Fermentation of glucose-xylose-Arabinose mixtures by a synthetic consortium of single-sugar-fermenting Saccharomyces cerevisiae strains

FEMS Yeast Research

Volumn 18, Issue 8, 2018, Pages

  Verhoeven, Maarten D ^a   De Valk, Sophie C ^a   Daran, Jean Marc G ^a   Van Maris, Antonius J A ^a   Pronk, Jack T ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Bioethanol; Division of labour; Evolutionary engineering; Pentose fermentation; Synthetic consortium; Yeast

Indexed keywords

ARABINOSE; CARBON DIOXIDE; GLUCOSE; HEXOSE; PENTOSE; SUGAR; XYLITOL; XYLOSE;

ANAEROBIC FERMENTATION; ANAEROBIC GROWTH; ARTICLE; BACTERIUM CULTURE; BIOMASS; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FERMENTATION; GLUCOSE INTAKE; INCUBATION TIME; KINETICS; MIXED CELL CULTURE; NONHUMAN; PH; SACCHAROMYCES CEREVISIAE; GROWTH, DEVELOPMENT AND AGING; METABOLIC ENGINEERING; METABOLISM; MICROBIAL CONSORTIUM;

ANAEROBIOSIS; ARABINOSE; FERMENTATION; GLUCOSE; METABOLIC ENGINEERING; MICROBIAL CONSORTIA; SACCHAROMYCES CEREVISIAE; XYLOSE;

EID: 85055076960     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1093/femsyr/foy075     Document Type: Article

References (76)

