Use of in vivo 13C nuclear magnetic resonance spectroscopy to elucidate L-arabinose metabolism in yeasts

Applied and Environmental Microbiology

Volumn 74, Issue 6, 2008, Pages 1845-1855

  Fonseca, César ^a   Neves, Ana Rute ^b   Antunes, Alexandra M M ^c   Noronha, João Paulo ^c   Hahn Hägerdal, Bärbel ^d   Santos, Helena ^b   Spencer Martins, Isabel ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c DEPARTAMENTO DE QUÍMICA   (Portugal)

^d LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CATABOLISM; PENTOSE PHOSPHATE PATHWAY (PPP);

METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; REDOX REACTIONS;

YEAST;

ARABINITOL; ARABINOSE; CARBON; CARBON 13; GLUCOSE 6 PHOSPHATE; LEVO ARABINOSE REDUCTASE; LEVO XYLULOSE REDUCTASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RIBITOL; TREHALOSE; UNCLASSIFIED DRUG; XYLITOL; XYLULOSE; SUGAR ALCOHOL;

CARBON ISOTOPE; CATABOLISM; COMPARATIVE STUDY; DETECTION METHOD; ENZYME ACTIVITY; EXPERIMENTAL STUDY; FERMENTATION; NUCLEAR MAGNETIC RESONANCE; YEAST;

AEROBIC METABOLISM; ARTICLE; CANDIDA; CANDIDA ARABINOFERMENTANS; CARBOHYDRATE METABOLISM; CARBON NUCLEAR MAGNETIC RESONANCE; CATABOLISM; FUNGAL STRAIN; ISOTOPE LABELING; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PICHIA; PICHIA GUILLERMONDII; YEAST; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CANDIDA ARABINOFERMENTANS; FUNGI; PICHIA GUILLIERMONDII;

ARABINOSE; CARBON ISOTOPES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL; RIBITOL; SUGAR ALCOHOLS; TREHALOSE; XYLITOL; YEASTS;

EID: 40849139270     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.02453-07     Document Type: Article

References (45)

