Simultaneously improving xylose fermentation and tolerance to lignocellulosic inhibitors through evolutionary engineering of recombinant Saccharomyces cerevisiae harbouring xylose isomerase

BMC Biotechnology

Volumn 14, Issue , 2014, Pages

  Smith, Justin ^a   van Rensburg, Eugéne ^a   Görgens, Johann F ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

Author keywords

EMS; Evolutionary engineering; Lignocellulose; Random mutagenesis; Saccharomyces cerevisiae; Triticale hydrolysate; Yeast hardening

Indexed keywords

BATCH CELL CULTURE; CARBON; CELLULOSE; CHEMOSTATS; ENGINEERING; ETHANOL; FERMENTATION; LIGNIN; MUTAGENESIS; YEAST;

EMS; EVOLUTIONARY ENGINEERING; LIGNOCELLULOSE; RANDOM MUTAGENESIS; TRITICALE HYDROLYSATE;

XYLOSE;

ACETIC ACID; BAGASSE; FURFURAL; LIGNOCELLULOSE; MESYLIC ACID ETHYL ESTER; PENTOSE; STEROID 5ALPHA REDUCTASE; XYLOSE; XYLOSE ISOMERASE; ISOMERASE; LIGNIN; RECOMBINANT PROTEIN;

AEROBIC FERMENTATION; AEROBIC METABOLISM; ALCOHOL PRODUCTION; ARTICLE; BACTERIUM CULTURE; CHEMOSTAT; CONTINUOUS CULTURE; DILUTION; FUNGAL STRAIN; FUNGUS GROWTH; LIQUID; MUTAGENESIS; NONHUMAN; SACCHARIFICATION; SACCHAROMYCES CEREVISIAE; SORGHUM; TRITICALE; YEAST; BATCH CELL CULTURE; BIOMASS; BIOSYNTHESIS; CHEMISTRY; GENETIC ENGINEERING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION;

SACCHAROMYCES CEREVISIAE; TRITICOSECALE;

ALDOSE-KETOSE ISOMERASES; BATCH CELL CULTURE TECHNIQUES; BIOMASS; EVOLUTION, MOLECULAR; GENETIC ENGINEERING; LIGNIN; MUTAGENESIS; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; XYLOSE;

EID: 84900839963     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-14-41     Document Type: Article

References (72)

