Lysine production from the sugar alcohol mannitol: Design of the cell factory Corynebacterium glutamicum SEA-3 through integrated analysis and engineering of metabolic pathway fluxes

Metabolic Engineering

Volumn 47, Issue , 2018, Pages 475-487

  Hoffmann, Sarah Lisa ^a   Jungmann, Lukas ^a   Schiefelbein, Sarah ^a   Peyriga, Lindsay ^b,c,d   Cahoreau, Edern ^b,c,d   Portais, Jean Charles ^b,c,d   Becker, Judith ^a   Wittmann, Christoph ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b INSA   (France)

^c UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

^d CNRS   (France)

Author keywords

13C; Biomass; Elementary flux mode; Fructokinase; Fructose; Glyceraldehyde 3 phosphate dehydrogenase; Lysine; Macroalgae; Metabolic flux analysis; NADPH; Oxidative pentose phosphate pathway; Seaweed

Indexed keywords

BIOMASS; CELL ENGINEERING; DRUG PRODUCTS; FRUCTOSE; METABOLISM; POLYOLS; SEAWEED;

ELEMENTARY FLUX MODE; FRUCTOKINASE; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE; LYSINE; MACRO-ALGAE; METABOLIC FLUX ANALYSIS; NADPH; OXIDATIVE PENTOSE PHOSPHATE PATHWAYS; ^13C;

AMINO ACIDS;

FRUCTOKINASE; FRUCTOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE (NADP)(PHOSPHORYLATING); LYSINE; MANNITOL; PENTOSE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; BACTERIAL PROTEIN;

ALCOHOL PRODUCTION; ARTICLE; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; GENE DELETION; METABOLIC ENGINEERING; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; REPRESSOR GENE; STREPTOCOCCUS MUTANS; BIOSYNTHESIS; GENETICS; METABOLISM; TRANSGENIC MICROORGANISM;

BACTERIAL PROTEINS; CORYNEBACTERIUM GLUTAMICUM; LYSINE; MANNITOL; METABOLIC ENGINEERING; MICROORGANISMS, GENETICALLY-MODIFIED; STREPTOCOCCUS MUTANS;

EID: 85047015170     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2018.04.019     Document Type: Article

References (58)