1. Alper H, Stephanopoulos G. Engineering for biofuels: exploiting innate microbial capacity or importing biosynthetic potential? Nat Rev Microbiol 2009;7:715-23.
2. Becker J, Boles E. A modified Saccharomyces cerevisiae strain that consumes l-Arabinose and produces ethanol. Appl Environ Microb 2003;69:4144-50.
3. Bellissimi E, Van Dijken JP, Pronk JT et al. Effects of acetic acid on the kinetics of xylose fermentation by an engineered, xyloseisomerase-based Saccharomyces cerevisiae strain. FEMS Yeast Res 2009;9:358-64.
4. Berkhout J, Bosdriesz E, Nikerel E et al. How biochemical constraints of cellular growth shape evolutionary adaptations in metabolism. Genetics 2013;194:505-12.
5. Bettiga M, Bengtsson O, Hahn-Hgerdal B et al. Arabinose and xylose fermentation by recombinant Saccharomyces cerevisiae expressing a fungal pentose utilization pathway. Microb Cell Fact 2009;8:40.
6. Boender LG, van Maris AJ, de Hulster EA et al. Cellular responses of Saccharomyces cerevisiae at near-zero growth rates: Transcriptome analysis of anaerobic retentostat cultures. FEMS Yeast Res 2011;11:603-20.
7. Bracher JM, Verhoeven MD, Wisselink HW et al. The Penicillium chrysogenum transporter PcAraT enables high-Affinity, glucose-insensitive l-Arabinose transport in Saccharomyces cerevisiae. Biotechnol Biofuels 2018;11:63.
8. Brat D, Boles E, Wiedemann B. Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl Environ Microb 2009;75:2304-11.
9. Chandrakant P, Bisaria V. Simultaneous bioconversion of cellulose and hemicellulose to ethanol. Crit Rev Biotechnol 1998;18:295-331.
10. Chang Q, Griest TA, Harter TM et al. Functional studies of aldoketo reductases in Saccharomyces cerevisiae. Biochim Biophys Acta 2007;1773:321-9.
11. Chen Y. Development and application of co-culture for ethanol production by co-fermentation of glucose and xylose: A systematic review. J Ind Microbiol Biot 2011;38:581-97.
12. Crook N, Abatemarco J, Sun J et al. In vivo continuous evolution of genes and pathways in yeast. Nat Commun 2016;7:13051.
13. Demeke MM, Foulqui-Moreno MR, Dumortier F et al. Rapid evolution of recombinant Saccharomyces cerevisiae for xylose fermentation through formation of extra-chromosomal circular DNA. PLoS Genet 2015;11:e1005010.
14. Dun B, Wang Z, Ye K et al. Functional expression of Arabidopsis thaliana xylose isomerase in Saccharomyces cerevisiae. Xinjiang Agric Sci 2012;49:681-6.
15. Eiteman MA, Lee SA, Altman E. A co-fermentation strategy to consume sugar mixtures effectively. J Biol Eng 2008;2:3.
16. Eiteman MA, Lee SA, Altman R et al. A substrate-selective cofermentation strategy with Escherichia coli produces lactate by simultaneously consuming xylose and glucose. Biotechnol Bioeng 2009;102:822-7.
17. Entian K-D, K?otter P. 25 Yeast genetic strain and plasmid collections. Method Microbiol 2007;36:629-66.
18. Farwick A, Bruder S, Schadeweg V et al. Engineering of yeast hexose transporters to transport d-xylose without inhibition by d-glucose. Proc Natl Acad Sci USA 2014;111:5159-64.
19. Gietz RD, Schiestl RH, Willems AR et al. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 1995;11:355-60.
20. Gombert AK, van Maris AJ. Improving conversion yield of fermentable sugars into fuel ethanol in 1st generation yeastbased production processes. Curr Opin Biotechnol 2015;33:81-86.
21. Gonzlez-Ramos D, de Vries ARG, Grijseels SS et al. A new laboratory evolution approach to select for constitutive acetic acid tolerance in Saccharomyces cerevisiae and identification of causal mutations. Biotechnol Biofuels 2016;9:173.
22. Grohmann K, Bothast RJ. Pectin-rich residues generated by processing of citrus fruits, apples, and sugar beets. ACS Symposium Series 1994;566:372-90.
23. Grohmann K, Bothast RJ. Saccharification of corn fibre by combined treatment with dilute sulphuric acid and enzymes. Process Biochem 1997;32:405-15.
24. Guadalupe Medina V, Almering MJ, van Maris AJ et al. Elimination of glycerol production in anaerobic cultures of a Saccharomyces cerevisiae strain engineered to use acetic acid as an electron acceptor. Appl Environ Microb 2010;76:190-5.
25. Ha S-J, Kim SR, Choi J-H et al. Xylitol does not inhibit xylose fermentation by engineered Saccharomyces cerevisiae expressing xylA as severely as it inhibits xylose isomerase reaction in vitro. Appl Environ Microb 2011;92:77-84.
26. Hahn-Hgerdal B, Wahlbom CF, G?ardonyiMet al. Metabolic engineering of Saccharomyces cerevisiae for xylose utilization. Adv Biochem Eng Biotechnol 2001;73:53-84.
27. Hamacher T, Becker J, Gardonyi M et al. Characterization of the xylose-Transporting properties of yeast hexose transporters and their influence on xylose utilization. Microbiology 2002;148:2783-8.
