Toward pectin fermentation by Saccharomyces cerevisiae: Expression of the first two steps of a bacterial pathway for D-galacturonate metabolism

Journal of Biotechnology

Volumn 162, Issue 2-3, 2012, Pages 303-310

  Huisjes, Eline H ^a   Luttik, Marijke A H ^a   Almering, Marinka J H ^a   Bisschops, Markus M M ^a   Dang, Dieu H N ^a   Kleerebezem, Michiel ^b   Siezen, Roland ^c,d,e   van Maris, Antonius J A ^a   Pronk, Jack T ^a  

^a KLUYVER CENTRE FOR GENOMICS OF INDUSTRIAL FERMENTATION   (Netherlands)

^b NIZO FOOD RESEARCH   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^e NETHERLANDS BIOINFORMATICS CENTRE   (Netherlands)

Author keywords

D Galacturonate; D Galacturonate isomerase; D Tagaturonate reductase; Ethanol; Metabolic engineering; Pectin; Saccharomyces cerevisiae

Indexed keywords

BIOETHANOL; ENZYME ACTIVITY; ETHANOL; METABOLIC ENGINEERING; METABOLISM; PHYSIOLOGY; YEAST;

ANAEROBIC GROWTH; BACTERIAL PATHWAY; BIO-ETHANOL PRODUCTION; FUNCTIONAL EXPRESSION; ISOMERASES; LACTOCOCCUS LACTIS; PECTIN; REDUCTASE GENES;

GENE EXPRESSION;

BIOETHANOL; GALACTURONIC ACID; PECTIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; ALCOHOL; BIOFUEL; HEXURONIC ACID; ISOMERASE; OXIDOREDUCTASE; TAGATURONATE REDUCTASE;

ANAEROBIC GROWTH; ARTICLE; BACTERIAL GENE; BIOFUEL PRODUCTION; CARBOHYDRATE METABOLISM; CARBON SOURCE; CODON; CONTROLLED STUDY; ENZYME ACTIVITY; FERMENTATION; GENE SEQUENCE; HETEROLOGOUS EXPRESSION; IN VIVO STUDY; KDGA GENE; KDGK GENE; LACTOCOCCUS LACTIS; METABOLIC ENGINEERING; NONHUMAN; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SACCHAROMYCES CEREVISIAE; UXAA GENE; UXAB GENE; UXAC GENE; BACTERIUM; BIOREACTOR; ENZYMOLOGY; GENETICS; METABOLISM; METHODOLOGY; MICROBIOLOGY; PHYLOGENY;

BACTERIA; BIOFUELS; BIOREACTORS; CARBOHYDRATE DEHYDROGENASES; CODON; ETHANOL; FERMENTATION; HEXURONIC ACIDS; ISOMERASES; LACTOCOCCUS LACTIS; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; PECTINS; PHYLOGENY; SACCHAROMYCES CEREVISIAE;

EID: 84868488951     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2012.10.003     Document Type: Article

References (66)

