Expression of heterologous non-oxidative pentose phosphate pathway from Bacillus methanolicus and phosphoglucose isomerase deletion improves methanol assimilation and metabolite production by a synthetic Escherichia coli methylotroph

Metabolic Engineering

Volumn 45, Issue , 2018, Pages 75-85

  Bennett, R Kyle ^a   Gonzalez, Jacqueline E ^a   Whitaker, W Brian ^a   Antoniewicz, Maciek R ^a   Papoutsakis, Eleftherios T ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

Escherichia coli; Methanol; Pentose phosphate pathway; Phosphoglucose isomerase; Synthetic methylotrophy

Indexed keywords

ACETONE; BACTERIOLOGY; ESCHERICHIA COLI; GLUCOSE; METABOLITES;

BACILLUS METHANOLICUS; FED-BATCH FERMENTATION; INTRACELLULAR METABOLITES; METABOLITE PRODUCTION; METHANOL UTILIZATION; PENTOSE PHOSPHATE PATHWAY; PHOSPHOGLUCOSE ISOMERASE; SYNTHETIC METHYLOTROPHY;

METHANOL;

ACETONE; CARBON; CARBON 13; GLUCOSE; GLUCOSE 6 PHOSPHATE ISOMERASE; METHANOL; SYNTHETIC DNA; ESCHERICHIA COLI PROTEIN; PGI PROTEIN, E COLI;

ARTICLE; BACILLUS; BACILLUS METHANOLICUS; BACTERIAL GROWTH; BACTERIAL STRAIN; CARBON METABOLISM; CELL METABOLISM; CONTROLLED STUDY; ESCHERICHIA COLI; FED BATCH CULTURE; FED BATCH FERMENTATION; GENE DELETION; GLYCOLYSIS; HETEROLOGOUS EXPRESSION; ISOTOPE LABELING; METABOLIC ENGINEERING; METABOLITE; METHYLOTROPHIC BACTERIUM; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PRIORITY JOURNAL; SYNTHETIC BIOLOGY; ENZYMOLOGY; GENE EXPRESSION; GENETICS; METABOLISM; TRANSGENIC MICROORGANISM;

BACILLUS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; GLUCOSE-6-PHOSPHATE ISOMERASE; METHANOL; MICROORGANISMS, GENETICALLY-MODIFIED; PENTOSE PHOSPHATE PATHWAY;

EID: 85036654608     PISSN: 10967176     EISSN: 10967184     Source Type: Journal    
DOI: 10.1016/j.ymben.2017.11.016     Document Type: Article

References (56)