1. Hahn-Hägerdal B, Wahlbom C, Gárdonyi M, van Zyl W, Cordero Otero R, Jönsson L. Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Adv Biochem Eng Biotechnol 2001, 73:53-84.
2. Hahn-Hägerdal B, Pamment N. Microbial pentose metabolism. Appl Biochem Biotechnol 2004, 116:1207-1209.
3. Lynd LR, Weimer PJ, Van Zyl WH, Pretorius IS. Microbial cellulose utilization: Fundamentals and biotechnology. Microbiol Mol Biol Rev 2002, 66:506-577. 10.1128/MMBR.66.3.506-577.2002, 120791, 12209002.
4. Stephanopoulos G, Aristidou AA, Nielsen J. Metabolic engineering: principles and methodologies 1998, San Diego: Academic.
5. von Sivers M, Zacchi G, Olsson L, Hahn-Hägerdal B. Cost analysis of ethanol production from willow using recombinant Escherichia coli. Biotechnol Prog 1994, 10:555-560. 10.1021/bp00029a017, 7765380.
6. Almeida J, Modig T, Petersson A, Hahn-Hägerdal B, Lidén G, Gorwa-Grauslund M. Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 2007, 82:340-349.
7. Larsson S, Reimann A, Nilvebrant NO, Jönsson LJ. Comparison of different methods for the detoxification of lignocellulose hydrolyzates of spruce. Appl Biochem Biotechnol 1999, 77:91-103.
8. Palmqvist E, Hahn-Hägerdal B. Fermentation of lignocellulosic hydrolysates. II: inhibitors and mechanisms of inhibition. Bioresour Technol 2000, 74:25-33.
9. Parajó J, Domínguez H, Domínguez J. Biotechnological production of xylitol. Part 3: operation in culture media made from lignocellulose hydrolysates. Bioresour Technol 1998, 66:25-40.
10. Wahlbom C, van Zyl W, Jönsson L, Hahn-Hägerdal B, Otero R. 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. 10.1016/S1567-1356(02)00206-4, 12689639.
11. Kuyper M, Winkler AA, Dijken JP, Pronk JT. Minimal metabolic engineering of Saccharomyces cerevisiae for efficient anaerobic xylose fermentation: a proof of principle. FEMS Yeast Res 2004, 4:655-664. 10.1016/j.femsyr.2004.01.003, 15040955.
12. Gorsich SW, Dien BS, Nichols NN, Slininger PJ, Liu ZL, Skory CD. Tolerance to furfural-induced stress is associated with pentose phosphate pathway genes ZWF1, GND1, RPE1, and TKL1 in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 2006, 71:339-349. 10.1007/s00253-005-0142-3, 16222531.
13. Toivari MH, Salusjarvi LS, Ruohonen L, Penttila M. Endogenous xylose pathway in Saccharomyces cerevisiae. Appl Environ Microbiol 2004, 70:3681-3686. 10.1128/AEM.70.6.3681-3686.2004, 427740, 15184173.
14. Sauer U. Evolutionary engineering of industrially important microbial phenotypes. Adv Biochem Eng Biotechnol 2001, 73:129-169.
15. Nevoigt E. Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiol Mol Biol Rev 2008, 72:379-412. 10.1128/MMBR.00025-07, 2546860, 18772282.
16. Demeke MM, Dietz H, Li Y, Foulquié-Moreno MR, Mutturi S, Deprez S, Den Abt T, Bonini BM, Lidén G, Dumortier F, Verplaetse A, Boles E, Thevelein JM. Development of a D-xylose fermenting and inhibitor tolerant industrial Saccharomyces cerevisiae strain with high performance in lignocellulose hydrolysates using metabolic and evolutionary engineering. Biotechnol Biofuels 2013, 6:89. 10.1186/1754-6834-6-89, 3698012, 23800147.
17. Heer D, Sauer U. Identification of furfural as a key toxin in lignocellulosic hydrolysates and evolution of a tolerant yeast strain. Microb Biotechnol 2008, 1:497-506. 10.1111/j.1751-7915.2008.00050.x, 3815291, 21261870.
18. Koppram R, Albers E, Olsson L. Evolutionary engineering strategies to enhance tolerance of xylose utilizing recombinant yeast to inhibitors derived from spruce biomass. Biotechnol Biofuels 2012, 5:32. 10.1186/1754-6834-5-32, 3408370, 22578262.
19. Eliasson A, Christensson C, Wahlbom CF, Hahn-Hägerdal B. Anaerobic xylose fermentation by recombinant Saccharomyces cerevisiae carrying XYL1, XYL2, and XKS1 in mineral medium chemostat cultures. Appl Environ Microbiol 2000, 66:3381-3386. 10.1128/AEM.66.8.3381-3386.2000, 92159, 10919795.