1. Amore, R., Wilhelm, M., Hollenberg, C.P., The fermentation of xylose – an analysis of the expression of Bacillus and Actinoplanes xylose isomerase genes in yeast. Applied Microbiology and Biotechnology 30 (1989), 351–357.
2. Ashwell, G., Wahba, A.J., Hickman, J., Uronic acid metabolism in bacteria. 1. Purification and properties of uronic acid isomerase in Escherichia coli. Journal of Biological Chemistry 235 (1960), 1559–1565.
3. Attfield, P.V., Bell, P.J.L., Use of population genetics to derive nonrecombinant Saccharomyces cerevisiae strains that grow using xylose as a sole carbon source. FEMS Yeast Research 6 (2006), 862–868.
4. Bakker, B.M., Overkamp, K.M., Van Maris, A.J.A., Kötter, P., Luttik, M.A.H., Van Dijken, J.P., Pronk, J.T., Stoichiometry and compartmentation of NADH metabolism in Saccharomyces cerevisiae. FEMS Microbiology Review 25 (2001), 15–37.
5. Barnett, J.A., Payne, R.W., Yarrow, D., A Guide to Identifying and Classifying Yeasts. 1990, Cambridge University Press, Cambridge, UK.
6. Becker, J., Boles, E., A modified Saccharomyces cerevisiae strain that consumes L-arabinose and produces ethanol. Applied and Environment Microbiology 69 (2003), 4144–4150.
7. Björkqvist, S., Ansell, R., Adler, L., Lidén, G., Physiological response to anaerobicity of glycerol-3-phosphate dehydrogenase mutants of Saccharomyces cerevisiae. Applied and Environment Microbiology 63 (1997), 128–132.
8. Brat, D., Boles, E., Wiedemann, B., Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Applied and Environment Microbiology 75 (2009), 2304–2311.
9. Burke, D., Dawson, D., Stearns, T., Laboratory, C.S.H., Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual. 2000, Cold Spring Harbor Laboratory Press, Cold Spring harbor, NY, USA.
10. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H., Hieter, P., Multifunctional yeast high-copy-number shuttle vectors. Gene 110 (1992), 119–122.
11. Cynkin, M.A., Ashwell, G., Uronic acid metabolism in bacteria. 4. Purification and properties of 2-keto-3-deoxy-D-gluconokinase in Escherichia coli. Journal of Biological Chemistry 235 (1960), 1576–1579.
12. Doran, J.B., Cripe, J., Sutton, M., Foster, B., Fermentations of pectin-rich biomass with recombinant bacteria to produce fuel ethanol. Applied Biochemistry and Biotechnology 84:6 (2000), 141–152.
13. Edwards, M., Doran-Peterson, J., Pectin-rich biomass as feedstock for fuel ethanol production. Applied Microbiology and Biotechnology 95 (2012), 565–575.
14. Ehrlich, F., Guttmann, R., Zur Kenntnis der d-Galakturonsäure, II. Mitteil.: Ihre Umlagerung in 5-Keto-l-galaktonsäure. Berichte der Deutschen Chemischen Gesellschaft 67 (1934), 573–589.
15. Entian, K.D., Kötter, P., Yeast genetic strain and plasmid collections. Stansfield, I., Stark, M.J.R., (eds.) Methods in Microbiology, 2007, Academic Press, San Diego, CA, USA, 629–666.
16. Gárdonyi, M., Hahn-Hägerdal, B., The Streptomyces rubiginosus xylose isomerase is misfolded when expressed in Saccharomyces cerevisiae. Enzyme and Microbial Technology 32 (2003), 252–259.
17. Grohmann, K., Bothast, R.J., Pectin-rich residues generated by processing of citrus fruits, apples, and sugar beets – enzymatic hydrolysis and biological conversion to value-added products. ACS Symposium Series 566 (1994), 372–390.
18. Guadalupe Medina, V.G., Almering, M.J.H., Van Maris, A.J.A., Pronk, J.T., Elimination of glycerol production in anaerobic cultures of a Saccharomyces cerevisiae strain engineered to use acetic acid as an electron acceptor. Applied and Environment Microbiology 76 (2010), 190–195.
19. Güldener, U., Heck, S., Fiedler, T., Beinhauer, J., Hegemann, J.H., A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Research 24 (1996), 2519–2524.
20. Hahn-Hägerdal, B., Karhumaa, K., Jeppsson, M., Gorwa-Grauslund, M., Metabolic engineering for pentose utilization in Saccharomyces cerevisiae. Olsson, L., (eds.) Biofuels, 2007, Springer, Berlin/Heidelberg, 147–177.
21. Hensing, M.C.M., Bangma, K.A., Raamsdonk, L.M., Hulster, E., Dijken, J.P., Pronk, J.T., Effects of cultivation conditions on the production of heterologous α-galactosidase by Kluyveromyces lactis. Applied Microbiology and Biotechnology 43 (1995), 58–64.
22. Hickman, J., Ashwell, G., Uronic acid metabolism in bacteria. 2. Purification and properties of D-altronic acid and D-mannonic acid dehydrogenases in Escherichia coli. Journal of Biological Chemistry 235 (1960), 1566–1570.