1. Becker, J., Buschke, N., Bücker, R., Wittmann, C., Systems level engineering of Corynebacterium glutamicum – reprogramming translational efficiency for superior production. Eng. Life Sci. 10 (2010), 430–438.
2. Becker, J., Gießelmann, G., Hoffmann, S.L., Wittmann, C., Corynebacterium glutamicum for sustainable bio-production: from metabolic physiology to systems metabolic engineering. Zhao, H., Zeng, A.P., (eds.) Synthetic Biology – Metabolic Engineering., 2016, Springer, Heidelberg.
3. Becker, J., Klopprogge, C., Herold, A., Zelder, O., Bolten, C.J., Wittmann, C., Metabolic flux engineering of L-lysine production in Corynebacterium glutamicum–over expression and modification of G6P dehydrogenase. J. Biotechnol. 132 (2007), 99–109.
4. Becker, J., Klopprogge, C., Zelder, O., Heinzle, E., Wittmann, C., Amplified expression of fructose 1,6-bisphosphatase in Corynebacterium glutamicum increases in vivo flux through the pentose phosphate pathway and lysine production on different carbon sources. Appl. Environ. Microbiol. 71 (2005), 8587–8596.
5. Becker, J., Wittmann, C., Bio-based production of chemicals, materials and fuels -Corynebacterium glutamicum as versatile cell factory. Curr. Opin. Biotechnol. 23 (2012), 631–640.
6. Becker, J., Wittmann, C., Advanced biotechnology: metabolically engineered cells for the bio-based production of chemicals and fuels, materials, and health-care products. Angew. Chem. Int. Ed. Engl. 54 (2015), 3328–3350.
7. Becker, J., Zelder, O., Haefner, S., Schröder, H., Wittmann, C., From zero to hero–design-based systems metabolic engineering of Corynebacterium glutamicum for L-lysine production. Metab. Eng. 13 (2011), 159–168.
8. Bommareddy, R.R., Chen, Z., Rappert, S., Zeng, A.P., 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 (2014), 30–37.
9. Buschke, N., Becker, J., Schäfer, R., Kiefer, P., Biedendieck, R., Wittmann, C., Systems metabolic engineering of xylose-utilizing Corynebacterium glutamicum for production of 1,5-diaminopentane. Biotechnol. J. 8 (2013), 557–570.
10. Buschke, N., Schäfer, R., Becker, J., Wittmann, C., Metabolic engineering of industrial platform microorganisms for biorefinery applications–optimization of substrate spectrum and process robustness by rational and evolutive strategies. Bioresour. Technol. 135 (2013), 544–554.
11. Buschke, N., Schröder, H., Wittmann, C., Metabolic engineering of Corynebacterium glutamicum for production of 1,5-diaminopentane from hemicellulose. Biotechnol. J. 6 (2011), 306–317.
12. 13C nuclear magnetic resonance spectroscopy. Infect. Immun. 66 (1998), 2996–2998.
13. Christensen, B., Thykaer, J., Nielsen, J., Metabolic characterization of high- and low-yielding strains of Penicillium chrysogenum. Appl. Microbiol. Biotechnol. 54 (2000), 212–217.
14. +-dependent glyceraldehyde-3-phosphate dehydrogenases from Streptococcus mutans. J. Biol. Chem. 254 (1979), 1134–1142.
15. Eggeling, L., Bott, M., A giant market and a powerful metabolism: L-lysine provided by Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 99 (2015), 3387–3394.
16. Enquist-Newman, M., Faust, A.M.E., Bravo, D.D., Santos, C.N.S., Raisner, R.M., Hanel, A., Sarvabhowman, P., Le, C., Regitsky, D.D., Cooper, S.R., Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature 505 (2014), 239–243.
17. Gibson, D.G., Young, L., Chuang, R.Y., Venter, J.C., Hutchison, C.A. 3rd, Smith, H.O., Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6 (2009), 343–345.
18. Goh, C.S., Lee, K.T., A visionary and conceptual macroalgae-based third-generation bioethanol (TGB) biorefinery in Sabah, Malaysia as an underlay for renewable and sustainable development. Renew. Sustain. Energy Rev. 14 (2010), 842–848.
19. Heider, S.A., Peters-Wendisch, P., Wendisch, V.F., Carotenoid biosynthesis and overproduction in Corynebacterium glutamicum. BMC Microbiol., 12, 2012, 198, 10.1186/1471-2180-12-198 Sep 10.