20. Sonderegger M, Sauer U. Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl Environ Microbiol 2003, 69:1990-1998. 10.1128/AEM.69.4.1990-1998.2003, 154834, 12676674.
21. Martín C, Marcet M, Almazán O, Jönsson LJ. Adaptation of a recombinant xylose-utilizing Saccharomyces cerevisiae strain to a sugarcane bagasse hydrolysate with high content of fermentation inhibitors. Bioresour Technol 2007, 98:1767-1773. 10.1016/j.biortech.2006.07.021, 16934451.
22. Tomás-Pejó E, Ballesteros M, Oliva J, Olsson L. Adaptation of the xylose fermenting yeast Saccharomyces cerevisiae F12 for improving ethanol production in different fed-batch SSF processes. J Ind Microbiol Biotechnol 2010, 37:1211-1220. 10.1007/s10295-010-0768-8, 20585830.
23. Tantirungkij M, Izuishi T, Seki T, Yoshida T. Fed-batch fermentation of xylose by a fast-growing mutant of xylose-assimilating recombinant Saccharomyces cerevisiae. Appl Microbiol Biotechnol 1994, 41:8-12.
24. Pitkänen JP, Rintala E, Aristidou A, Ruohonen L, Penttilä M. Xylose chemostat isolates of Saccharomyces cerevisiae show altered metabolite and enzyme levels compared with xylose, glucose, and ethanol metabolism of the original strain. Appl Microbiol Biotechnol 2005, 67:827-837. 10.1007/s00253-004-1798-9, 15630585.
25. Zha J, Shen M, Hu M, Song H, Yuan Y. Enhanced expression of genes involved in initial xylose metabolism and the oxidative pentose phosphate pathway in the improved xylose-utilizing Saccharomyces cerevisiae through evolutionary engineering. J Ind Microbiol Biotechnol 2014, 41:27-39. 10.1007/s10295-013-1350-y, 24113893.
26. Liu E, Hu Y. Construction of a xylose-fermenting Saccharomyces cerevisiae strain by combined approaches of genetic engineering, chemical mutagenesis and evolutionary adaptation. Biochem Eng J 2010, 48:204-210.
27. Laplace JM, Delgenes JP, Moletta R, Navarro JM. Fermentation of lignocellulosic sugars to ethanol: Selection of mutants of Pichia stipitis affected for D-glucose utilization. Enzyme Microb Technol 1992, 14:644-648.
28. James AP, Zahab DM, Mahmourides G, Maleszka R, Schneider H. Genetic and biochemical characterization of mutations affecting the ability of the yeast Pachysolen tannophilus to metabolize D-xylose. Appl Environ Microbiol 1989, 55:2871-2876. 203183, 16348049.
29. Amartey S, Jeffries T. An improvement in Pichia stipitis fermentation of acid-hydrolysed hemicellulose achieved by overliming (calcium hydroxide treatment) and strain adaptation. World J Microbiol Biotechnol 1996, 12:281-283. 10.1007/BF00360928, 24415238.
30. Almario MP, Reyes LH, Kao KC. Evolutionary engineering of Saccharomyces cerevisiae for enhanced tolerance to hydrolysates of lignocellulosic biomass. Biotechnol Bioeng 2013, 110:2616-2623. 10.1002/bit.24938, 23613173.
31. Almeida J, Bertilsson M, Gorwa-Grauslund M, Gorsich S, Lidén G. Metabolic effects of furaldehydes and impacts on biotechnological processes. Appl Microbiol Biotechnol 2009, 82:625-638. 10.1007/s00253-009-1875-1, 19184597.
32. Wisselink HW, Toirkens MJ, Wu Q, Pronk JT, van Maris AJ. Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl Environ Microbiol 2009, 75:907-914. 10.1128/AEM.02268-08, 2643596, 19074603.
33. Zhou H, Cheng J, Wang BL, Fink GR, Stephanopoulos G. Xylose isomerase overexpression along with engineering of the pentose phosphate pathway and evolutionary engineering enable rapid xylose utilization and ethanol production by Saccharomyces cerevisiae. Metab Eng 2012, 14:611-622. 10.1016/j.ymben.2012.07.011, 22921355.
34. Demeke MM, Dumortier F, Li Y, Broeckx T, Foulquie-Moreno R, Thevelein JM. Combining inhibitor tolerance and D-xylose fermentation in industrial Saccharomyces cerevisiae for efficient lignocellulose-based bioethanol production. Biotechnol Biofuels 2013, 6:120. 10.1186/1754-6834-6-120, 3765968, 23971950.
35. Bobleter O. Hydrothermal degradation of polymers derived from plants. Prog Polym Sci 1994, 19:797-841.
36. Garrote G, Dominguez H, Parajo JC. Hydrothermal processing of lignocellulosic materials. Eur J Wood Prod 1999, 57:191-202.