1. Barnett, J. A. 1976. The utilization of sugars by yeasts. Adv. Carbohydr. Chem. Biochem. 32:125-234.
2. Becker, J., and E. Boles. 2003. A modified Saccharomyces cerevisiae strain that consumes L-arabinose and produces ethanol. Appl. Environ. Microbiol. 69:4144-4150.
3. Bruinenberg, P. M., R. Jonker, J. P. van Dijken, and W. A. Scheffers. 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.
4. Bruinenberg, P. M., J. P. van Dijken, and W. A. Scheffers. 1983. An enzymic analysis of NADPH production and consumption in Candida utilis. J. Gen. Microbiol. 129:965-971.
5. Bruinenberg, P. M., J. P. van Dijken, and W. A. Scheffers. 1984. Production and consumption of NADPH and NADH during growth of Candida utilis on xylose. Antonie van Leeuwenhoek 50:81-82.
6. Chiang, C., and S. G. Knight. 1960. A new pathway of pentose metabolism. Biochim. Biophys. Res. Commun. 3:554-559.
7. De Graaf, A. A. 2000. Metabolic flux analysis of Corynebacterium glutamicum, p. 506-555. In K. Schügerl and K. H. Bellgardt (ed.), Bioreaction engineering. Springer Verlag, Berlin, Germany.
8. Dien, B. S., C. P. Kurtzman, B. C. Saha, and R. J. Bothast. 1996. Screening for L-arabinose fermenting yeasts. Appl. Biochem. Biotechnol. 57-58:233-242.
9. du Preez, J. C., B. van Driessel, and B. A. Prior. 1989. Effect of aerobiosis on fermentation and key enzyme levels during growth of Pichia stipitis, Candida shehatae and Candida tenuis on D-xylose. Arch. Microbiol. 152:143-147.
10. Fonseca, C., R. Romão, H. Rodrigues de Sousa, B. Hahn-Hägerdal, and I. Spencer-Martins. 2007. L-Arabinose transport and catabolism in yeast. FEBS J. 274:3589-3600.
11. T and Pichia guilliermondii PYCC 3012: influence of sugar and oxygen on product formation. Appl. Microbiol. Biotechnol. 75:303-310.
12. Granström, T., H. Ojamo, and M. Leisola. 2001. Chemostat study of xylitol production by Candida guilliermondii. Appl. Microbiol. Biotechnol. 55: 36-42.
13. Ho, N. W., Z. Chen, and A. P. Brainard. 1998. Genetically engineered Saccharomyces yeast capable of effective cofermentation of glucose and xylose. Appl. Environ. Microbiol. 64:1852-1859.
14. Höfer, M., and P. C. Misra. 1978. Evidence for a proton/sugar symport in the yeast Rhodotorula gracilis (glutinis). Biochem. J. 172:15-22.
15. Hui, M., S. W. Cheung, M. L. Chin, K. C. Chu, R. C. Chan, and A. F. Cheng. 2004. Development and application of a rapid diagnostic method for invasive Candidiasis by the detection of D-/L-arabinitol using gas chromatography/ mass spectrometry. Diagn. Microbiol. Infect. Dis. 49:117-123.
16. Jeppsson, H., N. J. Alexander, and B. Hahn-Hägerdal. 1995. Existence of cyanide-insensitive respiration in the yeast Pichia stipitis and its possible influence on product formation during xylose utilization. Appl. Environ. Microbiol. 61:2596-2600.
17. Jeppsson, M., B. Johansson, B. Hahn-Hägerdal, and M. F. Gorwa-Grauslund. 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.
18. Jeppsson, M., B. Johansson, P. R. Jensen, B. Hahn-Hägerdal, and M. F. Gorwa-Grauslund. 2003. The level of glucose-6-phosphate dehydrogenase activity strongly influences xylose fermentation and inhibitor sensitivity in recombinant Saccharomyces cerevisiae strains. Yeast 20:1263-1272.
19. Jin, Y. S., J. Cruz, and T. W. Jeffries. 2005. Xylitol production by a Pichia stipitis D-xylulokinase mutant. Appl. Microbiol. Biotechnol. 68:42-45.
20. Jin, Y. S., S. Jones, N. Q. Shi, and T. W. Jeffries. 2002. Molecular cloning of XYL3 (D-xylulokinase) from Pichia stipitis and characterization of its physiological function. Appl. Environ. Microbiol. 68:1232-1239.
21. Karhumaa, K., B. Wiedemann, B. Hahn-Hägerdal, E. Boles, and M. F. Gorwa-Grauslund. 2006. Co-utilization of L-arabinose and D-xylose by laboratory and industrial Saccharomyces cerevisiae strains. Microb. Cell Fact. 5:18-28.
22. Kötter, P., and M. Ciriacy. 1993. Xylose fermentation by Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 38:776-783.
23. Ligthelm, M. E., B. A. Prior, and J. C. du Preez. 1988. The oxygen requirements of yeasts for the fermentation of D-xylose and D-glucose to ethanol. Appl. Microbiol. Biotechnol. 28:63-68.
