Metabolic engineering of Ustilago trichophora TZ1 for improved malic acid production

Metabolic Engineering Communications

Volumn 4, Issue , 2017, Pages 12-21

  Zambanini, Thiemo ^a   Hosseinpour Tehrani, Hamed ^a   Geiser, Elena ^a   Sonntag, Christiane K ^a   Buescher, Joerg M ^b,c   Meurer, Guido ^b   Wierckx, Nick ^a   Blank, Lars M ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b BRAIN AG   (Germany)

^c Immunobiology and Epigenetics   (Germany)

Author keywords

Carbon balance; Glycerol; Malate; Metabolic engineering; Overexpression; Ustilago trichophora

Indexed keywords

2 OXOGLUTARIC ACID; CARBON DIOXIDE; CARBOXIN; GLYCEROL; HYGROMYCIN; MALATE DEHYDROGENASE; MALIC ACID; NOURSEOTHRICIN; PHLEOMYCIN; PYRUVATE CARBOXYLASE; PYRUVIC ACID; SUCCINIC ACID;

ARTICLE; BIOMASS PRODUCTION; BIOREACTOR; CARBON BALANCE; CLONING; DNA SEQUENCE; FILAMENTOUS FUNGUS; FLUORESCENCE MICROSCOPY; FUNGAL STRAIN; FUNGUS CULTURE; GENE OVEREXPRESSION; METABOLIC ENGINEERING; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; USTILAGO TRICHOPHORA TZ1;

EID: 85009997358     PISSN: None     EISSN: 22140301     Source Type: Journal    
DOI: 10.1016/j.meteno.2017.01.002     Document Type: Article

