Physiological characterization of the high malic acid-producing Aspergillus oryzae strain 2103a-68

Applied Microbiology and Biotechnology

Volumn 98, Issue 8, 2014, Pages 3517-3527

  Knuf, Christoph ^a   Nookaew, Intawat ^a   Remmers, Ilse ^a   Khoomrung, Sakda ^a   Brown, Stephen ^b   Berry, Alan ^b   Nielsen, Jens ^a,c  

^a CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^b Novozymes Biotech Inc   (United States)

^c Chalmers University of Technology   (Denmark)

Author keywords

Aspergillus oryzae; Dicarboxylic acid; Malate; Metabolic engineering; Xylose

Indexed keywords

ASPERGILLUS; CHEMICAL INDUSTRY; CULTIVATION; ENZYME ACTIVITY; METABOLIC ENGINEERING; XYLOSE;

ASPERGILLUS ORYZAE; DICARBOXYLIC ACID; MALATE; MALATE DEHYDROGENASE; MICROBIAL PRODUCTION; PYRUVATE CARBOXYLASE; SPECIFIC PRODUCTION RATE; TRICARBOXYLIC ACIDS;

STRAIN RATE;

CARBON; CARBON 13; GLUCOSE; HEXOSE; MALATE DEHYDROGENASE; MALIC ACID; PENTOSE; PYRUVATE CARBOXYLASE; TRICARBOXYLIC ACID; XYLOSE; MALIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; ASPERGILLUS ORYZAE; BIOMASS PRODUCTION; CARBON SOURCE; CITRIC ACID CYCLE; CONTROLLED STUDY; CYTOSOL; DRY WEIGHT; ENZYME ACTIVITY; ENZYME METABOLISM; FUNGAL GENE; FUNGAL STRAIN; GENE OVEREXPRESSION; INTRACELLULAR SIGNALING; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; NONHUMAN; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOTOPE LABELING; METABOLISM;

ASPERGILLUS ORYZAE; CARBON ISOTOPES; GENE EXPRESSION PROFILING; ISOTOPE LABELING; MALATES; METABOLIC ENGINEERING; METABOLIC FLUX ANALYSIS; METABOLIC NETWORKS AND PATHWAYS;

EID: 84898923712     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-5465-x     Document Type: Article

References (36)

