Engineering Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: Reflections and perspectives

Biotechnology Journal

Volumn 7, Issue 1, 2012, Pages 34-46

  Cai, Zhen ^a   Zhang, Bo ^a   Li, Yin ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Anaerobic xylose metabolism; Evolutionary engineering; Lignocellulosic ethanol; Metabolic engineering; Saccharomyces cerevisiae

Indexed keywords

COMPARATIVE ANALYSIS; ENERGY CRISIS; ETHANOL YIELD; EVOLUTIONARY ENGINEERING; LIGNOCELLULOSIC BIOMASS; LIGNOCELLULOSIC HYDROLYSATES; METABOLIC ENGINEERING; S.CEREVISIAE; SUSTAINABLE SOLUTION; XYLOSE FERMENTATION;

ENERGY POLICY; ENGINEERING; ETHANOL; FERMENTATION; METABOLISM; STRAIN;

YEAST;

ALCOHOL; ALCOHOL DEHYDROGENASE; LIGNOCELLULOSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; XYLITOL; XYLOSE;

ALCOHOL PRODUCTION; ANAEROBIC FERMENTATION; ANAEROBIC GROWTH; BACTERIAL GENE; BACTERIAL STRAIN; CELL METABOLISM; CELL TRANSPORT; COMPARATIVE STUDY; DIFFUSION; ENGINEERING; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE;

FERMENTATION; GENETIC ENGINEERING; HUMANS; SACCHAROMYCES CEREVISIAE; XYLOSE;

SACCHAROMYCES CEREVISIAE;

EID: 84862922807     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201100053     Document Type: Review

References (66)