References (71)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool. J. Mol. Biol. 215 (1990), 403–410.
2. Battat, E., Peleg, Y., Bercovitz, A., Rokem, J.S., Goldberg, I., Optimization of L-malic acid production by Aspergillus flavus in a stirred fermentor. Biotechnol. Bioeng. 37 (1991), 1108–1116.
3. Bercovitz, A., Peleg, Y., Battat, E., Rokem, J.S., Goldberg, I., Localization of pyruvate carboxylase in organic acid-producing Aspergillus strains. Appl. Environ. Microbiol. 56 (1990), 1594–1597.
4. Bölker, M., Bohnert, H.U., Braun, K.H., Gorl, J., Kahmann, R., Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 248 (1995), 547–552.
5. Brachmann, A., König, J., Julius, C., Feldbrügge, M., A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol. Genet. Genom. 272 (2004), 216–226.
6. Broomfield, P.L., Hargreaves, J.A., A single amino-acid change in the iron-sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis. Curr. Genet. 22 (1992), 117–121.
7. Brown, S.H., Bashkirova, L., Berka, R., Chandler, T., Doty, T., McCall, K., McCulloch, M., McFarland, S., Thompson, S., Yaver, D., Berry, A., Metabolic engineering of Aspergillus oryzae NRRL 3488 for increased production of L-malic acid. Appl. Microbiol. Biotechnol. 97 (2013), 8903–8912.
8. Chen, X., Wu, J., Song, W., Zhang, L., Wang, H., Liu, L., Fumaric acid production by Torulopsis glabrata: engineering the urea cycle and the purine nucleotide cycle. Biotechnol. Bioeng. 112 (2015), 156–167.
9. Chen, X., Xu, G., Xu, N., Zou, W., Zhu, P., Liu, L., Chen, J., Metabolic engineering of Torulopsis glabrata for malate production. Metab. Eng. 19 (2013), 10–16.
10. Choi, S., Song, C.W., Shin, J.H., Lee, S.Y., Biorefineries for the production of top building block chemicals and their derivatives. Metab. Eng. 28 (2015), 223–239.
11. Geiser, E., Przybilla, S.K., Engel, M., Kleineberg, W., Buttner, L., Sarikaya, E., Hartog, T.D., Klankermayer, J., Leitner, W., Bolker, M., Blank, L.M., Wierckx, N., Genetic and biochemical insights into the itaconate pathway of Ustilago maydis enable enhanced production. Metab. Eng., 2016, 10.1016/j.ymben.2016.10.006.
12. Geiser, E., Wiebach, V., Wierckx, N., Blank, L.M., Prospecting the biodiversity of the fungal family Ustilaginaceae for the production of value-added chemicals. BMC Fungal Biol. Biotechnol., 1, 2014, 2.
13. Geiser, E., Wierckx, N., Zimmermann, M., Blank, L.M., Identification of an endo-1,4-beta-xylanase of Ustilago maydis. BMC Biotechnol., 13, 2013, 59.
14. Gold, S.E., Bakkeren, G., Davies, J.E., Kronstad, J.W., Three selectable markers for transformation of Ustilago maydis. Gene 142 (1994), 225–230.
15. Goldberg, I., Rokem, J.S., Pines, O., Organic acids: old metabolites, new themes. J. Chem. Technol. Biotechnol. 81 (2006), 1601–1611.
16. Guettler, M.V., Rumler, D., Jain, M.K., Actinobacillus succinogenes sp. nov., a novel succinic-acid-producing strain from the bovine rumen. Int. J. Syst. Bacteriol. 49:Pt 1 (1999), 207–216.
17. Guevarra, E.D., Tabuchi, T., Accumulation of itaconic, 2-hydroxyparaconic, itatartaric, and malic acids by strains of the genus Ustilago. Agric. Biol. Chem. 54 (1990), 2353–2358.
18. Guevarra, E.D., Tabuchi, T., Production of 2-hydroxyparaconic and itatartaric acids by Ustilago cynodontis and simple recovery process of the acids. Agric. Biol. Chem. 54 (1990), 2359–2365.
19. Gyamerah, M.H., Oxygen requirement and energy relations of itaconic acid fermentation by Aspergillus terreus NRRL 1960. Appl. Microbiol. Biotechnol. 44 (1995), 20–26.
20. Hewald, S., Linne, U., Scherer, M., Marahiel, M.A., Kämper, J., Bölker, M., Identification of a gene cluster for biosynthesis of mannosylerythritol lipids in the basidiomycetous fungus Ustilago maydis. Appl. Environ. Microbiol. 72 (2006), 5469–5477.
21. Hoffman, C.S., Winston, F., A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57 (1987), 267–272.
22. Kaneuchi, C., Seki, M., Komagata, K., Production of succinic acid from citric acid and related acids by lactobacillus strains. Appl. Environ. Microbiol. 54 (1988), 3053–3056.
23. Katsumata, R., Ozaki, A., Oka, T., Furuya, A., Protoplast transformation of glutamate-producing bacteria with plasmid DNA. J. Bacteriol. 159 (1984), 306–311.
24. Kautola, H., Vahvaselkä, M., Linko, Y.Y., Linko, P., Itaconic acid production by immobilized Aspergillus terreus from xylose and glucose. Biotechnol. Lett. 7 (1985), 167–172.
