Metabolic engineering of an ATP-neutral embden-meyerhof-parnas pathway in Corynebacterium glutamicum: Growth restoration by an adaptive point mutation in NADH dehydrogenase

Applied and Environmental Microbiology

Volumn 81, Issue 6, 2015, Pages 1996-2005

  Reddy, Gajendar Komati ^a   Lindner, Steffen N ^a,b   Wendisch, Volker F ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b Algenol Biofuels   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ELECTRON TRANSPORT PROPERTIES; ESCHERICHIA COLI; GLUCOSE; PATHOLOGY; PHOSPHORYLATION; PLANTS (BOTANY); RESTORATION;

CLOSTRIDIUM ACETOBUTYLICUM; CORYNEBACTERIUM GLUTAMICUM; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GLYCOLYTIC PATHWAYS; HETEROLOGOUS EXPRESSION; SINGLE-POINT MUTATION; SOLE CARBON SOURCE; SOLUBLE TRANSHYDROGENASE;

METABOLIC ENGINEERING;

AMINO ACID; ENZYME ACTIVITY; GROWTH RATE; IDENTIFICATION KEY; METABOLISM; MICROBIAL ACTIVITY; MUTATION; SUBSTRATE;

CLOSTRIDIUM ACETOBUTYLICUM; CORYNEBACTERIUM GLUTAMICUM; ESCHERICHIA COLI;

ADENOSINE TRIPHOSPHATE; CARBON; GLUCOSE; MUTANT PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) TRANSHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

CLOSTRIDIUM ACETOBUTYLICUM; CORYNEBACTERIUM GLUTAMICUM; ENZYMOLOGY; ESCHERICHIA COLI; GENE REPRESSION; GENETICS; GLYCOLYSIS; GROWTH, DEVELOPMENT AND AGING; METABOLIC ENGINEERING; METABOLISM; POINT MUTATION;

ADENOSINE TRIPHOSPHATE; CARBON; CLOSTRIDIUM ACETOBUTYLICUM; CORYNEBACTERIUM GLUTAMICUM; ELECTRON TRANSPORT COMPLEX I; ESCHERICHIA COLI; GLUCOSE; GLYCOLYSIS; METABOLIC ENGINEERING; MUTANT PROTEINS; NADH DEHYDROGENASE; NADP TRANSHYDROGENASES; POINT MUTATION; SUPPRESSION, GENETIC;

EID: 84924678364     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03116-14     Document Type: Article

References (68)