20. Iwamoto, K., Shiraiwa, Y., Salt-regulated mannitol metabolism in algae. Mar. Biotechnol. 7 (2005), 407–415.
21. Kawaguchi, H., Vertes, A.A., Okino, S., Inui, M., Yukawa, H., Engineering of a xylose metabolic pathway in Corynebacterium glutamicum. Appl. Environ. Microbiol. 72 (2006), 3418–3428.
22. Kiefer, P., Heinzle, E., Zelder, O., Wittmann, C., Comparative metabolic flux analysis of lysine-producing Corynebacterium glutamicum cultured on glucose or fructose. Appl. Environ. Microbiol. 70 (2004), 229–239.
23. Kim, I.K., Jeong, W.K., Lim, S.H., Hwang, I.K., Kim, Y.H., The small ribosomal protein S12P gene rpsL as an efficient positive selection marker in allelic exchange mutation systems for Corynebacterium glutamicum. J. Microbiol. Methods 84 (2011), 128–130.
24. Koffas, M., Stephanopoulos, G., Strain improvement by metabolic engineering: lysine production as a case study for systems biology. Curr. Opin. Biotechnol. 16 (2005), 361–366.
25. Kotrba, P., Inui, M., Yukawa, H., A single V317A or V317M substitution in Enzyme II of a newly identified beta-glucoside phosphotransferase and utilization system of Corynebacterium glutamicum R extends its specificity towards cellobiose. Microbiology 149 (2003), 1569–1580.
26. Krömer, J.O., Fritz, M., Heinzle, E., Wittmann, C., In vivo quantification of intracellular amino acids and intermediates of the methionine pathway in Corynebacterium glutamicum. Anal. Biochem. 340 (2005), 171–173.
27. Marx, A., Striegel, K., de Graaf, A.A., Sahm, H., Eggeling, L., Response of the central metabolism of Corynebacterium glutamicum to different flux burdens. Biotechnol. Bioeng. 56 (1997), 168–180.
28. Melzer, G., Esfandabadi, M.E., Franco-Lara, E., Wittmann, C., Flux design: In silico design of cell factories based on correlation of pathway fluxes to desired properties. BMC Syst. Biol., 3, 2009, 120.
29. Moon, M.-W., Kim, H.-J., Oh, T.-K., Shin, C.-S., Lee, J.-S., Kim, S.-J., Lee, J.-K., Analyses of enzyme II gene mutants for sugar transport and heterologous expression of fructokinase gene in Corynebacterium glutamicum ATCC 13032. FEMS Microbiol. Lett. 244 (2005), 259–266.
30. Moon, M.W., Park, S.Y., Choi, S.K., Lee, J.K., The phosphotransferase system of Corynebacterium glutamicum: features of sugar transport and carbon regulation. J. Mol. Microbiol. Biotechnol. 12 (2007), 43–50.
31. Naik, S.N., Goud, V.V., Rout, P.K., Dalai, A.K., Production of first and second generation biofuels: a comprehensive review. Renew. Sustain. Energy Rev. 14 (2010), 578–597.
32. 13C labeling experiments. J. Biotechnol. 129 (2007), 249–267.
33. Ota, A., Kawai, S., Oda, H., Iohara, K., Murata, K., Production of ethanol from mannitol by the yeast strain Saccharomyces paradoxus NBRC 0259. J. Biosci. Bioeng. 116 (2013), 327–332.
34. Peng, X., Okai, N., Vertes, A.A., Inatomi, K., Inui, M., Yukawa, H., Characterization of the mannitol catabolic operon of Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 91 (2011), 1375–1387.
35. 13C-based metabolic flux analysis. Microb. Cell Fact., 8, 2009, 25.
36. Rasmus, B., Valderrama, D., Radulovich, R., Diana, J., Capron, M., Mckinnie, C., Amir Cedric, M., Hopkins, K., Yarish, C., Goudey, C., Forster, J., Seaweed Aquaculture for Food Security, Income Generation and Environmental Health in Tropical Developing Countries. 2016, World Bank Group, Washington, D.C.
37. Rohles, C.M., Giesselmann, G., Kohlstedt, M., Wittmann, C., Becker, J., Systems metabolic engineering of Corynebacterium glutamicum for the production of the carbon-5 platform chemicals 5-aminovalerate and glutarate. Microb. Cell Fact., 15, 2016, 154.
38. Ryu, S., Karim, M.N., A whole cell biocatalyst for cellulosic ethanol production from dilute acid-pretreated corn stover hydrolyzates. Appl. Microbiol. Biotechnol. 91 (2011), 529–542.