25. Kautola, H., Vassilev, N., Linko, Y.Y., Continuous itaconic acid production by immobilized biocatalysts. J. Biotechnol. 13 (1990), 315–323.
26. Kellner, R., Der Einfluss sexueller Reproduktion und Virulenz auf die Evolution und Speziation der biotrophen Brandpilzfamilie Ustilaginaceae. 2011, Ruhr-Universität Bochum, Germany.
27. Keon, J.P., White, G.A., Hargreaves, J.A., Isolation, characterization and sequence of a gene conferring resistance to the systemic fungicide carboxin from the maize smut pathogen, Ustilago maydis. Curr. Genet. 19 (1991), 475–481.
28. Khrunyk, Y., Munch, K., Schipper, K., Lupas, A.N., Kahmann, R., The use of FLP-mediated recombination for the functional analysis of an effector gene family in the biotrophic smut fungus Ustilago maydis. New Phytol. 187 (2010), 957–968.
29. Klement, T., Büchs, J., Itaconic acid - a biotechnological process in change. Bioresour. Technol. 135 (2013), 422–431.
30. Klement, T., Milker, S., Jäger, G., Grande, P.M., de Maria, P.D., Büchs, J., Biomass pretreatment affects Ustilago maydis in producing itaconic acid. Microb. Cell. Fact., 11, 2012, 43.
31. Knuf, C., Nookaew, I., Brown, S.H., McCulloch, M., Berry, A., Nielsen, J., Investigation of malic acid production in Aspergillus oryzae under nitrogen starvation conditions. Appl. Environ. Microbiol. 79 (2013), 6050–6058.
32. König, J., Die Identifikation von Ziel-Transkripten des RNA bindenden Proteins Rrm4 aus Ustilago maydis. 2008, Philipps-Universität Marburg, Germany.
33. Liu, X., Lv, J., Xu, J., Zhang, T., Deng, Y., He, J., Citric acid production in Yarrowia lipolytica SWJ-1b yeast when grown on waste cooking oil. Appl. Biochem. Biotechnol. 175 (2015), 2347–2356.
34. Maassen, N., Gewinnung von Gärungsmutanten der Hefe Pichia stipitis durch zufällige Integrationsmutagenese. 2007, RWTH Aachen University, Germany.
35. Maassen, N., Panakova, M., Wierckx, N., Geiser, E., Zimmermann, M., Bölker, M., Klinner, U., Blank, L.M., Influence of carbon and nitrogen concentration on itaconic acid production by the smut fungus Ustilago maydis. Eng. Life Sci. 14 (2013), 129–134.
36. Mahlert, M., Leveleki, L., Hlubek, A., Sandrock, B., Bölker, M., Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimorphic fungus Ustilago maydis. Mol. Microbiol. 59 (2006), 567–578.
37. Morita, T., Fukuoka, T., Imura, T., Kitamoto, D., Production of glycolipid biosurfactants by basidiomycetous yeasts. Biotechnol. Appl. Biochem. 53 (2009), 39–49.
38. Okabe, M., Lies, D., Kanamasa, S., Park, E.Y., Biotechnological production of itaconic acid and its biosynthesis in Aspergillus terreus. Appl. Microbiol. Biotechnol. 84 (2009), 597–606.
39. Osmani, S.A., Scrutton, M.C., The sub-cellular localisation of pyruvate carboxylase and of some other enzymes in Aspergillus nidulans. Eur. J. Biochem. 133 (1983), 551–560.
40. Papanikolaou, S., Muniglia, L., Chevalot, I., Aggelis, G., Marc, I., Accumulation of a cocoa-butter-like lipid by Yarrowia lipolytica cultivated on agro-industrial residues. Curr. Microbiol. 46 (2003), 124–130.
41. Peleg, Y., Stieglitz, B., Goldberg, I., Malic acid accumulation by Aspergillus flavus. Appl. Microbiol. Biotechnol 28 (1988), 69–75.
42. Przybilla, S., Genetische und biochemische Charakterisierung der Itaconsäure-Biosynthese in Ustilago maydis. 2014, Phillips University Marburg, Germany.
43. Rhodes, R.A., Lagoda, A.A., Misenheimer, T.J., Smith, M.L., Anderson, R.F., Jackson, R.W., Production of fumaric acid in 20-liter fermentors. Appl Microbiol. 10 (1962), 9–15.
44. Rymowicz, W., Rywinska, A., Marcinkiewicz, M., High-yield production of erythritol from raw glycerol in fed-batch cultures of Yarrowia lipolytica. Biotechnol. Lett. 31 (2009), 377–380.
45. Saenge, C., Cheirsilp, B., Suksaroge, T.T., Bourtoom, T., Potential use of oleaginous red yeast Rhodotorula glutinis for the bioconversion of crude glycerol from biodiesel plant to lipids and carotenoids. Process Biochem. 46 (2011), 210–218.
46. Sambrook, J., Russell, D.W., Molecular Cloning: A Laboratory Manual. 2001, Cold Spring Harbor Laboratory Press, New York.
47. Sarkari, P., Reindl, M., Stock, J., Muller, O., Kahmann, R., Feldbrugge, M., Schipper, K., Improved expression of single-chain antibodies in Ustilago maydis. J. Biotechnol. 191 (2014), 165–175.
