Increased production of L-serine in Escherichia coli through Adaptive Laboratory Evolution

Metabolic Engineering

Volumn 39, Issue , 2017, Pages 141-150

  Mundhada, Hemanshu ^a   Seoane, Jose M ^a   Schneider, Konstantin ^a   Koza, Anna ^a   Christensen, Hanne B ^a   Klein, Tobias ^a   Phaneuf, Patrick V ^b   Herrgard, Markus ^a   Feist, Adam M ^a,b   Nielsen, Alex T ^a  

^a Chalmers University of Technology   (Denmark)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Adaptive laboratory evolution (ALE); E. coli; Fermentation; Serine production; Serine tolerance

Indexed keywords

BIOLOGY; ESCHERICHIA COLI; FERMENTATION;

ADAPTIVE LABORATORY EVOLUTION (ALE); DEGRADATION PATHWAYS; E. COLI; GENOME SEQUENCING; INDUSTRIAL BIOTECHNOLOGY; POTENTIAL MECHANISM; SERINE INHIBITION; TOLERANT STRAINS;

AMINO ACIDS;

SERINE; GLUCOSE;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOTECHNOLOGICAL PRODUCTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEGRADATION; ESCHERICHIA COLI; FED BATCH FERMENTATION; MOLECULAR EVOLUTION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; REVERSE ENGINEERING; WHOLE GENOME SEQUENCING; BIOSYNTHESIS; DIRECTED MOLECULAR EVOLUTION; GENE EXPRESSION REGULATION; GENETIC ENHANCEMENT; GENETICS; ISOLATION AND PURIFICATION; METABOLIC ENGINEERING; METABOLISM; PHYSIOLOGY; PROCEDURES; UPREGULATION;

BIOSYNTHETIC PATHWAYS; DIRECTED MOLECULAR EVOLUTION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC ENHANCEMENT; GLUCOSE; METABOLIC ENGINEERING; METABOLIC NETWORKS AND PATHWAYS; SERINE; UP-REGULATION;

EID: 85008192136     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2016.11.008     Document Type: Article

References (50)