1. Antoniewicz, M.R., Parallel labeling experiments for pathway elucidation and (13)C metabolic flux analysis. Curr. Opin. Biotechnol. 36 (2015), 91–97.
2. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Determination of confidence intervals of metabolic fluxes estimated from stable isotope measurements. Metab. Eng. 8 (2006), 324–337.
3. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Elementary metabolite units (EMU): a novel framework for modeling isotopic distributions. Metab. Eng. 9 (2007), 68–86.
4. Antoniewicz, M.R., Kelleher, J.K., Stephanopoulos, G., Measuring deuterium enrichment of glucose hydrogen atoms by gas chromatography/mass spectrometry. Anal. Chem. 83 (2011), 3211–3216.
5. Antoniewicz, M.R., Kraynie, D.F., Laffend, L.A., Gonzalez-Lergier, J., Kelleher, J.K., Stephanopoulos, G., Metabolic flux analysis in a nonstationary system: fed-batch fermentation of a high yielding strain of E. coli producing 1,3-propanediol. Metab. Eng. 9 (2007), 277–292.
6. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L., Mori, H., Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol., 2, 2006 (2006 0008).
7. Basan, M., Hui, S., Okano, H., Zhang, Z., Shen, Y., Williamson, J.R., Hwa, T., Overflow metabolism in Escherichia coli results from efficient proteome allocation. Nature 528 (2015), 99–104.
8. Bermejo, L.L., Welker, N.E., Papoutsakis, E.T., Expression of Clostridium acetobutylicum ATCC 824 genes in Escherichia coli for acetone production and acetate detoxification. Appl. Environ. Microbiol. 64 (1998), 1079–1085.
9. Borujeni, A.E., Channarasappa, A.S., Salis, H.M., Translation rate is controlled by coupled trade-offs between site accessibility, selective RNA unfolding and sliding at upstream standby sites. Nucleic Acids Res. 42 (2014), 2646–2659.
10. Brautaset, T., Jakobsen, M.O., Flickinger, M.C., Valla, S., Ellingsen, T.E., Plasmid-dependent methylotrophy in thermotolerant Bacillus methanolicus. J. Bacteriol. 186 (2004), 1229–1238.
11. Charusanti, P., Conrad, T.M., Knight, E.M., Venkataraman, K., Fong, N.L., Xie, B., Gao, Y., Palsson, B.O., Genetic basis of growth adaptation of Escherichia coli after deletion of pgi, a major metabolic gene. PLoS Genet., 6, 2010, e1001186.
12. Chu, I.M., Papoutsakis, E.T., Growth dynamics of a methylotroph (Methylomonas L3) in continuous cultures. I. Fast transients induced by methanol pulses and methanol accumulation. Biotechnol. Bioeng. 29 (1987), 55–64.
13. Crown, S.B., Long, C.P., Antoniewicz, M.R., Integrated 13C-metabolic flux analysis of 14 parallel labeling experiments in Escherichia coli. Metab. Eng. 28 (2015), 151–158.
14. Crown, S.B., Long, C.P., Antoniewicz, M.R., Optimal tracers for parallel labeling experiments and 13C metabolic flux analysis: a new precision and synergy scoring system. Metab. Eng. 38 (2016), 10–18.
15. Dai, Z., Gu, H., Zhang, S., Xin, F., Zhang, W., Dong, W., Ma, J., Jia, H., Jiang, M., Metabolic construction strategies for direct methanol utilization in Saccharomyces cerevisiae. Bioresour. Technol., 2017.
16. Datsenko, K.A., Wanner, B.L., One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97 (2000), 6640–6645.
17. Dehio, C., Meyer, M., Maintenance of broad-host-range incompatibility group P and group Q plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli. J. Bacteriol. 179 (1997), 538–540.
18. Englaender, J.A., Jones, J.A., Cress, B.F., Kuhlman, T.E., Linhardt, R.J., Koffas, M.A.G., Effect of genomic integration location on heterologous protein expression and metabolic engineering in E. coli. ACS Synth. Biol. 6 (2017), 710–720.
19. Fernandez, C.A., Des Rosiers, C., Previs, S.F., David, F., Brunengraber, H., Correction of 13C mass isotopomer distributions for natural stable isotope abundance. J. Mass Spectrom. 31 (1996), 255–262.
20. Galisa, P.S., da Silva, H.A.P., Macedo, A.V.M., Reis, V.M., Vidal, M.S., Baldani, J.I., Simoes-Araujo, J.L., Identification and validation of reference genes to study the gene expression in Gluconacetobacter diazotrophicus grown in different carbon sources using RT-qPCR. J. Microbiol. Methods 91 (2012), 1–7.