48. Scholten, E., Renz, T., Thomas, J., Continuous cultivation approach for fermentative succinic acid production from crude glycerol by Basfia succiniciproducens DD1. Biotechnol. Lett. 31 (2009), 1947–1951.
49. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schafer, W., Martin, T., Herskowitz, I., Kahmann, R., The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60 (1990), 295–306.
50. Schuster, M., Schweizer, G., Reissmann, S., Kahmann, R., Genome editing in Ustilago maydis using the CRISPR-Cas system. Fungal Genet. Biol. 89 (2016), 3–9.
51. Shen, H.B., Chou, K.C., Signal-3L: a 3-layer approach for predicting signal peptides. Biochem. Biophys. Res. Commun. 363 (2007), 297–303.
52. Shockman, G.D., Lampen, J.O., Inhibition by antibiotics of the growth of bacterial and yeast protoplasts. J. Bacteriol. 84 (1962), 508–512.
53. Song, H., Lee, S.Y., Production of succinic acid by bacterial fermentation. Enzym. Microb. Technol. 39 (2006), 352–361.
54. Spellig, T., Bottin, A., Kahmann, R., Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252 (1996), 503–509.
55. Steiger, M.G., Blumhoff, M.L., Mattanovich, D., Sauer, M., Biochemistry of microbial itaconic acid production. Front Microbiol., 4, 2013, 23.
56. Takata, I., Yamamoto, K., Tosa, T., Chibata, I., Immobilization of Brevibacterium flavum with carrageenan and its application for continuous production of L-malic acid. Enzym. Microb. Technol. 2 (1980), 30–36.
57. Teichmann, B., Linne, U., Hewald, S., Marahiel, M.A., Bölker, M., A biosynthetic gene cluster for a secreted cellobiose lipid with antifungal activity from Ustilago maydis. Mol. Microbiol. 66 (2007), 525–533.
58. Terfrüchte, M., Joehnk, B., Fajardo-Somera, R., Braus, G.H., Riquelme, M., Schipper, K., Feldbrügge, M., Establishing a versatile Golden Gate cloning system for genetic engineering in fungi. Fungal Genet. Biol. 62 (2014), 1–10.
59. Tsukuda, T., Carleton, S., Fotheringham, S., Holloman, W.K., Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol. Cell. Biol. 8 (1988), 3703–3709.
60. Weinzierl, G., Isolierung und Charakterisierung von Komponenten der b-vermittelten Regulationskaskade in Ustilago maydis. 2001, Philipps-University Marburg, Germany.
61. West, T.P., Malic acid production from thin stillage by Aspergillus species. Biotechnol. Lett. 33 (2011), 2463–2467.
62. West, T.P., Crude glycerol: a feedstock for organic acid production by microbial bioconversion. J. Microb. Biochem. Technol., 4, 2012 (ii-ii).
63. West, T.P., Citric acid production by Candida species grown on a soy-based crude glycerol. Prep. Biochem. Biotechnol. 43 (2013), 601–611.
64. Willke, T., Vorlop, K.D., Biotechnological production of itaconic acid. Appl. Microbiol. Biotechnol. 56 (2001), 289–295.
65. Xu, D.B., Madrid, C.P., Rohr, M., Kubicek, C.P., The influence of type and concentration of the carbon source on production of citric acid by Aspergillus niger. Appl. Microbiol. Biotechnol. 30 (1989), 553–558.
66. Yang, F., Hanna, M.A., Sun, R., Value-added uses for crude glycerol–a byproduct of biodiesel production. Biotechnol. Biofuels, 5, 2012, 13.
67. Yuzbashev, T.V., Yuzbasheva, E.Y., Laptev, I.A., Sobolevskaya, T.I., Vybornaya, T.V., Larina, A.S., Gvilava, I.T., Antonova, S.V., Sineoky, S.P., Is it possible to produce succinic acid at a low pH?. Bioeng. Bugs 2 (2011), 115–119.
68. Zambanini, T., Buescher, J.M., Meurer, G., Wierckx, N., Blank, L.M., Draft genome Sequence of Ustilago trichophora RK089, a promising malic acid producer. Genome Announc., 2016, 4.
69. Zambanini, T., Kleineberg, W., Sarikaya, E., Buescher, J.M., Meurer, G., Wierckx, N., Blank, L.M., Enhanced malic acid production from glycerol with high-cell-density Ustilago trichophora TZ1 cultivations. Biotechnol. Biofuels, 9, 2016, 135.
70. Zambanini, T., Sarikaya, E., Kleineberg, W., Buescher, J.M., Meurer, G., Wierckx, N., Blank, L.M., Efficient malic acid production from glycerol with Ustilago trichophora TZ1. Biotechnol. Biofuels, 9, 2016, 67.
71. Zelle, R.M., de Hulster, E., van Winden, W.A., de Waard, P., Dijkema, C., Winkler, A.A., Geertman, J.M., van Dijken, J.P., Pronk, J.T., van Maris, A.J., Malic acid production by Saccharomyces cerevisiae: engineering of pyruvate carboxylation, oxaloacetate reduction, and malate export. Appl. Environ. Microbiol. 74 (2008), 2766–2777.