37. Gupta R, Khasa YP, Kuhad RC. Evaluation of pretreatment methods in improving the enzymatic saccharification of cellulosic materials. Carbohydr Polym 2011, 84:1103-1109.
38. Samuel R, Foston M, Jaing N, Cao S, Allison L, Studer M, Wyman C, Ragauskas AJ. HSQC (heteronuclear single quantum coherence) 13C-1H correlation spectra of whole biomass in perdeuterated pyridinium chloride-DMSO system: an effective tool for evaluating pretreatment. Fuel 2011, 90:2836-2842.
39. Taylor MP, Mulako I, Tuffin M, Cowan D. Understanding physiological responses to pre-treatment inhibitors in ethanologenic fermentations. Biotechnol J 2012, 7:1169-1181. 10.1002/biot.201100335, 22331581.
40. Favaro L, Basaglia M, van Zyl W, Casella S. Using an efficient fermenting yeast enhances ethanol production from unfiltered wheat bran hydrolysates. Appl Energy 2013, 102:170-178.
41. van Zyl J, van Rensburg E, van Zyl W, Harms T, Lynd L. A kinetic model for simultaneous saccharification and fermentation of avicel with Saccharomyces cerevisiae. Biotechnol Bioeng 2011, 108:924-933. 10.1002/bit.23000, 21404265.
42. Wahlbom C, Hahn-Hägerdal 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. 10.1002/bit.10188, 11870608.
43. Kuyper M, Hartog MM, Toirkens MJ, Almering MJ, Winkler AA, Dijken JP, Pronk JT. Metabolic engineering of a xylose-isomerase-expressing Saccharomyces cerevisiae strain for rapid anaerobic xylose fermentation. FEMS Yeast Res 2005, 5:399-409. 10.1016/j.femsyr.2004.09.010, 15691745.
44. Harder W, Kuenen JG, Matin A. A review. Microbial selection in continuous culture. J Appl Bacteriol 1977, 43:1-24. 10.1111/j.1365-2672.1977.tb00717.x, 332677.
45. Taherzadeh MJ, Gustafsson L, Niklasson C, Lidén G. Physiological effects of 5-hydroxymethylfurfural on Saccharomyces cerevisiae. Appl Microbiol Biotechnol 2000, 53:701-708. 10.1007/s002530000328, 10919330.
46. Keller FA, Bates D, Ruiz R, Nguyen Q. Yeast adaptation on softwood prehydrolysate. Appl Biochem Biotechnol 1998, 70:137-148.
47. Liu ZL, Slininger PJ, Gorsich SW. Enhanced biotransformation of furfural and hydroxymethylfurfural by newly developed ethanologenic yeast strains. Appl Biochem Biotechnol 2005, 121-124:451-460.
48. Jeffries T, Shi N-Q. Genetic engineering for improved xylose fermentation by yeasts. Adv Biochem Eng Biotechnol 1999, 65:117-161.
49. Souto-Maior AM, Runquist D, Hahn-Hägerdal B. Crabtree-negative characteristics of recombinant xylose-utilizing Saccharomyces cerevisiae. J Biotechnol 2009, 143:119-123. 10.1016/j.jbiotec.2009.06.022, 19560495.
50. Liu ZL. Molecular mechanisms of yeast tolerance and in situ detoxification of lignocellulose hydrolysates. Appl Microbiol Biotechnol 2011, 90:809-825. 10.1007/s00253-011-3167-9, 21380517.
51. Klinke HB, Thomsen AB, Ahring BK. Inhibition of ethanol-producing yeast and bacteria by degradation products produced during pre-treatment of biomass. Appl Microbiol Biotechnol 2004, 66:10-26. 10.1007/s00253-004-1642-2, 15300416.
52. Palmqvist E, Grage H, Meinander NQ, Hahn-Hägerdal B. Main and interaction effects of acetic acid, furfural, and ρ-hydroxybenzoic acid on growth and ethanol productivity of yeasts. Biotechnol Bioeng 1999, 63:46-55. 10.1002/(SICI)1097-0290(19990405)63:1<46::AID-BIT5>3.0.CO;2-J, 10099580.
53. Helle S, Cameron D, Lam J, White B, Duff S. Effect of inhibitory compounds found in biomass hydrolysates on growth and xylose fermentation by a genetically engineered strain of S. cerevisiae. Enzyme Microb Technol 2003, 33:786-792.
54. Brandberg T, Franzén CJ, Gustafsson L. The fermentation performance of nine strains of Saccharomyces cerevisiae in batch and fed-batch cultures in dilute-acid wood hydrolysate. J Biosci Bioeng 2004, 98:122-125. 10.1016/S1389-1723(04)70252-2, 16233676.
55. Liu ZL, Slininger PJ, Dien BS, Berhow MA, Kurtzman CP, Gorsich SW. Adaptive response of yeasts to furfural and 5-hydroxymethylfurfural and new chemical evidence for HMF conversion to 2,5-bis-hydroxymethylfuran. J Ind Microbiol Biotechnol 2004, 31:345-352.