28. Hanly TJ, Urello M, Henson MA. Dynamic flux balance modeling of S. cerevisiae and E. coli co-cultures for efficient consumption of glucose/xylose mixtures. Appl Environ Microb 2012;93:2783-8.
29. Hector RE, Dien BS, Cotta MA et al. Growth and fermentation of d-xylose by Saccharomyces cerevisiae expressing a novel d-xylose isomerase originating from the bacterium Prevotella ruminicola TC2-24. Biotechnol Biofuels 2013;6:1.
30. Hou J, Jiao C, Peng B et al. Mutation of a regulator Ask10p improves xylose isomerase activity through up-regulation of molecular chaperones in Saccharomyces cerevisiae. Metab Eng 2016a;38:241-50.
31. Hou J, Shen Y, Jiao C et al. Characterization and evolution of xylose isomerase screened from the bovine rumen metagenome in Saccharomyces cerevisiae. J Biosci Bioeng 2016b;121:160-5.
32. Jansen ML, Bracher JM, Papapetridis I et al. Saccharomyces cerevisiae strains for second-generation ethanol production: from academic exploration to industrial implementation. FEMS Yeast Res 2017;17.
33. Jeffries TW. Engineering yeasts for xylose metabolism. Curr Opin Biotechnol 2006;17:320-6.
34. Knoshaug EP, Vidgren V, Magalhães F et al. Novel transporters from Kluyveromyces marxianus and Pichia guilliermondii expressed in Saccharomyces cerevisiae enable growth on larabinose and d-xylose. Yeast 2015;32:615-28.
35. Kotter P, Ciriacy M. Xylose fermentation by Saccharomyces cerevisiae. Appl Microbiol Biot 1993;38:776-83.
36. Kuyper M, Harhangi HR, Stave AK et al. High-level functional expression of a fungal xylose isomerase: The key to efficient ethanolic fermentation of xylose by? FEMS Yeast Res 2003;4:69-78.
37. Kuyper M, Toirkens MJ, Diderich JA et al. Evolutionary engineering ofmixed-sugar utilization by a xylose-fermenting strain. FEMS Yeast Res 2005;5:925-34.
38. Laplace JM, Delgenes JP, Moletta R et al. Cofermentation of glucose and xylose to ethanol by a respiratory-deficient mutant of Saccharomyces cerevisiae co-cultivated with a xylosefermenting yeast. J Ferment Bioeng 1993;75:207-12.
39. Lee M, Rozeboom HJ, de Waal PP et al. Metal dependence of the xylose isomerase from Piromyces sp. E2 explored by activity profiling and protein crystallography. Biochemistry 2017;56:5991-6005.
40. Lee SM, Jellison T, Alper HS. Directed Evolution of xylose isomerase for improved xylose catabolism and fermentation in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 2012;78:5708-16.
41. Lee SM, Jellison T, Alper HS. Systematic and evolutionary engineering of a xylose isomerase-based pathway in Saccharomyces cerevisiae for efficient conversion yields. Biotechnol Biofuels 2014;7:122.
42. Li J, Xu J, Cai P et al. Functional analysis of two l-Arabinose transporters from filamentous fungi reveals promising characteristics for improved pentose utilization in Saccharomyces cerevisiae. Appl Environ Microb 2015;81:4062-70.
43. Luttik MA, K?otter P, Salomons FA et al. The Saccharomyces cerevisiae ICL2 gene encodes a mitochondrial 2-methylisocitrate lyase involved in propionyl-coenzyme A metabolism. J Bacteriol 2000;182:7007-13.
44. Lynd LR. Overview and evaluation of fuel ethanol from cellulosic biomass: Technology, economics, the environment, and policy. Annu Rev Energy Environ 1996;21:403-65.
45. Madhavan A, Tamalampudi S, Ushida K et al. Xylose isomerase from polycentric fungus Orpinomyces: gene sequencing, cloning, and expression in Saccharomyces cerevisiae for bioconversion of xylose to ethanol. Appl Microbiol Biot 2009;82:1067-78.
46. Mans R, Daran J-MG, Pronk JT. Under pressure: evolutionary engineering of yeast strains for improved performance in fuels and chemicals production. Curr Opin Biotechnol 2018;50:47-56.
47. Mans R, van RossumHM, WijsmanMet al. CRISPR/Cas9: Amolecular Swiss army knife for simultaneous introduction of multiple genetic modifications in Saccharomyces cerevisiae. FEMS Yeast Res 2015;15:fov004.
48. Nijkamp JF, van den Broek M, Datema E et al. De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microb Cell Fact 2012;11:36.
49. Nijland JG, Shin HY, de Jong RM et al. Engineering of an endogenous hexose transporter into a specific d-xylose transporter facilitates glucose-xylose co-consumption in Saccharomyces cerevisiae. Biotechnol Biofuels 2014;7:168.
50. Oud B, Maris AJA, Daran JM et al. Genome-wide analytical approaches for reverse metabolic engineering of industrially relevant phenotypes in yeast. FEMS Yeast Res 2012;12:183-96.