1. Bar-Even A, Flamholz A, Noor E, Milo R. 2012. Rethinking glycolysis: on the biochemical logic of metabolic pathways. Nat Chem Biol 8:509-517. http://dx.doi.org/10.1038/nchembio.971.
2. Pfeiffer T, Schuster S, Bonhoeffer S. 2001. Cooperation and competition in the evolution of ATP-producing pathways. Science 292:504-507. http://dx.doi.org/10.1126/science.1058079.
3. Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R. 2013. Glycolytic strategy as a tradeoff between energy yield and protein cost. Proc Natl Acad Sci USA 110:10039-10044. http://dx.doi.org/10.1073/pnas.1215283110.
4. Benisch F, Boles E. 2014. The bacterial Entner-Doudoroff pathway does not replace glycolysis in Saccharomyces cerevisiae due to the lack of activity of iron-sulfur cluster enzyme 6-phosphogluconate dehydratase. J Biotechnol 171:45-55. http://dx.doi.org/10.1016/j.jbiotec.2013.11.025.
5. Valverde F, Losada M, Serrano A. 1999. Engineering a central metabolic pathway: glycolysis with no net phosphorylation in an Escherichia coli gap mutant complemented with a plant GapN gene. FEBS Lett 449:153-158. http://dx.doi.org/10.1016/S0014-5793(99)00430-5.
6. +-dependent glyceraldehyde 3-phosphate dehydrogenase from Streptococcus mutans. Antonie Van Leeuwenhoek 104:913-924. http://dx.doi.org/10.1007/s10482-013-0010-6.
7. Chinen A, Kozlov YI, Hara Y, Izui H, Yasueda H. 2007. Innovative metabolic pathway design for efficient L-glutamate production by suppressing CO2 emission. J Biosci Bioeng 103:262-269. http://dx.doi.org/10.1263/jbb.103.262.
8. Jensen JV, Wendisch VF. 2013. Ornithine cyclodeaminase-based proline production by Corynebacterium glutamicum. Microb Cell Fact 12:63. http://dx.doi.org/10.1186/1475-2859-12-63.
9. Sindelar G, Wendisch VF. 2007. Improving lysine production by Corynebacterium glutamicum through DNA microarray-based identification of novel target genes. Appl Microbiol Biotechnol 76:677-689. http://dx.doi.org/10.1007/s00253-007-0916-x.
10. Peters-Wendisch P, Stolz M, Etterich H, Kennerknecht N, Sahm H, Eggeling L. 2005. Metabolic engineering of Corynebacterium glutamicum for L-serine production. Appl Environ Microbiol 71:7139-7144. http://dx.doi.org/10.1128/AEM.71.11.7139-7144.2005.
11. Heider SA, Peters-Wendisch P, Wendisch VF. 2012. Carotenoid biosynthesis and overproduction in Corynebacterium glutamicum. BMC Microbiol 12:198. http://dx.doi.org/10.1186/1471-2180-12-198.
12. 40 carotenoids by metabolically engineered Corynebacterium glutamicum. Appl Microbiol Biotechnol 98:1223-1235. http://dx.doi.org/10.1007/s00253-013-5359-y.
13. Blombach B, Riester T, Wieschalka S, Ziert C, Youn JW, Wendisch VF, Eikmanns BJ. 2011. Corynebacterium glutamicum tailored for efficient isobutanol production. Appl Environ Microbiol 77:3300-3310. http://dx.doi.org/10.1128/AEM.02972-10.
14. Wieschalka S, Blombach B, Bott M, Eikmanns BJ. 2013. Bio-based production of organic acids with Corynebacterium glutamicum. Microb Biotechnol 6:87-102. http://dx.doi.org/10.1111/1751-7915.12013.
15. Zahoor A, Otten A, Wendisch VF. 2014. Metabolic engineering of Corynebacterium glutamicum for glycolate production. J Biotechnol 192: 366-375. http://dx.doi.org/10.1016/j.jbiotec.2013.12.020.
16. Schneider J, Wendisch VF. 2010. Putrescine production by engineered Corynebacterium glutamicum. Appl Microbiol Biotechnol 88:859-868. http://dx.doi.org/10.1007/s00253-010-2778-x.
17. Seibold G, Auchter M, Berens S, Kalinowski J, Eikmanns BJ. 2006. Utilization of soluble starch by a recombinant Corynebacterium glutamicum strain: growth and lysine production. J Biotechnol 124:381-391. http://dx.doi.org/10.1016/j.jbiotec.2005.12.027.
18. Tsuchidate T, Tateno T, Okai N, Tanaka T, Ogino C, Kondo A. 2011. Glutamate production from beta-glucan using endoglucanase-secreting Corynebacterium glutamicum. Appl Microbiol Biotechnol 90:895-901. http://dx.doi.org/10.1007/s00253-011-3116-7.