56. Larroy C, Fernández M, González E, Parás X, Biosca JA. Characterization of the Saccharomyces cerevisiae YMR318C (ADH6) gene product as a broad specificity NADPH-dependent alcohol dehydrogenase: relevance in aldehyde reduction. Biochem J 2002, 361:163-172. 10.1042/0264-6021:3610163, 1222291, 11742541.
57. Larroy C, Pares X, Biosca JA. Characterization of a Saccharomyces cerevisiae NADP (H)-dependent alcohol dehydrogenase (ADHVII), a member of the cinnamyl alcohol dehydrogenase family. Eur J Biochem 2002, 269:5738-5745. 10.1046/j.1432-1033.2002.03296.x, 12423374.
58. Liu ZL, Moon J, Andersh BJ, Slininger PJ, Weber S. Multiple gene-mediated NAD (P) H-dependent aldehyde reduction is a mechanism of in situ detoxification of furfural and 5-hydroxymethylfurfural by Saccharomyces cerevisiae. Appl Microbiol Biotechnol 2008, 81:743-753. 10.1007/s00253-008-1702-0, 18810428.
59. Petersson A, Almeida J, Modig T, Karhumaa K, Hahn-Hägerdal B, Gorwa-Grauslund M, Lidén G. A 5-hydroxymethyl furfural reducing enzyme encoded by the Saccharomyces cerevisiae ADH6 gene conveys HMF tolerance. Yeast 2006, 23:455-464. 10.1002/yea.1370, 16652391.
60. Kuhn A, van Zyl C, van Tonder A, Prior BA. Purification and partial characterization of an aldo-keto reductase from Saccharomyces cerevisiae. Appl Environ Microbiol 1995, 61:1580-1585. 167412, 7747971.
61. Walfridsson M, Bao X, Anderlund M, Lilius G, Bülow L, Hahn-Hägerdal B. Ethanolic fermentation of xylose with Saccharomyces cerevisiae harboring the Thermus thermophilus xylA gene, which expresses an active xylose (glucose) isomerase. Appl Environ Microbiol 1996, 62:4648-4651. 168291, 8953736.
62. Taherzadeh MJ, Karimi K. Fermentation inhibitors in ethanol processes and different strategies to reduce their effects. Biofuels: Alternative feedstocks and conversion processes 2011, 287-311. Oxford: Academic, Pandey A, Larroche C, Ricke S, Dussap C, Gnansounou E.
63. Olofsson K, Rudolf A, Lidén G. Designing simultaneous saccharification and fermentation for improved xylose conversion by a recombinant strain of Saccharomyces cerevisiae. J Biotechnol 2008, 134:112-120. 10.1016/j.jbiotec.2008.01.004, 18294716.
64. Öhgren K, Bengtsson O, Gorwa-Grauslund M, Galbe M, Hahn-Hägerdal B, Zacchi G. 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. 10.1016/j.jbiotec.2006.05.001, 16828190.
65. Ballesteros M, Oliva J, Negro M, Manzanares P, Ballesteros I. Ethanol from lignocellulosic materials by a simultaneous saccharification and fermentation process (SFS) with Kluyveromyces marxianus CECT 10875. Process Biochem 2004, 39:1843-1848.
66. Shen F, Hu J, Zhong Y, Liu ML, Saddler JN, Liu R. Ethanol production from steam-pretreated sweet sorghum bagasse with high substrate consistency enzymatic hydrolysis. Biomass Bioenergy 2012, 41:157-164.
67. Sedlak M, Ho N. Production of ethanol from cellulosic biomass hydrolysates using genetically engineered Saccharomyces yeast capable of cofermenting glucose and xylose. Appl Biochem Biotechnol 2004, 113-116:403-416.
68. Yu L, Pei X, Lei T, Wang Y, Feng Y. Genome shuffling enhanced L-lactic acid production by improving glucose tolerance of Lactobacillus rhamnosus. J Biotechnol 2008, 134:154-159. 10.1016/j.jbiotec.2008.01.008, 18289712.
69. de Villiers G. Development of recombinant Saccharomyces cerevisiae for improved D-xylose utilisation 2006, Stellenbosch: Stellenbosch University, Microbiology Department, MSc thesis.
70. Verduyn C, Postma E, Scheffers WA, van Dijken JP. 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. 10.1002/yea.320080703, 1523884.
71. Winston F. EMS and UV mutagenesis in yeast. Curr Protoc Mol Biol 2008, 82:13.3B.1-13.3B.5.
72. Cannella D, Hsieh CW, Felby C, Jørgensen H. Production and effect of aldonic acids during enzymatic hydrolysis of lignocellulose at high dry matter content. Biotechnol Biofuels 2012, 5:26. 10.1186/1754-6834-5-26, 3458932, 22546481.