24. 13C} xylose metabolism in Pichia stipitis under aerobic and anaerobic conditions. Appl. Microbiol. Biotechnol. 28:293-296.
25. 13C labeling in studies of metabolic regulation. Prog. Nucl. Magn. Res. Spectrosc. 20:337-383.
26. Luyten, K., J. Albertyn, W. F. Skibbe, B. A. Prior, J. Ramos, J. M. Thevelein, and S. Hohmann. 1995. Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J. 14:1360-1371.
27. McMillan, J. D., and B. L. Boynton. 1994. Arabinose utilization by xylose-fermenting yeasts and fungi. Appl. Biochem. Biotechnol. 45:569-584.
28. Neves, A. R., A. Ramos, H. Costa, I. I. van Swam, J. Hugenholtz, M. Kleerebezem, W. de Vos, and H. Santos. 2002. Effect of different NADH oxidase levels on glucose metabolism by Lactococcus lactis: kinetics of intracellular metabolite pools determined by in vivo nuclear magnetic resonance. Appl. Environ. Microbiol. 68:6332-6342.
29. Neves, A. R., A. Ramos, M. C. Nunes, M. Kleerebezem, J. Hugenholtz, W. M. de Vos, J. Almeida, and H. Santos. 1999. In vivo nuclear magnetic resonance studies of glycolytic kinetics in Lactococcus lactis. Biotechnol. Bioeng. 64: 200-212.
30. Oliveira, R., F. Lages, M. Silva-Graça, and C. Lucas. 2003. Fps1p channel is the mediator of the major part of glycerol passive diffusion in Saccharomyces cerevisiae: artefacts and re-definitions. Biochim. Biophys. Acta 1613:57-71.
31. Richard, P., R. Verho, M. Putkonen, J. Londesborough, and M. Penttilä. 2003. Production of ethanol from L-arabinose by Saccharomyces cerevisiae containing a fungal L-arabinose pathway. FEMS Yeast Res. 3:185-189.
32. Saha, B. C., and R. J. Bothast. 1996. Production of L-arabitol from L-arabinose by Candida entomaea and Pichia guilliermondii. Appl. Microbiol. Biotechnol. 45:299-306.
33. 13C and proton NMR studies of horse cytochrome c. Assignment and temperature dependence of methyl resonances. FEBS Lett. 194:73-77.
34. Shi, N. Q., K. Prahl, J. Hendrick, J. Cruz, P. Lu, J. Y. Cho, S. Jones, and T. Jeffries. 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.
35. Skoog, K., and B. Hahn-Hägerdal. 1990. Effect of oxygenation on xylose fermentation by Pichia stipitis. Appl. Environ. Microbiol. 56:3389-3394.
36. Sutherland, F. C., F. Lages, C. Lucas, K. Luyten, J. Albertyn, S. Hohmann, B. A. Prior, and S. G. Kilian. 1997. Characteristics of Fps1-dependent and -independent glycerol transport in Saccharomyces cerevisiae. J. Bacteriol. 179:7790-7795.
37. Tamás, M. J., K. Luyten, F. C. Sutherland, A. Hernandez, J. Albertyn, H. Valadi, H. Li, B. A. Prior, S. G. Kilian, J. Ramos, L. Gustafsson, J. M. Thevelein, and S. Hohmann. 1999. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol. Microbiol. 31:1087-1104.
38. Tang, X. M., G. Kayingo, and B. A. Prior. 2005. Functional analysis of the Zygosaccharomyces rouxii Fps1p homologue. Yeast 22:571-581.
39. Tantirungkij, M., N. Nakashima, T. Seki, and T. Yoshida. 1993. Construction of xylose-assimilating Saccharomyces cerevisiae. J. Ferment. Bioeng. 75:83-88.
40. Taylor, K. B., M. J. Beck, D. H. Huang, and T. T. Sakai. 1990. The fermentation of xylose: studies by carbon-13 nuclear magnetic resonance spectroscopy. J. Ind. Microbiol. 6:29-41.
41. van Zyl, C., B. A. Prior, S. G. Kilian, and E. V. Brandt. 1993. Role of D-ribose as a cometabolite in D-xylose metabolism by Saccharomyces cerevisiae. Appl. Environ. Microbiol. 59:1487-1494.
42. Verduyn, C., E. Postma, W. A. Scheffers, and J. P. van Dijken. 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.
43. Verho, R., M. Putkonen, J. Londesborough, M. Penttilä, and P. Richard. 2004. A novel NADH-linked L-xylulose reductase in the L-arabinose catabolic pathway of yeast. J. Biol. Chem. 279:14746-14751.
44. Wisselink, H. W., M. J. Toirkens, B. M. Rosario Franco, A. A. Winkler, J. P. van Dijken, J. T. Pronk, and A. J. van Maris. 2007. Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of L-arabinose. Appl. Environ. Microbiol. 73:4881-4891.
45. Witteveen, C. F. B., R. Busink, P. Vandevondervoort, C. Dijkema, K. Swart, and J. Visser. 1989. L-Arabinosc and D-xylose catabolism in Aspergillus niger. J. Gen. Microbiol. 135:2163-2171.