19. Meiswinkel TM, Rittmann D, Lindner SN, Wendisch VF. 2013. Crude glycerol-based production of amino acids and putrescine by Corynebacterium glutamicum. Bioresour Technol 145:254-258. http://dx.doi.org/10.1016/j.biortech.2013.02.053.
20. Uhde A, Youn JW, Maeda T, Clermont L, Matano C, Kramer R, Wendisch VF, Seibold GM, Marin K. 2013. Glucosamine as carbon source for amino acid-producing Corynebacterium glutamicum. Appl Microbiol Biotechnol 97:1679-1687. http://dx.doi.org/10.1007/s00253-012-4313-8.
21. Matano C, Uhde A, Youn JW, Maeda T, Clermont L, Marin K, Kramer R, Wendisch VF, Seibold GM. 2014. Engineering of Corynebacterium glutamicum for growth and L-lysine and lycopene production from Nacetylglucosamine. Appl Microbiol Biotechnol 98:5633-5643. http://dx.doi.org/10.1007/s00253-014-5676-9.
22. Meiswinkel TM, Gopinath V, Lindner SN, Nampoothiri KM, Wendisch VF. 2013. Accelerated pentose utilization by Corynebacterium glutamicum for accelerated production of lysine, glutamate, ornithine and putrescine. Microb Biotechnol 6:131-140. http://dx.doi.org/10.1111/1751-7915.12001.
23. Adachi N, Takahashi C, Ono-Murota N, Yamaguchi R, Tanaka T, Kondo A. 2013. Direct L-lysine production from cellobiose by Corynebacterium glutamicum displaying beta-glucosidase on its cell surface. Appl Microbiol Biotechnol 97:7165-7172. http://dx.doi.org/10.1007/s00253-013-5009-4.
24. Kelle R, Hermann T, Bathe B. 2005. L-Lysine production, p 465-488. In Eggeling L, BottM(ed), Handbook of Corynebacterium glutamicum. CRC Press, Boca Raton, FL.
25. Mori M, Shiio I. 1987. Phosphoenolpyruvate:sugar phosphotransferase systems and sugar metabolism in Brevibacterium flavum. Agric Biol Chem 51:2671-2678. http://dx.doi.org/10.1271/bbb1961.51.2671.
26. Zahoor A, Lindner SN, Wendisch VF. 2012. Metabolic engineering of Corynebacterium glutamicum aimed at alternative carbon sources and new products. Comput Struct Biotechnol J 3:e201210004. http://dx.doi.org/10.5936/csbj.201210004.
27. Reinscheid DJ, Schnicke S, Rittmann D, Zahnow U, Sahm H, Eikmanns BJ. 1999. Cloning, sequence analysis, expression and inactivation of the Corynebacterium glutamicum pta-ack operon encoding phosphotransacetylase and acetate kinase. Microbiology 145:503-513. http://dx.doi.org/10.1099/13500872-145-2-503.
28. Kabus A, Niebisch A, Bott M. 2007. Role of cytochrome bd oxidase from Corynebacterium glutamicum in growth and lysine production. Appl Environ Microbiol 73:861-868. http://dx.doi.org/10.1128/AEM.01818-06.
29. Bott M, Niebisch A. 2003. The respiratory chain of Corynebacterium glutamicum. J Biotechnol 104:129-153. http://dx.doi.org/10.1016/S0168-1656(03)00144-5.
30. Niebisch A, Bott M. 2003. Purification of a cytochrome bc1-aa3 supercomplex with quinol oxidase activity from Corynebacterium glutamicum. Identification of a fourth subunit of cytochrome aa3 oxidase and mutational analysis of diheme cytochrome c1. J Biol Chem 278:4339-4346. http://dx.doi.org/10.1074/jbc.M210499200.
31. o-ATP synthase mutant devoid of oxidative phosphorylation. Biochim Biophys Acta 1817:370-380. http://dx.doi.org/10.1016/j.bbabio.2011.10.006.
32. Noor E, Eden E, Milo R, Alon U. 2010. Central carbon metabolism as a minimal biochemical walk between precursors for biomass and energy. Mol Cell 39:809-820. http://dx.doi.org/10.1016/j.molcel.2010.08.031.
33. Reddy GK, Wendisch VF. 2014. Characterization of 3-phosphoglycerate kinase from Corynebacterium glutamicum and its impact on amino acid production. BMC Microbiol 14:54. http://dx.doi.org/10.1186/1471-2180-14-54.
34. Rosenberg LL, Arnon DI. 1955. The preparation and properties of a new glyceraldehyde-3-phosphate dehydrogenase from photosynthetic tissues. J Biol Chem 217:361-371.
35. Takeno S, Murata R, Kobayashi R, Mitsuhashi S, Ikeda M. 2010. Engineering of Corynebacterium glutamicum with an NADPH-generating glycolytic pathway for L-lysine production. Appl Environ Microbiol 76: 7154-7160. http://dx.doi.org/10.1128/AEM.01464-10.
36. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557-580. http://dx.doi.org/10.1016/S0022-2836(83)80284-8.