1. Ambartsoumian, G., D'Ari, R., Lin, R.T., Newman, E.B., Altered amino acid metabolism in lrp mutants of Escherichia coli K12 and their derivatives. Microbiology 140:Pt 7 (1994), 1737–1744.
2. Arense, P., Bernal, V., Iborra, J.L., Cánovas, M., Metabolic adaptation of Escherichia coli to long-term exposure to salt stress. Process Biochem. 45 (2010), 1459–1467.
3. Ariza, R.R., Cohen, S.P., Bachhawat, N., Levy, S.B., Demple, B., Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli. J. Bacteriol. 176 (1994), 143–148.
4. Arnold, K., Bordoli, L., Kopp, J., Schwede, T., The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 (2006), 195–201.
5. Becker, J., Wittmann, C., Systems and synthetic metabolic engineering for amino acid production - the heartbeat of industrial strain development. Curr. Opin. Biotechnol. 23 (2012), 718–726.
6. Conrad, T.M., Lewis, N.E., Palsson, B.O., Microbial laboratory evolution in the era of genome-scale science. Mol. Syst. Biol., 7, 2011, 509.
7. Costrejean, J.M., Truffa-Bachi, P., Threonine-sensitive homoserine dehydrogenase and aspartokinase activities of Escherichia coli K12. Kinetic and spectroscopic effects upon binding of serine and threonine. J. Biol. Chem. 252 (1977), 5332–5336.
8. de Lorenzo, V., Sekowska, A., Danchin, A., Chemical reactivity drives spatiotemporal organisation of bacterial metabolism. FEMS Microbiol. Rev. 39 (2015), 96–119.
9. Deatherage, D.E., Barrick, J.E., Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol. Biol. 1151 (2014), 165–188.
10. Dragosits, M., Mattanovich, D., Adaptive laboratory evolution - principles and applications for biotechnology. Micro. Cell Fact., 12, 2013, 64.
11. Faehnle, C.R., Liu, X., Pavlovsky, A., Viola, R.E., The initial step in the archaeal aspartate biosynthetic pathway catalyzed by a monofunctional aspartokinase. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 62 (2006), 962–966.
12. Gu, P., Yang, F., Su, T., Li, F., Li, Y., Qi, Q., Construction of an L-serine producing Escherichia coli via metabolic engineering. J. Ind. Microbiol. Biotechnol. 41 (2014), 1443–1450.
13. Guadalupe-Medina, V., Metz, B., Oud, B., van Der Graaf, C.M., Mans, R., Pronk, J.T., van Maris, A.J., Evolutionary engineering of a glycerol-3-phosphate dehydrogenase-negative, acetate-reducing Saccharomyces cerevisiae strain enables anaerobic growth at high glucose concentrations. Microb. Biotechnol. 7 (2014), 44–53.
14. Haft, R.J., Keating, D.H., Schwaegler, T., Schwalbach, M.S., Vinokur, J., Tremaine, M., Peters, J.M., Kotlajich, M.V., Pohlmann, E.L., Ong, I.M., Grass, J.A., Kiley, P.J., Landick, R., Correcting direct effects of ethanol on translation and transcription machinery confers ethanol tolerance in bacteria. Proc. Natl. Acad. Sci. USA 111 (2014), E2576–E2585.
15. Hama, H., Sumita, Y., Kakutani, Y., Tsuda, M., Tsuchiya, T., Target of serine inhibition in Escherichia coli. Biochem. Biophys. Res. Commun. 168 (1990), 1211–1216.
16. Heck, H., Threonine-sensitive aspartokinase-homoserine dehydrognease of Escherichia coli K 12. Evidence for a cooperative tetramer. Biochemistry 11 (1972), 4421–4427.
17. Hemm, M.R., Paul, B.J., Miranda-Rios, J., Zhang, A., Soltanzad, N., Storz, G., Small stress response proteins in Escherichia coli: proteins missed by classical proteomic studies. J. Bacteriol. 192 (2010), 46–58.
18. Kwon, Y.D., Kim, S., Lee, S.Y., Kim, P., Long-term continuous adaptation of Escherichia coli to high succinate stress and transcriptome analysis of the tolerant strain. J. Biosci. Bioeng. 111 (2011), 26–30.
19. LaCroix, R.A., Sandberg, T.E., O'Brien, E.J., Utrilla, J., Ebrahim, A., Guzman, G.I., Szubin, R., Palsson, B.O., Feist, A.M., Use of adaptive laboratory evolution to discover key mutations enabling rapid growth of Escherichia coli K-12 MG1655 on glucose minimal medium. Appl. Environ. Microbiol. 81 (2015), 17–30.
20. Lee, J., Hiibel, S.R., Reardon, K.F., Wood, T.K., Identification of stress-related proteins in Escherichia coli using the pollutant cis-dichloroethylene. J. Appl. Microbiol. 108 (2010), 2088–2102.
21. Lee, J.H., Lee, D.E., Lee, B.U., Kim, H.S., Global analyses of transcriptomes and proteomes of a parent strain and an L-threonine-overproducing mutant strain. J. Bacteriol. 185 (2003), 5442–5451.
22. Lennen, R.M., Nilsson Wallin, A.I., Pedersen, M., Bonde, M., Luo, H., Herrgard, M.J., Sommer, M.O., Transient overexpression of DNA adenine methylase enables efficient and mobile genome engineering with reduced off-target effects. Nucleic Acids Res., 44, 2016, e36.
23. Leuchtenberger, W., Huthmacher, K., Drauz, K., Biotechnological production of amino acids and derivatives: current status and prospects. Appl. Microbiol. Biotechnol. 69 (2005), 1–8.
24. Mattevi, A., Valentini, G., Rizzi, M., Speranza, M.L., Bolognesi, M., Coda, A., Crystal structure of Escherichia coli pyruvate kinase type I: molecular basis of the allosteric transition. Structure 3 (1995), 729–741.