1. Olsson, L., Nielsen, J., The role of metabolic engineering in the improvement of Saccharomyces cerevisiae: Utilization of industrial media. Enzyme Microb. Technol. 2000, 26, 785-792.
2. Pettersen, R., The chemical composition of wood. Adv. Chem. Ser. 1984, 57-126.
3. Carroll, A., Somerville, C., Cellulosic biofuels. Ann. Rev. Plant Biol. 2009, 60, 165-182.
4. Jeffries, T. W., Engineering yeasts for xylose metabolism. Curr. Opin. Biotechnol. 2006, 17, 320-326.
5. Matsushika, A., Inoue, H., Kodaki, T., Sawayama, S., Ethanol production from xylose in engineered Saccharomyces cerevisiae strains: Current state and perspectives. Appl. Microbiol. Biotechnol. 2009, 84, 37-53.
6. Jeffries, T. W., Jin, Y. S., Metabolic engineering for improved fermentation of pentoses by yeasts. Appl. Microbiol. Biotechnol. 2004, 63, 495-509.
7. Hahn-Hagerdal, B., Karhumaa, K., Jeppsson, M., Gorwa-Grauslund, M. F., Metabolic engineering for pentose utilization in Saccharomyces cerevisiae. Adv. Biochem. Eng. Biotechnol. 2007, 108, 147-177.
8. Toivari, M. H., Aristidou, A., Ruohonen, L., Penttila, M., Conversion of xylose to ethanol by recombinant Saccharomyces cerevisiae: Importance of xylulokinase (XKS1) and oxygen availability. Metab. Eng. 2001, 3, 236-249.
9. Jin, Y. S., Jones, S., Shi, N. Q., Jeffries, T. W., Molecular cloning of XYL3 (D-XK) from Pichia stipitis and characterization of its physiological function. Appl. Environ. Microbiol. 2002, 68, 1232-1239.
10. Ni, H., Laplaza, J. M., Jeffries, T. W., Transposon mutagenesis to improve the growth of recombinant Saccharomyces cerevisiae on D-xylose. Appl. Environ. Microbiol. 2007, 73, 2061-2066.
11. Kuyper, M., Winkler, A. A., van Dijken, J. P., Pronk, J. T., Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: A proof of principle. FEMS Yeast Res. 2004, 4, 655-664.
12. Sonderegger, M., Jeppsson, M., Larsson, C., Gorwa-Grauslund, M. F. et al., Fermentation performance of engineered and evolved xylose-fermenting Saccharomyces cerevisiae strains. Biotechnol. Bioeng. 2004, 87, 90-98.
13. Matsushika, A., Inoue, H., Murakami, K., Takimura, O. et al., Bioethanol production performance of five recombinant strains of laboratory and industrial xylose-fermenting Saccharomyces cerevisiae. Bioresour. Technol. 2009, 100, 2392-2398.
14. +-dependent xylitol dehydrogenase gene. Appl. Environ. Microbiol. 2009, 75, 3818-3822.
15. Garay-Arroyo, A., Covarrubias, A. A., Clark, I., Nino, I. et al., Response to different environmental stress conditions of industrial and laboratory Saccharomyces cerevisiae strains. Appl. Microbiol. Biotechnol. 2004, 63, 734-741.
16. Nilsson, A., Gorwa-Grauslund, M. F., Hahn-Hagerdal, B., Liden, G., Cofactor dependence in furan reduction by Saccharomyces cerevisiae in fermentation of acid-hydrolyzed lignocellulose. Appl. Environ. Microbiol. 2005, 71, 7866-7871.
17. Hahn-Hagerdal, B., Karhumaa, K., Fonseca, C., Spencer-Martins, I. et al., Towards industrial pentose-fermenting yeast strains. Appl. Microbiol. Biotechnol. 2007, 74, 937-953.
18. Bell, P. J., Higgins, V. J., Attfield, P. V., Comparison of fermentative capacities of industrial baking and wild-type yeasts of the species Saccharomyces cerevisiae in different sugar media. Lett. Appl. Microbiol. 2001, 32, 224-229.
19. Rollini, M., Casiraghi, E., Pagani, M. A., Manzoni, M., Technological performances of commercial yeast strains in different complex dough formulations. Eur. Food Res. Technol. 2007, 226, 19-24.
20. Almeida, J. R., Karhumaa, K., Bengtsson, O., Gorwa-Grauslund, M. F., Screening of Saccharomyces cerevisiae strains with respect to anaerobic growth in non-detoxified lignocellulose hydrolysate. Bioresour. Technol. 2009, 100, 3674-3677.
21. Futcher, A. B., Cox, B. S., Copy number and the stability of 2-micron circle-based artificial plasmids of Saccharomyces cerevisiae. J. Bacteriol. 1984, 157, 283-290.
22. Zhang, Z., Moo-Young, M., Chisti, Y., Plasmid stability in recombinant Saccharomyces cerevisiae. Biotechnol. Adv. 1996, 14, 401-435.
23. Brat, D., Boles, E., Wiedemann, B., Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2009, 75, 2304-2311.
24. Zaldivar, J., Borges, A., Johansson, B., Smits, H. P. et al., Fermentation performance and intracellular metabolite patterns in laboratory and industrial xylose-fermenting Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 2002, 59, 436-442.