23. Hilditch, S., Berghall, S., Kalkkinen, N., Penttila, M., Richard, P., The missing link in the fungal D-galacturonate pathway; identification of the L-threo-3-deoxy-hexulosonate aldolase. Journal of Biological Chemistry 282 (2007), 26195–26201.
24. Hong, K.-K., Nielsen, J., Metabolic engineering of Saccharomyces cerevisiae: a key cell factory platform for future biorefineries. Cellular and Molecular Life Sciences, 2012, 1–20.
25. Huisjes, E.H., De Hulster, E., Van Dam, J.C., Pronk, J.T., Van Maris, A.J.A., Galacturonic acid inhibits growth of Saccharomyces cerevisiae on galactose, xylose and arabinose. Applied and Environment Microbiology 78 (2012), 5052–5059.
26. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E., Knop, M., A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21 (2004), 947–962.
27. Kovachevich, R., Wood, W.A., Carbohydrate metabolism by Pseudomonas fluorescens. IV. Purification and properties of 2-keto-3-deoxy-6-phosphogluconate aldolase. Journal of Biological Chemistry 213 (1955), 757–767.
28. Kuorelahti, S., Jouhten, P., Maaheimo, H., Penttila, M., Richard, P., l-Galactonate dehydratase is part of the fungal path for D-galacturonic acid catabolism. Molecular Microbiology 61 (2006), 1060–1068.
29. Kuorelahti, S., Kalkkinen, N., Penttila, M., Londesborough, J., Richard, P., Identification in the mold Hypocrea jecorina of the first fungal D-galacturonic acid reductase. Biochemistry 44 (2005), 11234–11240.
30. Liepins, J., Kuorelahti, S., Penttila, M., Richard, P., Enzymes for the NADPH-dependent reduction of dihydroxyacetone and d-glyceraldehyde and l-glyceraldehyde in the mould Hypocrea jecorina. FEBS Journal 273 (2006), 4229–4235.
31. Linster, C.L., Van Schaftingen, E., A spectrophotometric assay of d-glucuronate based on Escherichia coli uronate isomerase and mannonate dehydrogenase. Protein Expression and Purification 37 (2004), 352–360.
32. Martens-Uzunova, E.S., Schaap, P.J., An evolutionary conserved D-galacturonic acid metabolic pathway operates across filamentous fungi capable of pectin degradation. Fungal Genetics and Biology 45 (2008), 1449–1457.
33. Mata-Gilsinger, M., Ritzenthaler, P., Physical mapping of the exuT and uxaC operators by use of exu plasmids and generation of deletion mutants in vitro. Journal of Bacteriology 155 (1983), 973–982.
34. Micard, V., Renard, C.M.G.C., Thibault, J.F., Enzymatic saccharification of sugar-beet pulp. Enzyme and Microbial Technology 19 (1996), 162–170.
35. Moes, C.J., Pretorius, I.S., Zyl, W.H., Cloning and expression of the Clostridium thermosulfurogenes D-xylose isomerase gene (xyLA) in Saccharomyces cerevisiae. Biotechnology Letters 18 (1996), 269–274.
36. Mumberg, D., Müller, R., Funk, M., Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156 (1995), 119–122.
37. Naesby, M., Nielsen, S., Nielsen, C., Green, T., Tange, T., Simon, E., Knechtle, P., Hansson, A., Schwab, M., Titiz, O., Folly, C., Archila, R., Maver, M., Van Sint Fiet, S., Boussemghoune, T., Janes, M., Kumar, A., Sonkar, S., Mitra, P., Benjamin, V., Korrapati, N., Suman, I., Hansen, E., Thybo, T., Goldsmith, N., Sorensen, A., Yeast artificial chromosomes employed for random assembly of biosynthetic pathways and production of diverse compounds in Saccharomyces cerevisiae. Microbial Cell Factories, 8, 2009, 45.
38. Nevoigt, E., Progress in metabolic engineering of Saccharomyces cerevisiae. Microbiology and Molecular Biology Reviews 72 (2008), 379–412.
39. Nijkamp, J., Van den Broek, M., Datema, E., De Kok, S., Bosman, L., Luttik, M., Daran-Lapujade, P., Vongsangnak, W., Nielsen, J., Heijne, W., Klaassen, P., Paddon, C., Platt, D., Kotter, P., Van Ham, R., Reinders, M., Pronk, J., De Ridder, D., Daran, J.-M., De novo sequencing, assembly and analysis of the genome of the laboratory strain Saccharomyces cerevisiae CEN.PK113-7D, a model for modern industrial biotechnology. Microbial Cell Factories, 11, 2012, 36.
40. Pfaffl, M.W., A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, 2001, e45.
41. Piper, M.D.W., Daran-Lapujade, P., Bro, C., Regenberg, B., Knudsen, S., Nielsen, J., Pronk, J.T., Reproducibility of oligonucleotide microarray transcriptome analyses. Journal of Biological Chemistry 277 (2002), 37001–37008.
42. Postma, E., Verduyn, C., Scheffers, W.A., Van Dijken, J.P., Enzymic analysis of the Crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Applied and Environment Microbiology 55 (1989), 468–477.