38. Eggeling L, Bott M (ed). 2005. Handbook of Corynebacterium glutamicum. CRC Press, Boca Raton, FL.
39. Sambrook J, Russell D. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Eikmanns BJ, Thum-Schmitz N, Eggeling L, Ludtke KU, Sahm H. 1994. Nucleotide sequence, expression and transcriptional analysis of the Corynebacterium glutamicum gltA gene encoding citrate synthase. Microbiology 140:1817-1828. http://dx.doi.org/10.1099/13500872-140-8-1817.
41. Tauch A, Kirchner O, Loffler B, Gotker S, Puhler A, Kalinowski J. 2002. Efficient electrotransformation of Corynebacterium diphtheriae with a mini-replicon derived from the Corynebacterium glutamicum plasmid pGA1. Curr Microbiol 45:362-367. http://dx.doi.org/10.1007/s00284-002-3728-3.
42. Schäfer A, Tauch A, Jäger W, Kalinowski J, Thierbach G, Puhler A. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73. http://dx.doi.org/10.1016/0378-1119(94)90324-7.
43. Siedler S, Lindner SN, Bringer S, Wendisch VF, Bott M. 2013. Reductive whole-cell biotransformation with Corynebacterium glutamicum: improvement of NADPH generation from glucose by a cyclized pentose phosphate pathway using pfkA and gapA deletion mutants. Appl Microbiol Biotechnol 97:143-152. http://dx.doi.org/10.1007/s00253-012-4314-7.
44. Milse J, Petri K, Ruckert C, Kalinowski J. 2014. Transcriptional response of Corynebacterium glutamicum ATCC 13032 to hydrogen peroxide stress and characterization of the OxyR regulon. J Biotechnol 190:40-54. http://dx.doi.org/10.1016/j.jbiotec.2014.07.452.
45. Blom J, Jakobi T, Doppmeier D, Jaenicke S, Kalinowski J, Stoye J, Goesmann A. 2011. Exact and complete short-read alignment to microbial genomes using Graphics Processing Unit programming. Bioinformatics 27:1351-1358. http://dx.doi.org/10.1093/bioinformatics/btr151.
46. Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, Burkovski A, Dusch N, Eggeling L, Eikmanns BJ, Gaigalat L, Goesmann A, Hartmann M, Huthmacher K, Kramer R, Linke B, McHardy AC, Meyer F, Mockel B, Pfefferle W, Puhler A, Rey DA, Ruckert C, Rupp O, Sahm H, Wendisch VF, Wiegrabe I, Tauch A. 2003. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol 104:5-25. http://dx.doi.org/10.1016/S0168-1656(03)00154-8.
47. Peters-Wendisch P, Gotker S, Heider SAE, Komati Reddy G, Nguyen AQ, Stansen KC, Wendisch VF. 2014. Engineering biotin prototrophic Corynebacterium glutamicum strains for amino acid, diamine and carotenoid production. J Biotechnol 192:346-354. http://dx.doi.org/10.1016/j.jbiotec.2014.01.023.
48. Stansen C, Uy D, Delaunay S, Eggeling L, Goergen JL, Wendisch VF. 2005. Characterization of a Corynebacterium glutamicum lactate utilization operon induced during temperature-triggered glutamate production. Appl Environ Microbiol 71:5920-5928. http://dx.doi.org/10.1128/AEM.71.10.5920-5928.2005.
49. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 72:248-254. http://dx.doi.org/10.1016/0003-2697(76)90527-3.
50. Omumasaba CA, Okai N, Inui M, Yukawa H. 2004. Corynebacterium glutamicum glyceraldehyde-3-phosphate dehydrogenase isoforms with opposite, ATP-dependent regulation. J Mol Microbiol Biotechnol 8:91-103. http://dx.doi.org/10.1159/000084564.
51. Iddar A, Valverde F, Serrano A, Soukri A. 2002. Expression, purification, and characterization of recombinant nonphosphorylating NADPdependent glyceraldehyde-3-phosphate dehydrogenase from Clostridium acetobutylicum. Protein Expr Purif 25:519-526. http://dx.doi.org/10.1016/S1046-5928(02)00032-3.
52. Sauer U, Canonaco F, Heri S, Perrenoud A, Fischer E. 2004. The soluble and membrane-bound transhydrogenases UdhA and PntAB have divergent functions in NADPH metabolism of Escherichia coli. J Biol Chem 279:6613-6619. http://dx.doi.org/10.1074/jbc.M311657200.
53. Matsushita K, Otofuji A, Iwahashi M, Toyama H, Adachi O. 2001. NADH dehydrogenase of Corynebacterium glutamicum. Purification of an NADH dehydrogenase II homolog able to oxidize NADPH. FEMS Microbiol Lett 204:271-276. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10896.x.