25. Modi, S.R., Camacho, D.M., Kohanski, M.A., Walker, G.C., Collins, J.J., Functional characterization of bacterial sRNAs using a network biology approach. Proc. Natl. Acad. Sci. USA 108 (2011), 15522–15527.
26. Moon, K., Gottesman, S., A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol. Microbiol. 74 (2009), 1314–1330.
27. Morris, G.M., Huey, R., Lindstrom, W., Sanner, M.F., Belew, R.K., Goodsell, D.S., Olson, A.J., AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30 (2009), 2785–2791.
28. Mundhada, H., Schneider, K., Christensen, H.B., Nielsen, A.T., Engineering of high yield production of L-serine in Escherichia coli. Biotechnol. Bioeng. 113 (2016), 807–816.
29. Pereira, B., Zhang, H., De Mey, M., Lim, C.G., Li, Z.J., Stephanopoulos, G., Engineering a novel biosynthetic pathway in Escherichia coli for production of renewable ethylene glycol. Biotechnol. Bioeng. 113 (2016), 376–383.
30. Peters-Wendisch, P., Stolz, M., Etterich, H., Kennerknecht, N., Sahm, H., Eggeling, L., Metabolic engineering of Corynebacterium glutamicum for L-serine production. Appl. Environ. Microbiol. 71 (2005), 7139–7144.
31. Portnoy, V.A., Bezdan, D., Zengler, K., Adaptive laboratory evolution-harnessing the power of biology for metabolic engineering. Curr. Opin. Biotechnol. 22 (2011), 590–594.
32. Pulvermacher, S.C., Stauffer, L.T., Stauffer, G.V., Role of the sRNA GcvB in regulation of cycA in Escherichia coli. Microbiology 155 (2009), 106–114.
33. Pulvermacher, S.C., Stauffer, L.T., Stauffer, G.V., The small RNA GcvB regulates sstT mRNA expression in Escherichia coli. J. Bacteriol. 191 (2009), 238–248.
34. Reyes, L.H., Gomez, J.M., Kao, K.C., Improving carotenoids production in yeast via adaptive laboratory evolution. Metab. Eng. 21 (2014), 26–33.
35. Robbins, J.C., Oxender, D.L., Transport systems for alanine, serine, and glycine in Escherichia coli K-12. J. Bacteriol. 116 (1973), 12–18.
36. Ronda, C., Pedersen, L.E., Sommer, M.O., Nielsen, A.T., CRMAGE: CRISPR Optimized MAGE Recombineering. Sci. Rep., 6, 2016, 19452.
37. Sandberg, T.E., Pedersen, M., LaCroix, R.A., Ebrahim, A., Bonde, M., Herrgard, M.J., Palsson, B.O., Sommer, M., Feist, A.M., Evolution of Escherichia coli to 42 degrees C and subsequent genetic engineering reveals adaptive mechanisms and novel mutations. Mol. Biol. Evol. 31 (2014), 2647–2662.
38. Siddiquee, K.A., Arauzo-Bravo, M.J., Shimizu, K., Effect of a pyruvate kinase (pykF-gene) knockout mutation on the control of gene expression and metabolic fluxes in Escherichia coli. FEMS Microbiol. Lett. 235 (2004), 25–33.
39. St-Pierre, F., Cui, L., Priest, D.G., Endy, D., Dodd, I.B., Shearwin, K.E., One-step cloning and chromosomal integration of DNA. ACS Synth. Biol. 2 (2013), 537–541.
40. Stolz, M., Peters-Wendisch, P., Etterich, H., Gerharz, T., Faurie, R., Sahm, H., Fersterra, H., Eggeling, L., Reduced folate supply as a key to enhanced L-serine production by Corynebacterium glutamicum. Appl. Environ. Microbiol. 73 (2007), 750–755.
41. Sun, W., Wang, S., Curtiss, R. 3rd, Highly efficient method for introducing successive multiple scarless gene deletions and markerless gene insertions into the Yersinia pestis chromosome. Appl. Environ. Microbiol. 74 (2008), 4241–4245.
42. Tani, T.H., Khodursky, A., Blumenthal, R.M., Brown, P.O., Matthews, R.G., Adaptation to famine: a family of stationary-phase genes revealed by microarray analysis. Proc. Natl. Acad. Sci. USA 99 (2002), 13471–13476.
43. Thony, B., Hwang, D.S., Fradkin, L., Kornberg, A., iciA, an Escherichia coli gene encoding a specific inhibitor of chromosomal initiation of replication in vitro. Proc. Natl. Acad. Sci. USA 88 (1991), 4066–4070.
44. Wang, H.H., Church, G.M., Multiplexed genome engineering and genotyping methods applications for synthetic biology and metabolic engineering. Methods Enzymol. 498 (2011), 409–426.
45. Werpy, T., Petersen, G., 2004. Top Value Added Chemicals from Biomass: Results of Screening for Potential Candidates from Sugars and Synthesis Gas, vol. 1. pp. 1–76.
46. Yamada, S., Awano, N., Inubushi, K., Maeda, E., Nakamori, S., Nishino, K., Yamaguchi, A., Takagi, H., Effect of drug transporter genes on cysteine export and overproduction in Escherichia coli. Appl. Environ. Microbiol. 72 (2006), 4735–4742.
47. Zhang, X., El-Hajj, Z.W., Newman, E., Deficiency in L-serine deaminase interferes with one-carbon metabolism and cell wall synthesis in Escherichia coli K-12. J. Bacteriol. 192 (2010), 5515–5525.
48. Zhang, X., Newman, E., Deficiency in l-serine deaminase results in abnormal growth and cell division of Escherichia coli K-12. Mol. Microbiol. 69 (2008), 870–881.
49. Zhao, G., Winkler, M.E., A novel alpha-ketoglutarate reductase activity of the serA-encoded 3-phosphoglycerate dehydrogenase of Escherichia coli K-12 and its possible implications for human 2-hydroxyglutaric aciduria. J. Bacteriol. 178 (1996), 232–239.
50. Zhu, Q., Zhang, X., Luo, Y., Guo, W., Xu, G., Shi, J., Xu, Z., L-Serine overproduction with minimization of by-product synthesis by engineered Corynebacterium glutamicum. Appl. Microbiol. Biotechnol. 99 (2015), 1665–1673.