21. Gonzalez, C.F., Proudfoot, M., Brown, G., Korniyenko, Y., Mori, H., Savchenko, A.V., Yakunin, A.F., Molecular basis of formaldehyde detoxification. Characterization of two S-formylglutathione hydrolases from Escherichia coli, FrmB and YeiG. J. Biol. Chem. 281 (2006), 14514–14522.
22. Gonzalez, J.E., Antoniewicz, M.R., Tracing metabolism from lignocellulosic biomass and gaseous substrates to products with stable-isotopes. Curr. Opin. Biotechnol. 43 (2017), 86–95.
23. Gonzalez, J.E., Long, C.P., Antoniewicz, M.R., Comprehensive analysis of glucose and xylose metabolism in Escherichia coli under aerobic and anaerobic conditions by 13C metabolic flux analysis. Metab. Eng. 39 (2017), 9–18.
24. Haynes, C.A., Gonzalez, R., Rethinking biological activation of methane and conversion to liquid fuels. Nat. Chem. Biol. 10 (2014), 331–339.
25. Hirt, W., Papoutsakis, E., Krug, E., Lim, H.C., Tsao, G.T., Formaldehyde incorporation by a new methylotroph (L3). Appl. Environ. Microbiol. 36 (1978), 56–62.
26. Hua, Q., Yang, C., Baba, T., Mori, H., Shimizu, K., Responses of the central metabolism in Escherichia coli to phosphoglucose isomerase and glucose-6-phosphate dehydrogenase knockouts. J. Bacteriol. 185 (2003), 7053–7067.
27. Jakobsen, O.M., Benichou, A., Flickinger, M.C., Valla, S., Ellingsen, T.E., Brautaset, T., Upregulated transcription of plasmid and chromosomal ribulose monophosphate pathway genes is critical for methanol assimilation rate and methanol tolerance in the methylotrophic bacterium Bacillus methanolicus. J. Bacteriol. 188 (2006), 3063–3072.
28. Kataoka, N., Vangnai, A.S., Pongtharangkul, T., Tajima, T., Yakushi, T., Matsushita, K., Kato, J., Construction of CoA-dependent 1-butanol synthetic pathway functions under aerobic conditions in Escherichia coli. J. Biotechnol. 204 (2015), 25–32.
29. Leighty, R.W., Antoniewicz, M.R., Parallel labeling experiments with [U-13C]glucose validate E. coli metabolic network model for 13C metabolic flux analysis. Metab. Eng. 14 (2012), 533–541.
30. Lessmeier, L., Pfeifenschneider, J., Carnicer, M., Heux, S., Portais, J.C., Wendisch, V.F., Production of carbon-13-labeled cadaverine by engineered Corynebacterium glutamicum using carbon-13-labeled methanol as co-substrate. Appl. Microbiol. Biotechnol. 99 (2015), 10163–10176.
31. Long, C.P., Antoniewicz, M.R., Quantifying biomass composition by gas chromatography/mass spectrometry. Anal. Chem. 86 (2014), 9423–9427.
32. Long, C.P., Au, J., Gonzalez, J.E., Antoniewicz, M.R., 13C metabolic flux analysis of microbial and mammalian systems is enhanced with GC-MS measurements of glycogen and RNA labeling. Metab. Eng. 38 (2016), 65–72.
33. Long, C.P., Gonzalez, J.E., Sandoval, N.R., Antoniewicz, M.R., Characterization of physiological responses to 22 gene knockouts in Escherichia coli central carbon metabolism. Metab. Eng. 37 (2016), 102–113.
34. May, A., Fischer, R.J., Maria Thum, S., Schaffer, S., Verseck, S., Durre, P., Bahl, H., A modified pathway for the production of acetone in Escherichia coli. Metab. Eng. 15 (2013), 218–225.
35. McConnell, B.O., Antoniewicz, M.R., Measuring the composition and stable-isotope labeling of algal biomass carbohydrates via gas chromatography/mass spectrometry. Anal. Chem. 88 (2016), 4624–4628.
36. Mermelstein, L.D., Papoutsakis, E.T., Petersen, D.J., Bennett, G.N., Metabolic engineering of Clostridium acetobutylicum ATCC 824 for increased solvent production by enhancement of acetone formation enzyme activities using a synthetic acetone operon. Biotechnol. Bioeng. 42 (1993), 1053–1060.
37. Muller, J.E., Meyer, F., Litsanov, B., Kiefer, P., Potthoff, E., Heux, S., Quax, W.J., Wendisch, V.F., Brautaset, T., Portais, J.C., Vorholt, J.A., Engineering Escherichia coli for methanol conversion. Metab. Eng. 28 (2015), 190–201.
38. Philippe, N., Alcaraz, J.P., Coursange, E., Geiselmann, J., Schneider, D., Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51 (2004), 246–255.