39. Sasaki, M., Jojima, T., Inui, M., Yukawa, H., Simultaneous utilization of D-cellobiose, D-glucose, and D-xylose by recombinant Corynebacterium glutamicum under oxygen-deprived conditions. Appl. Microbiol. Biotechnol. 81 (2008), 691–699.
40. Schilling, O., Frick, O., Herzberg, C., Ehrenreich, A., Heinzle, E., Wittmann, C., Stulke, J., Transcriptional and metabolic responses of Bacillus subtilis to the availability of organic acids: transcription regulation is important but not sufficient to account for metabolic adaptation. Appl. Environ. Microbiol. 73 (2007), 499–507.
41. Schneider, J., Niermann, K., Wendisch, V.F., Production of the amino acids L-glutamate, L-lysine, L-ornithine and L-arginine from arabinose by recombinant Corynebacterium glutamicum. J. Biotechnol. 154 (2011), 191–198.
42. Stokstad, E., Biofuels. Engineered superbugs boost hopes of turning seaweed into fuel. Science, 335, 2012, 273.
43. Takeno, S., Hori, K., Ohtani, S., Mimura, A., Mitsuhashi, S., Ikeda, M., L-Lysine production independent of the oxidative pentose phosphate pathway by Corynebacterium glutamicum with the Streptococcus mutans gapN gene. Metab. Eng. 37 (2016), 1–10.
44. Takeno, S., Murata, R., Kobayashi, R., Mitsuhashi, S., Ikeda, M., Engineering of Corynebacterium glutamicum with an NADPH-generating glycolytic pathway for L-lysine production. Appl. Environ. Microbiol. 76 (2010), 7154–7160.
45. Tan, K.T., Lee, K.T., Mohamed, A.R., Role of energy policy in renewable energy accomplishment: the case of second-generation bioethanol. Energy Policy 36 (2008), 3360–3365.
46. Tiwari, B.K., Troy, D.J., Seaweed Sustainability: Food and Non-Food Applications. 2015, Elsevier Inc., Heidelberg.
47. Ullah, K., Ahmad, M., Sofia, Sharma, V.K., Lu, P., Harvey, A., Zafar, M., Sultana, S., Anyanwu, C.N., Algal biomass as a global source of transport fuels: overview and development perspectives. Prog. Nat. Sci.: Mater. Int. 24 (2014), 329–339.
48. van Hal, J.W., Huijgen, W.J.J., López-Contreras, A.M., Opportunities and challenges for seaweed in the biobased economy. Trends Biotechnol. 32 (2014), 231–233.
49. van Winden, W.A., Wittmann, C., Heinzle, E., Heijnen, J.J., Correcting mass isotopomer distributions for naturally occurring isotopes. Biotechnol. Bioeng. 80 (2002), 477–479.
50. Wang, J., Kim, Y.M., Rhee, H.S., Lee, M.W., Park, J.M., Bioethanol production from mannitol by a newly isolated bacterium, Enterobacter sp. JMP3. Bioresour. Technol. 135 (2013), 199–206.
51. Wittmann, C., Fluxome analysis using GC-MS. Microb. Cell Fact., 6, 2007, 6.
52. Wittmann, C., Becker, J., The L-lysine story. From metabolic pathways to industrial production. Wendisch, V.F., (eds.) Amino Acid Biosynthesis – Pathways, Regulation and Metabolic Engineering., vol. 5, 2007, Springer, Berlin Heidelberg, 40–68.
53. Wittmann, C., De Graaf, A.A., Metabolic flux analysis in Corynebacterium glutamicum. Eggeling, L., Bott, M., (eds.) Handbook of Corynebacterium glutamicum., 2005, CRC Press, Boca Raton, 277–304.
54. Wittmann, C., Hans, M., Heinzle, E., In vivo analysis of intracellular amino acid labelings by GC/MS. Anal. Biochem. 307 (2002), 379–382.
55. Wittmann, C., Heinzle, E., Genealogy profiling through strain improvement by using metabolic network analysis: metabolic flux genealogy of several generations of lysine-producing Corynebacteria. Appl. Environ. Microbiol. 68 (2002), 5843–5859.
56. Wittmann, C., Kiefer, P., Zelder, O., Metabolic fluxes in Corynebacterium glutamicum during lysine production with sucrose as carbon source. Appl. Environ. Microbiol. 70 (2004), 7277–7287.
57. 2 in shake-flasks. Biotechnol. Lett. 25 (2003), 377–380.
58. Yokota, A., Lindley, N.D., Central metabolism: sugar uptake and conversion. Eggeling, L., Bott, M., (eds.) Handbook of Corynebacterium glutamicum., 2005, CRC Press, Boca Raton, 215–240.