51. Paalme T, Kevvai K, Vilbaste A et al. Uptake and accumulation of B-group vitamers in Saccharomyces cerevisiae in ethanol-stat fed-batch culture. World J Microb Biot 2014;30:2351-9.
52. Renewable Fuels Association.World Fuel Ethanol Production. 2017. http://ethanolrfa.org/resources/industry/statistics /(20 July 2018 date last accessed)
53. Runquist D, Hahn-Hagerdal B, Bettiga M. Increased ethanol productivity in xylose-utilizing Saccharomyces cerevisiae via a randomly mutagenized xylose reductase. Appl Environ Microb 2010;76:7796-802.
54. Runquist D, Hahn-Hgerdal B, Radstrm P. Comparison of heterologous xylose transporters in recombinant Saccharomyces cerevisiae. Biotechnol Biofuels 2010;3:7796-802.
55. Sanchez RG, Karhumaa K, Fonseca C et al. Improved xylose and arabinose utilization by an industrial recombinant Saccharomyces cerevisiae strain using evolutionary engineering. Biotechnol Biofuels 2010;3:13.
56. Sedlak M, Ho NW. Expression of E. coli araBAD operon encoding enzymes for metabolizing l-Arabinose in Saccharomyces cerevisiae. Enzyme Microb Technol 2001;28:16-24.
57. Sedlak M, Ho NW. Characterization of the effectiveness of hexose transporters for transporting xylose during glucose and xylose co-fermentation by a recombinant Saccharomyces yeast. Yeast 2004;21:671-84.
58. Sonderegger M, Sauer U. Evolutionary engineering of Saccharomyces cerevisiae for anaerobic growth on xylose. Appl Environ Microb 2003;69:1990-8.
59. Subtil T, Boles E. Improving l-Arabinose utilization of pentose fermenting Saccharomyces cerevisiae cells by heterologous expression of l-Arabinose transporting sugar transporters. Biotechnol Biofuels 2011;4:1990-8.
60. Subtil T, Boles E. Competition between pentoses and glucose during uptake and catabolism in recombinant Saccharomyces cerevisiae. Biotechnol Biofuels 2012;5:14.
61. Tr ?aff K, Jnsson LJ, Hahn-Hgerdal B. Putative xylose and arabinose reductases in Saccharomyces cerevisiae. Yeast 2002;19:1233-41.
62. van Maris AJ, Abbott DA, Bellissimi E et al. Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Anton Leeuw 2006;90:391-418.
63. Verduyn C, Postma E, Scheffers WA et al. Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. Microbiology 1990;136:395-403.
64. Verduyn C, Postma E, Scheffers WA et al. Effect of benzoic acid on metabolic fluxes in yeasts: A continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 1992;8:501-17.
65. Verhoeven MD, Bracher JM, Nijland JG et al. Mutations in the galactose-Transporter gene GAL2 enable anaerobic growth of glucose-phosphorylation-negative, arabinose-fermenting yeast strains in the presence of glucose. FEMS Yeast Res 2018;18:foy062.
66. Verhoeven MD, Lee M, Kamoen L et al. Mutations in PMR1 stimulate xylose isomerase activity and anaerobic growth on xylose of engineered Saccharomyces cerevisiae by influencing manganese homeostasis. Sci Rep 2017;7:46155.
67. Walfridsson M, Hallborn J, Penttil M et al. Xylose-metabolizing Saccharomyces cerevisiae strains overexpressing the TKL1 and TAL1 genes encoding the pentose phosphate pathway enzymes transketolase and transaldolase. Appl Environ Microb 1995;61:4184-90.
68. Wang C, Li Y, Qiu C et al. Identification of important amino acids in Gal2p for improving the l-Arabinose transport and metabolism in Saccharomyces cerevisiae. Front Microbiol 2017a;8:1391.
69. Wang C, Zhao J, Qiu C et al. Coutilization of d-glucose, d-xylose, and l-Arabinose in Saccharomyces cerevisiae by coexpressing the metabolic pathways and evolutionary engineering. Biomed Res Int 2017b;2017:5318232.
70. Watanabe S, Saleh AA, Pack SP et al. Ethanol production from xylose by recombinant Saccharomyces cerevisiae expressing protein-engineered NADH-preferring xylose reductase from Pichia stipitis. Microbiology 2007;153:3044-54.
71. Wisselink HW, Cipollina C, Oud B et al. Metabolome, transcriptome and metabolic flux analysis of arabinose fermentation by engineered Saccharomyces cerevisiae. Metab Eng 2010;12:537-51.
72. Wisselink HW, Toirkens MJ, Del Rosario Franco Berriel M et al. Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of l-Arabinose. Appl EnvironMicrob 2007;73:4881-91.
73. Wisselink HW, Toirkens MJ, Wu Q et al. Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Appl Environ Microb 2009;75:907-14.
74. Wisselink HW, Van Maris AJA, Pronk JT et al. Polypeptides with permease activity. US Patent 9034608 B2, 2015.
75. Wright J, Bellissimi E, De Hulster E et al. Batch and continuous culture-based selection strategies for acetic acid tolerance in xylose-fermenting Saccharomyces cerevisiae. FEMS Yeast Res 2011;11:299-306.
76. Zhou H, Cheng JS, Wang BL et al. 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;14:611-22.