25. Ganga, M. A., Pinaga, F., Valles, S., Ramon, D., Querol, A., Aroma improving in microvinification processes by the use of a recombinant wine yeast strain expressing the Aspergillus nidulans xlnA gene. Int. J. Food Microbiol. 1999, 47, 171-178.
26. Karhumaa, K., Garcia Sanchez, R., Hahn-Hagerdal, B., Gorwa-Grauslund, M. F., Comparison of the xylose reductase-xylitol dehydrogenase and the xylose isomerase pathways for xylose fermentation by recombinant Saccharomyces cerevisiae. Microb. Cell Fact. 2007, 6, 5.
27. Ohgren, K., Bengtsson, O., Gorwa-Grauslund, M. F., Galbe, M. et al., Simultaneous saccharification and co-fermentation of glucose and xylose in steam-pretreated corn stover at high fiber content with Saccharomyces cerevisiae TMB3400. J. Biotechnol. 2006, 126, 488-498.
28. Sedlak, M., Ho, N. W., Production of ethanol from cellulosic biomass hydrolysates using genetically engineered Saccharomyces yeast capable of cofermenting glucose and xylose. Appl. Biochem. Biotechnol. 2004, 114, 403-416.
29. Katahira, S., Mizuike, A., Fukuda, H., Kondo, A., Ethanol fermentation from lignocellulosic hydrolysate by a recombinant xylose- and cellooligosaccharide-assimilating yeast strain. Appl. Microbiol. Biotechnol. 2006, 72, 1136-1143.
30. Alexander, N. J., Acetone stimulation of ethanol production from d-xylose by Pachysolen tannophilus. Appl. Microbiol. Biotechnol. 1986, 25, 203-207.
31. Ligthelm, M. E., Prior, B. A., du Preez, J. C., Effect of hydrogen acceptors on D-xylose fermentation by anaerobic culture of immobilized Pachysolen tannophilus cells. Biotechnol. Bioeng. 1989, 33, 839-944.
32. Wahlbom, C. F., Hahn-Hagerdal, B., Furfural, 5-hydroxymethyl furfural, and acetoin act as external electron acceptors during anaerobic fermentation of xylose in recombinant Saccharomyces cerevisiae. Biotechnol. Bioeng. 2002, 78, 172-178.
33. Lee, W. J., Kim, M. D., Ryu, Y. W., Bisson, L. F., Seo, J. H., Kinetic studies on glucose and xylose transport in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 2002, 60, 186-191.
34. Saloheimo, A., Rauta, J., Stasyk, O. V., Sibirny, A. A. et al., Xylose transport studies with xylose-utilizing Saccharomyces cerevisiae strains expressing heterologous and homologous permeases. Appl. Microbiol. Biotechnol. 2007, 74, 1041-1052.
35. Hamacher, T., Becker, J., Gardonyi, M., Hahn-Hagerdal, B., Boles, E., Characterization of the xylose-transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 2002, 148, 2783-2788.
36. Weierstall, T., Hollenberg, C. P., Boles, E., Cloning and characterization of three genes (SUT1-3) encoding glucose transporters of the yeast Pichia stipitis. Mol. Microbiol. 1999, 31, 871-883.
37. Leandro, M. J., Goncalves, P., Spencer-Martins, I., Two glucose/xylose transporter genes from the yeast Candida intermedia: First molecular characterization of a yeast xylose-H+ symporter. Biochem. J. 2006, 395, 543-549.
38. Hector, R. E., Qureshi, N., Hughes, S. R., Cotta, M. A., Expression of a heterologous xylose transporter in a Saccharomyces cerevisiae strain engineered to utilize xylose improves aerobic xylose consumption. Appl. Microbiol. Biotechnol. 2008, 80, 675-684.
39. Sedlak, M., Ho, N. W., Characterization of the effectiveness of hexose transporters for transporting xylose during glucose and xylose co-fermentation by a recombinant Saccharomyces yeast. Yeast 2004, 21, 671-684.
40. Gardonyi, M., Jeppsson, M., Liden, G., Gorwa-Grauslund, M. F., Hahn-Hagerdal, B., Control of xylose consumption by xylose transport in recombinant Saccharomyces cerevisiae. Biotechnol. Bioeng. 2003, 82, 818-824.
41. Runquist, D., Fonseca, C., Radstrom, P., Spencer-Martins, I., Hahn-Hagerdal, B., Expression of the Gxf1 transporter from Candida intermedia improves fermentation performance in recombinant xylose-utilizing Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 2009, 82, 123-130.
42. Liang, L., Zhang, J., Lin, Z., Altering coenzyme specificity of Pichia stipitis xylose reductase by the semi-rational approach CASTing. Microb. Cell Fact. 2007, 6, 36.
43. Watanabe, S., Abu Saleh, A., Pack, S. P., Annaluru, N. et al., Ethanol production from xylose by recombinant Saccharomyces cerevisiae expressing protein-engineered NADH-preferring xylose reductase from Pichia stipitis. Microbiology 2007, 153, 3044-3054.