39. Ritz, M., Garenaux, A., Berge, M., Federighi, M., Determination of rpoA as the most suitable internal control to study stress response in C-jejuni by RT-qPCR and application to oxidative stress. J. Microbiol. Methods 76 (2009), 196–200.
40. Rohlhill, J., Sandoval, N.R., Papoutsakis, E.T., Sort-seq approach to engineering a formaldehyde-inducible promoter for dynamically regulated escherichia coli growth on methanol. ACS Synth. Biol., 2017.
41. Salis, H.M., Mirsky, E.A., Voigt, C.A., Automated design of synthetic ribosome binding sites to control protein expression. Nat. Biotechnol. 27 (2009), 946–950.
42. Sheehan, M.C., Bailey, C.J., Dowds, B.C.A., Mcconnell, D.J., A new alcohol-dehydrogenase, reactive towards methanol, from Bacillus-Stearothermophilus. Biochem. J. 252 (1988), 661–666.
43. Toya, Y., Ishii, N., Nakahigashi, K., Hirasawa, T., Soga, T., Tomita, M., Shimizu, K., 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 (2010), 975–992.
44. Usui, Y., Hirasawa, T., Furusawa, C., Shirai, T., Yamamoto, N., Mori, H., Shimizu, H., Investigating the effects of perturbations to pgi and eno gene expression on central carbon metabolism in Escherichia coli using (13)C metabolic flux analysis. Microb. Cell Fact., 11, 2012, 87.
45. Valgepea, K., Adamberg, K., Nahku, R., Lahtvee, P.J., Arike, L., Vilu, R., Systems biology approach reveals that overflow metabolism of acetate in Escherichia coli is triggered by carbon catabolite repression of acetyl-CoA synthetase. BMC Syst. Biol., 4, 2010, 166.
46. Vemuri, G.N., Altman, E., Sangurdekar, D.P., Khodursky, A.B., Eiteman, M.A., Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio. Appl. Environ. Microbiol. 72 (2006), 3653–3661.
47. Vogl, T., Sturmberger, L., Kickenweiz, T., Wasmayer, R., Schmid, C., Hatzl, A.M., Gerstmann, M.A., Pitzer, J., Wagner, M., Thallinger, G.G., Geier, M., Glieder, A., A toolbox of diverse promoters related to methanol utilization: functionally verified parts for heterologous pathway expression in Pichia pastoris. ACS Synth. Biol. 5 (2016), 172–186.
48. Whitaker, W.B., Jones, J.A., Bennett, R.K., Gonzalez, J.E., Vernacchio, V.R., Collins, S.M., Palmer, M.A., Schmidt, S., Antoniewicz, M.R., Koffas, M.A., Papoutsakis, E.T., Engineering the biological conversion of methanol to specialty chemicals in Escherichia coli. Metab. Eng. 39 (2017), 49–59.
49. Whitaker, W.B., Sandoval, N.R., Bennett, R.K., Fast, A.G., Papoutsakis, E.T., Synthetic methylotrophy: engineering the production of biofuels and chemicals based on the biology of aerobic methanol utilization. Curr. Opin. Biotechnol. 33 (2015), 165–175.
50. Witthoff, S., Schmitz, K., Niedenfuhr, S., Noh, K., Noack, S., Bott, M., Marienhagen, J., Metabolic engineering of Corynebacterium glutamicum for methanol metabolism. Appl. Environ. Microbiol. 81 (2015), 2215–2225.
51. Wu, G., Yan, Q., Jones, J.A., Tang, Y.J., Fong, S.S., Koffas, M.A., Metabolic burden: cornerstones in synthetic biology and metabolic engineering applications. Trends Biotechnol. 34 (2016), 652–664.
52. Wu, T.Y., Chen, C.T., Liu, J.T., Bogorad, I.W., Damoiseaux, R., Liao, J.C., Characterization and evolution of an activator-independent methanol dehydrogenase from Cupriavidus necator N-1. Appl. Microbiol. Biotechnol. 100 (2016), 4969–4983.
53. Xu, P., Vansiri, A., Bhan, N., Koffas, M.A., ePathBrick: a synthetic biology platform for engineering metabolic pathways in E. coli. ACS Synth. Biol. 1 (2012), 256–266.
54. Yoo, H., Antoniewicz, M.R., Stephanopoulos, G., Kelleher, J.K., Quantifying reductive carboxylation flux of glutamine to lipid in a brown adipocyte cell line. J. Biol. Chem. 283 (2008), 20621–20627.
55. Zhang, M., Lidstrom, M.E., Promoters and transcripts for genes involved in methanol oxidation in Methylobacterium extorquens AM 1. Microbiology 149 (2003), 1033–1040.
56. Zhou, K., Zhou, L., Lim, Q., Zou, R., Stephanopoulos, G., Too, H.P., Novel reference genes for quantifying transcriptional responses of Escherichia coli to protein overexpression by quantitative PCR. BMC Mol. Biol., 12, 2011, 18.