 15:311–322

    Article  PubMed  Google Scholar 

  • Skountzou P, Soupioni M, Bekatorou A, Kanellaki M, Koutinas AA, Marchant R, Banat IM (2003) Lead(II) uptake during baker’s yeast production by aerobic fermentation of molasses. Proc Biochem 38:1479–1482

    Article  CAS  Google Scholar 

  • Sonawat HM, Agrawal A, Dutta SM (1981) Production of b-galactosidase from Kluyveromyces fragilis grown on whey. Folia Microbiol 26:370–376

    Article  CAS  Google Scholar 

  • Souciet J-L, Artiguenave MAF, Blandin G, Bolotin-Fukuhara M, Bon E, Brottier P et al (2000) Genomic exploration of the hemiascomycetous yeasts: 1. A set of yeast species for molecular evolution studies. FEBS Letters 487:3–12

    Article  PubMed  Google Scholar 

  • Stambuk BU, Franden MA, Singh A, Zhang M (2003) D-Xylose transport by Candida succiphila and Kluyveromyces marxianus. Appl Biochem Biotechnol 108:255–263

    Article  Google Scholar 

  • Steensma HY, Ter Linde JJ (2001) Plasmids with the Cre-recombinase and the dominant nat marker, suitable for use in prototrophic strains of Saccharomyces cerevisiae and Kluyveromyces lactis. Yeast 18:469–472

    Article  CAS  PubMed  Google Scholar 

  • Steensma HY, de Jongh FCM, Linnekamp M (1988) The use of electrophoretic karyotypes in the classification of yeasts: Kluyveromyces marxianus and K. lactis. Curr Genet 14:311–317

    Article  CAS  Google Scholar 

  • Stephanopoulos GN, Aristidou AA, Nielsen J (1998) Metabolic Engineering Principles and Methodologies. Academic Press, San Diego

    Google Scholar 

  • Sukroongreung S, Schappert KT, Khachatourians GG (1984) Survey of sensitivity of twelve yeast genera toward T-2 toxin. Appl Environ Microbiol 48:416–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tin CSF, Mawson AJ (1993) Ethanol production from whey in a membrane recycle bioreactor. Proc Biochem 28:217–221

    Article  CAS  Google Scholar 

  • Ternan NG, McMullan G (2000) The utilization of 4-aminobutylphosphonate as sole nitrogen source by a strain of Kluuyveromyces fragilis. FEMS Microbiol Lett 184:237–240

    Article  CAS  PubMed  Google Scholar 

  • Ternan NG, McMullan G (2002) Iminodiacetate and nitrilotriacetate degradation by Kluyveromyces marxianus IMB3. Biochem Biophys Res Comm 290:802–805

    Article  CAS  PubMed  Google Scholar 

  • Toyoda Y, Sy J (1984) Purification and phosphorylation of fructose-1,6-bisphosphatase from Kluyveromyces fragilis. J Biol Chem 259:8718–8723

    Article  CAS  PubMed  Google Scholar 

  • van den Berg JA, van der Laken KJ, van Ooyen AJJ, Renniers TCHM, Rietveld K et al (1990) Kluyveromyces as a host for heterologous gene expression. Expression and secretion of prochymosin. Bio/Techno 8:135–139

    Google Scholar 

  • van den Broek PJ, de Bruijne AW, van Steveninck J (1987) The role of ATP in the control of H+-galactoside symport in the yeast Kluyveromyces marxianus. Biochem J 242:729–734

    Article  PubMed  PubMed Central  Google Scholar 

  • van der Walt JP (1956) Kluyveromyces- a new yeast genus of the Endomycetales. Antonie van Leeuwenhoek 22:265–272

    Article  Google Scholar 

  • van der Walt JP (1970) Kluyveromyces van der Walt emend. van der Walt. In: Lodder J (ed) The yeasts: a taxonomic study, 2nd edn. NHPC, Amsterdam, pp 316–378

    Google Scholar 

  • van der Walt JP, Johannsen E (1984) Kluyveromyces van der Walt emend. van der Walt. In: Kreger-van Rij NJW (ed) The yeasts: a taxonomic study, 3rd edn. Elsevier, Amsterdam, pp 224–251

    Google Scholar 

  • van Dijken JP, Weusthuis RA, Pronk JT (1993) Kinetics of growth and sugar consumption in yeasts. Antonie van Leeuwenhoek 63:343–352

    Article  PubMed  Google Scholar 

  • van Dijken JP, Bauer J, Brambilla L et al (2000) An interlaboratory comparison of physiological and genetic properties of four Saccharomyces cerevisiae strains. Enz Microb Technol 26:706–714

    Article  Google Scholar 

  • van Leeuwen CC, Postma E, van den Broek PJ, van Steveninck J (1991) Proton-motive force-driven D-galactose transport in plasma membrane vesicles from the yeast Kluyveromyces marxianus. J Biol Chem 266:12146–12151

    Article  PubMed  Google Scholar 

  • van Ooyen AJ, Dekker P, Huang M, Olsthoorn MM, Jacobs DI, Colussi PA, Taron CH (2006) Heterologous protein production in the yeast Kluyveromyces lactis. FEMS Yeast Res 6:381–392