54. Baumgart M, Unthan S, Ruckert C, Sivalingam J, Grunberger A, Kalinowski J, Bott M, Noack S, Frunzke J. 2013. Construction of a prophage-free variant of Corynebacterium glutamicum ATCC 13032 for use as a platform strain for basic research and industrial biotechnology. Appl Environ Microbiol 79:6006-6015. http://dx.doi.org/10.1128/AEM.01634-13.
55. Michalecka AM, Agius SC, Moller IM, Rasmusson AG. 2004. Identification of a mitochondrial externalNADPHdehydrogenase by overexpression in transgenic Nicotiana sylvestris. Plant J 37:415-425. http://dx.doi.org/10.1046/j.1365-313X.2003.01970.x.
56. Nantapong N, Otofuji A, Migita CT, Adachi O, Toyama H, Matsushita K. 2005. Electron transfer ability from NADH to menaquinone and from NADPH to oxygen of type II NADH dehydrogenase of Corynebacterium glutamicum. Biosci Biotechnol Biochem 69:149-159. http://dx.doi.org/10.1271/bbb.69.149.
57. Bommareddy RR, Chen Z, Rappert S, Zeng AP. 2014. A de novo NADPH generation pathway for improving lysine production of Corynebacterium glutamicum by rational design of the coenzyme specificity of glyceraldehyde 3-phosphate dehydrogenase. Metab Eng 25:30-37. http://dx.doi.org/10.1016/j.ymben.2014.06.005.
58. Canonaco F, Hess TA, Heri S, Wang T, Szyperski T, Sauer U. 2001. Metabolic flux response to phosphoglucose isomerase knock-out in Escherichia coli and impact of overexpression of the soluble transhydrogenase UdhA. FEMS Microbiol Lett 204:247-252. http://dx.doi.org/10.1111/j.1574-6968.2001.tb10892.x.
59. Lindner SN, Petrov DP, Hagmann CT, Henrich A, Kramer R, Eikmanns BJ, Wendisch VF, Seibold GM. 2013. Phosphotransferase systemmediated glucose uptake is repressed in phosphoglucoisomerase-deficient Corynebacterium glutamicum strains. Appl Environ Microbiol 79:2588-2595. http://dx.doi.org/10.1128/AEM.03231-12.
60. 13C-metabolic flux analysis for batch culture of Escherichia coli and its pyk and pgi gene knockout mutants based on mass isotopomer distribution of intracellular metabolites. Biotechnol Prog 26: 975-992. http://dx.doi.org/10.1002/btpr.420.
61. Jackson JB. 2003. Proton translocation by transhydrogenase. FEBS Lett 555:176-177. http://dx.doi.org/10.1016/S0014-5793(03)01123-2.
62. 13C metabolic flux analysis of pyruvate dehydrogenase complex-deficient, L-valine-producing Corynebacterium glutamicum. Appl Environ Microbiol 77:6644-6652. http://dx.doi.org/10.1128/AEM.00575-11.
63. Jiang LY, Zhang YY, Li Z, Liu JZ. 2013. Metabolic engineering of Corynebacterium glutamicum for increasing the production of L-ornithine by increasing NADPH availability. J Ind Microbiol Biotechnol 40:1143-1151. http://dx.doi.org/10.1007/s10295-013-1306-2.
64. Kabus A, Georgi T, Wendisch VF, Bott M. 2007. Expression of the Escherichia coli pntAB genes encoding a membrane-bound transhydrogenase in Corynebacterium glutamicum improves L-lysine formation. Appl Microbiol Biotechnol 75:47-53. http://dx.doi.org/10.1007/s00253-006-0804-9.
65. Auriol C, Bestel-Corre G, Claude JB, Soucaille P, Meynial-Salles I. 2011. Stress-induced evolution of Escherichia coli points to original concepts in respiratory cofactor selectivity. Proc Natl Acad Sci USA 108:1278-1283. http://dx.doi.org/10.1073/pnas.1010431108.
66. Bott M, Niebisch A. 2005. Respiratory energy metabolism, p 305-332. In Eggeling L, BottM(ed), Handbook of Corynebacterium glutamicum. CRC Press, Boca Raton, FL.
67. Kato O, Youn JW, Stansen KC, Matsui D, Oikawa T, Wendisch VF. 2010. Quinone-dependent D-lactate dehydrogenase Dld (Cg1027) is essential for growth of Corynebacterium glutamicum on D-lactate. BMC Microbiol 10:321. http://dx.doi.org/10.1186/1471-2180-10-321.
68. Molenaar D, van der Rest ME, Petrovic S. 1998. Biochemical and genetic characterization of the membrane-associated malate dehydrogenase (acceptor) from Corynebacterium glutamicum. Eur J Biochem 254:395-403. http://dx.doi.org/10.1046/j.1432-1327.1998.2540395.x.