43. Pronk, J.T., Auxotrophic yeast strains in fundamental and applied research. Applied and Environment Microbiology 68 (2002), 2095–2100.
44. Saitou, N., Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4 (1987), 406–425.
45. Sarthy, A.V., McConaughy, B.L., Lobo, Z., Sundstrom, J.A., Furlong, C.E., Hall, B.D., Expression of the Escherichia coli xylose isomerase gene in Saccharomyces cerevisiae. Applied and Environment Microbiology 53 (1987), 1996–2000.
46. Schmitt, M.E., Brown, T.A., Trumpower, B.L., A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Research 18 (1990), 3091–3092.
47. Sedlak, M., Ho, N.W.Y., Expression of E. coli araBAD operon encoding enzymes for metabolizing L-arabinose in Saccharomyces cerevisiae. Enzyme and Microbial Technology 28 (2001), 16–24.
48. Sikorski, R.S., Hieter, P., A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122 (1989), 19–27.
49. Smiley, J.D., Ashwell, G., Uronic acid metabolism in bacteria. 3. Purification and properties of D-altronic acid and D-mannonic acid dehydrases in Escherichia coli. Journal of Biological Chemistry 235 (1960), 1571–1575.
50. Souffriau, B., den Abt, T., Thevelein, J.M., Evidence for rapid uptake of D-galacturonic acid in the yeast Saccharomyces cerevisiae by a channel-type transport system. FEBS Letters 586 (2012), 2494–2499.
51. Tamura, K., Nei, M., Kumar, S., Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America 101 (2004), 11030–11035.
52. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28 (2011), 2731–2739.
53. Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22 (1994), 4673–4680.
54. Van Dijken, J.P., Scheffers, W.A., Redox balances in the metabolism of sugars by yeasts. FEMS Microbiology Letters 32 (1986), 199–224.
55. Van Hoek, P., Van Dijken, J.P., Pronk, J.T., Regulation of fermentative capacity and levels of glycolytic enzymes in chemostat cultures of Saccharomyces cerevisiae. Enzyme and Microbial Technology 26 (2000), 724–736.
56. Van Hylckama Vlieg, J.E.T., Rademaker, J.L.W., Bachmann, H., Molenaar, D., Kelly, W.J., Siezen, R.J., Natural diversity and adaptive responses of Lactococcus lactis. Current Opinion in Biotechnology 17 (2006), 183–190.
57. Van Maris, A., Winkler, A., Kuyper, M., De Laat, W., Van Dijken, J., Pronk, J., Development of efficient xylose fermentation in Saccharomyces cerevisiae: xylose isomerase as a key component. Olsson, L., (eds.) Adv. Biochem. Eng./Biotechnol., 2007, Springer, Berlin/Heidelberg, 179–204.
58. Van Maris, A.J.A., Abbott, D.A., Bellissimi, E., Van den Brink, J., Kuyper, M., Luttik, M.A.H., Wisselink, H.W., Scheffers, W.A., Van Dijken, J.P., Pronk, J.T., Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: current status. Antonie Van Leeuwenhoek 90 (2006), 391–418.
59. Verduyn, C., Postma, E., Scheffers, W.A., Van Dijken, J.P., Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. Journal of General Microbiology 136 (1990), 395–403.
60. 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 8 (1992), 501–517.
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. Applied and Environment Microbiology 62 (1996), 4648–4651.
62. Weber, C., Farwick, A., Benisch, F., Brat, D., Dietz, H., Subtil, T., Boles, E., Trends and challenges in the microbial production of lignocellulosic bioalcohol fuels. Applied Microbiology and Biotechnology 87 (2010), 1303–1315.
63. Wiedemann, B., Boles, E., Codon-optimized bacterial genes improve L-arabinose fermentation in recombinant Saccharomyces cerevisiae. Applied and Environment Microbiology 74 (2008), 2043–2050.
64. Wisselink, H.W., Cipollina, C., Oud, B., Crimi, B., Heijnen, J.J., Pronk, J.T., Van Maris, A.J.A., Metabolome, transcriptome and metabolic flux analysis of arabinose fermentation by engineered Saccharomyces cerevisiae. Metabolic Engineering 12 (2010), 537–551.
65. Wisselink, H.W., Toirkens, M.J., Del Rosario Franco Berriel, M., Winkler, A.A., van Dijken, J.P., Pronk, J.T., Van Maris, A.J.A., Engineering of Saccharomyces cerevisiae for efficient anaerobic alcoholic fermentation of L-arabinose. Applied and Environment Microbiology 73 (2007), 4881–4891.
66. Wisselink, H.W., Toirkens, M.J., Wu, Q., Pronk, J.T., Van Maris, A.J.A., Novel evolutionary engineering approach for accelerated utilization of glucose, xylose, and arabinose mixtures by engineered Saccharomyces cerevisiae strains. Applied and Environment Microbiology 75 (2009), 907–914.