    Article  CAS  PubMed  Google Scholar 

  • van Urk H, Voll WSL, Scheffers WA, van Dijken JP (1990) Transient-state analyses of metabolic fluxes in Crabtree-positive and Crabtree-negative yeasts. Appl Environ Microbiol 56:281–287

    Article  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Verzotti E, Geymonat M, Valetti F, Lanzetti L, Giunta C (1994) In the budding yeast Kluyveromyces marxianus, adenylate cyclase is regulated by Ras protein(s) in vitro. Yeast 10:993–1001

    Article  CAS  PubMed  Google Scholar 

  • Viegas CA, Rosa MF, Sá-Correia I, Novais JM (1989) Inhibition of yeast growth by octanoic and decanoic acids produced during ethanolic fermentation. Appl Environ Microbiol 55:21–28

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoda K, Ko JH, Nagamatsu T, Lin Y, Kaibara C, Kawada T, Tomishige N, Hashimoto H, Noda Y, Yamasaki M (2000) Molecular characterization of a novel yeast cell-wall acid phosphatase cloned from Kluyveromyces marxianus. Biosci Biotechnol Biochem 64:142–148

    Article  CAS  PubMed  Google Scholar 

  • Ward C, Nolan AM, O’Hanlon F, McAree T, Barron N, McHale L, McHale AP (1995) Production of ethanol at 45°C on starch-containing media by mixed cultures of the thermotolerant, ethanol-producing yeast Kluyveromyces marxianus IMB3 and the thermophilic filamentous fungus Talaromyces emersonii CBS 813.70. Appl Microbiol Biotechnol 43:408–411

    Article  CAS  Google Scholar 

  • Wésolowski-Louvel M, Breunig KD, Fukuhara H (1996) Kluyveromyces lactis: genetics, biochemistry and molecular biology of non-conventional yeast. Springer-Verlag, Berlin Heidelberg New York

    Book  Google Scholar 

  • Welsh FW, Murray WD, Williams RE (1989) Microbiological and enzymatic production of flavor and fragrance chemicals. Crit Rev Biotechnol 9:105–169

    Article  CAS  Google Scholar 

  • Wimborne MP, Rickard PAD (1978) Pectinolytic activity of Saccharomyces fragilis cultured in controlled environments. Biotechnol Bioeng 20:231–242

    Article  CAS  PubMed  Google Scholar 

  • Wittmann C, Hans M, Bluemke W (2002) Metabolic physiology of aroma-producing Kluyveromyces marxianus. Yeast 19:1351–1363

    Article  CAS  PubMed  Google Scholar 

  • Wolf K, Breunig K, Barth G (eds) (2003) Non-conventional yeasts in genetics, biochemistry and biotechnology: practical protocols. Springer-Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Workman WE, Day DF (1984) The cell wall-associated inulinase of Kluyveromyces fragilis. Antonie van Leeuwenhoek 50:349–353

    Article  CAS  PubMed  Google Scholar 

  • Yoshida Y, Yokoi W, Wada Y, Ohishi K, Ito M, Sawada H (2004) Potent hypocholesterolemic activity of the yeast Kluyveromyces marxianus YIT 8292 in rats fed a high cholesterol diet. Biosci Biotechnol Biochem 68:1185–1192

    Article  CAS  PubMed  Google Scholar 

  • Yoshida Y, Yokoi W, Ohishi K, Ito M, Naito E, Sawada H (2005) Effects of the cell wall of Kluyveromyces marxianus YIT 8292 on the plasma cholesterol and fecal sterol excretion in rats fed on a high-cholesterol diet. Biosci Biotechnol Biochem 69:714–723

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Yuan H, Wen T, Xu F, Di Y, Huo K, Li YY (2003) Cloning of the KcURA3 gene and development of a transformation system for Kluyveromyces cicerisporus. Appl Microbiol Biotechnol 62:387–391

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Brazil), Deutscher Akademischer Austausch Dienst (DAAD) (Germany), and Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Brazil) are acknowledged.

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Authors and Affiliations

  1. Department of Chemical Engineering, University of São Paulo, São Paulo, São Paulo, Brazil

    Gustavo Graciano Fonseca & Andreas K. Gombert

  2. Biochemical Engineering Institute, Saarland University, Saarbrücken, Germany

    Gustavo Graciano Fonseca, Elmar Heinzle & Christoph Wittmann

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

    Andreas K. Gombert

Authors
  1. Gustavo Graciano Fonseca
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  2. Elmar Heinzle
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  3. Christoph Wittmann
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  4. Andreas K. Gombert
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Correspondence to Andreas K. Gombert.

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Fonseca, G.G., Heinzle, E., Wittmann, C. et al. The yeast Kluyveromyces marxianus and its biotechnological potential. Appl Microbiol Biotechnol 79, 339–354 (2008). https://doi.org/10.1007/s00253-008-1458-6

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  • DOI: https://doi.org/10.1007/s00253-008-1458-6

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