44. Watanabe, S., Kodaki, T., Makino, K., Complete reversal of coenzyme specificity of xylitol dehydrogenase and increase of thermostability by the introduction of structural zinc. J. Biol. Chem. 2005, 280, 10340-10349.
45. Jeppsson, M., Johansson, B., Hahn-Hagerdal, B., Gorwa-Grauslund, M. F., Reduced oxidative pentose phosphate pathway flux in recombinant xylose-utilizing Saccharomyces cerevisiae strains improves the ethanol yield from xylose. Appl. Environ. Microbiol. 2002, 68, 1604-1609.
46. Verho, R., Londesborough, J., Penttila, M., Richard, P., Engineering redox cofactor regeneration for improved pentose fermentation in Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2003, 69, 5892-5897.
47. Bro, C., Regenberg, B., Forster, J., Nielsen, J., In silico aided metabolic engineering of Saccharomyces cerevisiae for improved bioethanol production. Metab. Eng. 2006, 8, 102-111.
48. Sauer, U., Evolutionary engineering of industrially important microbial phenotypes. Adv. Biochem. Eng. Biotechnol. 2001, 73, 129-169.
49. Sonderegger, M., Sauer, U., Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl. Environ. Microbiol. 2003, 69, 1990-1998.
50. Sonderegger, M., Jeppsson, M., Hahn-Hagerdal, B., Sauer, U., Molecular basis for anaerobic growth of Saccharomyces cerevisiae on xylose, investigated by global gene expression and metabolic flux analysis. Appl. Environ. Microbiol. 2004, 70, 2307-2317.
51. Donalies, U. E., Nguyen, H. T., Stahl, U., Nevoigt, E., Improvement of Saccharomyces yeast strains used in brewing, wine making and baking. Adv. Biochem. Eng. Biotechnol. 2008, 111, 67-98.
52. Atsumi, S., Cann, A. F., Connor, M. R., Shen, C. R. et al., Metabolic engineering of Escherichia coli for 1-butanol production. Metab. Eng. 2008, 10, 305-311.
53. Inui, M., Suda, M., Kimura, S., Yasuda, K. et al., Expression of Clostridium acetobutylicum butanol synthetic genes in Escherichia coli. Appl. Microbiol. Biotechnol. 2008, 77, 1305-1316.
54. Bond-Watts, B. B., Bellerose, R. J., Chang, M. C., Enzyme mechanism as a kinetic control element for designing synthetic biofuel pathways. Nat. Chem. Biol. 2011, 7, 222-227.
55. Suh, S. O., McHugh, J. V., Pollock, D. D., Blackwell, M., The beetle gut: A hyperdiverse source of novel yeasts. Mycol. Res. 2005, 109, 261-265.
56. Suh, S. O., White, M. M., Nguyen, N. H., Blackwell, M., The status and characterization of Enteroramus dimorphus: A xylose-fermenting yeast attached to the gut of beetles. Mycologia 2004, 96, 756-760.
57. Suh, S. O., McHugh, J. V., Blackwell, M., Expansion of the Candida tanzawaensis yeast clade: 16 Novel Candida species from basidiocarp-feeding beetles. Int. J. Syst. Evol. Microbiol. 2004, 54, 2409-2429.
58. Suh, S. O., Marshall, C. J., McHugh, J. V., Blackwell, M., Wood ingestion by passalid beetles in the presence of xylose-fermenting gut yeasts. Mol. Ecol. 2003, 12, 3137-3145.
59. Ho, N. W., Chen, Z., Brainard, A. P., Genetically engineered Saccharomyces yeast capable of effective cofermentation of glucose and xylose. Appl. Environ. Microbiol. 1998, 64, 1852-1859.
60. Wahlbom, C. F., van Zyl, W. H., Jonsson, L. J., Hahn-Hagerdal, B. et al., 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. 2003, 3, 319-326.
61. Traff, K. L., Otero Cordero, R. R., van Zyl, W. H., Hahn-Hagerdal, B., 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. 2001, 67, 5668-5674.
62. Madhavan, A., Tamalampudi, S., Ushida, K., Kanai, D. et al., Xylose isomerase from polycentric fungus Orpinomyces: Gene sequencing, cloning, and expression in Saccharomyces cerevisiae for bioconversion of xylose to ethanol. Appl. Microbiol. Biotechnol. 2009, 82, 1067-1078.
63. Madhavan, A., Tamalampudi, S., Srivastava, A., Fukuda, H. et al., Alcoholic fermentation of xylose and mixed sugars using recombinant Saccharomyces cerevisiae engineered for xylose utilization. Appl. Microbiol. Biotechnol. 2009, 82, 1037-1047.
64. Kuyper, M., Hartog, M. M., Toirkens, M. J., Almering, M. J. et al., Metabolic engineering of a xylose-isomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation. FEMS Yeast Res. 2005, 5, 399-409.
65. Kuyper, M., Toirkens, M. J., Diderich, J. A., Winkler, A. A. et al., Evolutionary engineering of mixed-sugar utilization by a xylose-fermenting Saccharomyces cerevisiae strain. FEMS Yeast Res. 2005, 5, 925-934.
66. Verduyn, C., Postma, E., Scheffers, W. A., Van Dijken, J. P., Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 1992, 8, 501-517.