1. Abe S, Furuya A, Saito T, Takayama K (1962) Method of producing l-malic acid by fermentation. US Patent 3,063,910
2. Battat E, Peleg Y, Bercovitz A, Rokem JS, Goldberg I (1991) Optimization of l-malic acid production by Aspergillus flavus in a stirred fermentor. Biotechnol Bioeng 37(11):1108-1116. doi: 10.1002/bit.260371117
3. Becker J, Reinefeld J, Stellmacher R, Schäfer R, Lange A, Meyer H, Lalk M, Zelder O, von Abendroth G, Schröder H, Haefner S, Wittmann C (2013) Systems-wide analysis and engineering of metabolic pathway fluxes in bio-succinate producing Basfia succiniciproducens. Biotechnol Bioeng 110(11):3013-3023. doi: 10.1002/bit.24963
4. Bercovitz A, Peleg Y, Battat E, Rokem JS, Goldberg I (1990) Localization of pyruvate carboxylase in organic acid-producing Aspergillus strains. Appl Environ Microbiol 56(6):1594-1597
5. Brown SH, Bashkirova L, Berka R, Chandler T, Doty T, McCall K, McCulloch M, McFarland S, Thompson S, Yaver D, Berry A (2013) Metabolic engineering of Aspergillus oryzae NRRL 3488 for increased production of l-malic acid. Appl Microbiol Biotechnol 97(20):8903-8912. doi: 10.1007/s00253-013-5132-2
6. Buschke N, Schröder H, Wittmann C (2011) Metabolic engineering of Corynebacterium glutamicum for production of 1,5-diaminopentane from hemicellulose. Biotechnol J 6(3):306-317. doi: 10.1002/biot.201000304
7. Camarasa C, Bidard F, Bony M, Barre P, Dequin S (2001) Characterization of Schizosaccharomyces pombe malate permease by expression in Saccharomyces cerevisiae. Appl Environ Microbiol 67(9):4144-4151. doi: 10.1128/aem.67.9.4144- 4151.2001
8. Cvijovic M, Olivares-Hernández R, Agren R, Dahr N, Vongsangnak W, Nookaew I, Patil KR, Nielsen J (2010) BioMet Toolbox: genome-wide analysis of metabolism. Nucleic Acids Res 38(Suppl 2):W144-W149. doi: 10.1093/nar/gkq404
9. de Jongh WA, Nielsen J (2008) Enhanced citrate production through gene insertion in Aspergillus niger. Metab Eng 10(2):87-96. doi: 10.1016/j.ymben. 2007.11.002
10. Goldberg I, Rokem JS, Pines O (2006) Organic acids: old metabolites, new themes. J Chem Technol Biotechnol 81(10):1601-1611. doi: 10.1002/jctb.1590
11. Gombert AK, Moreira dos Santos M, Christensen B, Nielsen J (2001) Network identification and flux quantification in the central metabolism of Saccharomyces cerevisiae under different conditions of glucose repression. J Bacteriol 183(4):1441-1451. doi: 10.1128/jb.183.4.1441-1451.2001
12. Grotkjaer T, Christakopoulos P, Nielsen J, Olsson L (2005) Comparative metabolic network analysis of two xylose fermenting recombinant Saccharomyces cerevisiae strains. Metab Eng 7(5-6):437-444. doi: 10.1016/j.ymben.2005.07.003
13. Karaffa L, Kubicek C (2003) Aspergillus niger citric acid accumulation: do we understand this well working black box? Appl Microbiol Biotechnol 61(3):189-196. doi: 10.1007/s00253-002-1201-7
14. Kawaguchi H, Vertès AA, Okino S, Inui M, Yukawa H (2006) Engineering of a xylose metabolic pathway in Corynebacterium glutamicum. Appl Environ Microbiol 72(5):3418-3428. doi: 10.1128/aem.72.5.3418-3428.2006
15. Knuf C, Nookaew I, Brown SH, McCulloch M, Berry A, Nielsen J (2013) Investigation of malic acid production in Aspergillus oryzae under nitrogen starvation conditions. Appl Environ Microbiol 79(19):6050-6058. doi: 10.1128/aem.01445-13
16. Liu R, Liang L, Chen K, Ma J, Jiang M, Wei P, Ouyang P (2012) Fermentation of xylose to succinate by enhancement of ATP supply in metabolically engineered Escherichia coli. Appl Microbiol Biotechnol 94(4):959-968. doi: 10.1007/s00253-012-3896-4
17. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402-408. doi: 10.1006/meth.2001.1262
18. Meijer S, Otero J, Olivares R, Andersen MR, Olsson L, Nielsen J (2009) Overexpression of isocitrate lyase - glyoxylate bypass influence on metabolism in Aspergillus niger. Metab Eng 11(2):107-116. doi: 10.1016/j.ymben.2008.12.002
19. Nolan T, Hands RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1(3):1559-1582
20. Panagiotou G, Andersen MR, Grotkjaer T, Regueira TB, Hofmann G, Nielsen J, Olsson L (2008) Systems analysis unfolds the relationship between the phosphoketolase pathway and growth in Aspergillus nidulans. PLoS One 3(12):e3847. doi: 10.1371/journal.pone.0003847
21. 13C-based metabolic flux analysis. Appl Microbiol Biotechnol 95(4):1001-1010. doi: 10.1007/s00253-012-3936-0
22. Payne GA, Nierman WC, Wortman JR, Pritchard BL, Brown D, Dean RA, Bhatnagar D, Cleveland TE, Machida M, Yu J (2006) Whole genome comparison of Aspergillus flavus and A. oryzae. Med Mycol 44(s1):9-11. doi: 10.1080/13693780600835716
23. Pedersen H, Carlsen M, Nielsen J (1999) Identification of enzymes and quantification of metabolic fluxes in the wild type and in a recombinant Aspergillus oryzae strain. Appl Environ Microbiol 65(1):11-19
24. Peleg Y, Barak A, Scrutton M, Goldberg I (1989) Malic acid accumulation by Aspergillus flavus. Appl Microbiol Biotechnol 30(2):176-183. doi: 10.1007/bf00264008
25. Regev-Rudzki N, Battat E, Goldberg I, Pines O (2009) Dual localization of fumarase is dependent on the integrity of the glyoxylate shunt. Mol Microbiol 72(2):297-306. doi: 10.1111/j.1365-2958.2009.06659.x
26. Sakai K, Kinoshita H, Nihira T (2012) Heterologous expression system in Aspergillus oryzae for fungal biosynthetic gene clusters of secondary metabolites. Appl Microbiol Biotechnol 93(5):2011-2022. doi: 10.1007/s00253-011-3657-9
27. Scalcinati G, Otero JM, Van Vleet JRH, Jeffries TW, Olsson L, Nielsen J (2012) Evolutionary engineering of Saccharomyces cerevisiae for efficient aerobic xylose consumption. FEMS Yeast Res 12(5):582-597. doi: 10.1111/j.1567-1364.2012.00808.x
28. Schmidt K, Marx A, de Graaf AA, Wiechert W, Sahm H, Nielsen J, Villadsen J (1998) 13C Tracer experiments and metabolite balancing for metabolic flux analysis: comparing two approaches. Biotechnol Bioeng 58(2-3):254-257. doi: 10.1002/(sici)1097-0290(19980420)58:2/3<254::aid-bit19>3.0.co;2-c
29. Shen Y, Chen X, Peng B, Chen L, Hou J, Bao X (2012) An efficient xylose-fermenting recombinant Saccharomyces cerevisiae strain obtained through adaptive evolution and its global transcription profile. Appl Microbiol Biotechnol 96(4):1079-1091. doi: 10.1007/s00253-012-4418-0
30. Udvardi MK, Czechowski T, Scheible W-R (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20(7):1736-1737. doi: 10.1105/tpc.108.061143
31. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 - new capabilities and interfaces. Nucleic Acids Res 40(15):e115. doi: 10.1093/nar/gks596
32. van Winden W, Wittmann C, Heinzle E, Heijnen J (2002) Correcting mass isotopomer distributions for naturally occurring isotopes. Biotechnol Bioeng 80:477-479
33. Vongsangnak W, Olsen P, Hansen K, Krogsgaard S, Nielsen J (2008) Improved annotation through genome-scale metabolic modeling of Aspergillus oryzae. BMC Genomics 9(1):245
34. 13C metabolic flux analysis. Metab Eng 3:195-206
35. Wittmann C (2007) Fluxome analysis using GC-MS. Microb Cell Fact 6(1):6
36. Zelle RM, de Hulster E, van Winden WA, de Waard P, Dijkema C, Winkler AA, Geertman J-MA, van Dijken JP, Pronk JT, van Maris AJA (2008) Malic acid production by Saccharomyces cerevisiae: engineering of pyruvate carboxylation, oxaloacetate reduction, and malate export. Appl Environ Microbiol 74(9):2766-2777. doi: 10.1128/aem.02591-07