Systematic comparison of co-expression of multiple recombinant thermophilic enzymes in Escherichia coli BL21(DE3)

Applied Microbiology and Biotechnology

Volumn 101, Issue 11, 2017, Pages 4481-4493

  Chen, Hui ^a   Huang, Rui ^a   Zhang, Y H Percival ^a,b  

^a Virginia Polytechnic Institute and State University   (United States)

^b Tianjin Airport Economic Area   (China)

Author keywords

Cascade biocatalysis; Co expression; E. coli BL21(DE3); Expression control; T7 terminator

Indexed keywords

BIOCATALYSTS; BIOSYNTHESIS; CATALYSIS; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GENES; GLUCOSE; METABOLIC ENGINEERING; SUGAR SUBSTITUTES;

BIOCATALYSIS; CO-EXPRESSION; E. COLI BL21(DE3); EXPRESSION CONTROLS; T7 TERMINATOR;

ENZYMES;

ALPHA GLUCAN PHOSPHORYLASE; BACTERIAL ENZYME; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; MALTODEXTRIN; PHOSPHOGLUCOMUTASE; PHOSPHOGLUCONATE DEHYDROGENASE; PHOSPHORYLASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG; XYLITOL; XYLOSE; ENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; POLYSACCHARIDE; RECOMBINANT PROTEIN;

BIOTECHNOLOGY; COLIFORM BACTERIUM; COMPARATIVE STUDY; ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR ANALYSIS; PLASMID; PROTEIN; THERMOPHILIC BACTERIUM;

ARTICLE; COENZYME; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION; GEOBACILLUS STEAROTHERMOPHILUS; MORELLA; MORELLA THERMOACETICA; NONHUMAN; PLASMID; PROMOTER REGION; PROTEIN EXPRESSION; THERMOCOCCUS KODAKARENSIS; THERMOTOGA MARITIMA; BIOCATALYSIS; COMPARATIVE STUDY; ENZYMOLOGY; GENETICS; METABOLIC ENGINEERING; METABOLISM; REGULATOR GENE;

ESCHERICHIA COLI;

BIOCATALYSIS; ENZYMES; ESCHERICHIA COLI; GENE EXPRESSION; GLUCOSEPHOSPHATE DEHYDROGENASE; METABOLIC ENGINEERING; NADP; PHOSPHOGLUCOMUTASE; PHOSPHOGLUCONATE DEHYDROGENASE; PHOSPHORYLASES; PLASMIDS; POLYSACCHARIDES; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS; TERMINATOR REGIONS, GENETIC; XYLOSE;

EID: 85014090750     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-017-8206-8     Document Type: Article

References (50)

1. Alexandrov A, Vignali M, LaCount DJ, Quartley E, de Vries C, De Rosa D, Babulski J, Mitchell SF, Schoenfeld LW, Fields S (2004) A facile method for high-throughput co-expression of protein pairs. Mol Cell Proteomics 3(9):934–938. doi:10.1074/mcp.T400008-MCP200
2. Burda E, Hummel W, Gröger H (2008) Modular chemoenzymatic one-pot syntheses in aqueous media: combination of a palladium-catalyzed cross-coupling with an asymmetric biotransformation. Angew Chem Int Ed 47(49):9551–9554. doi:10.1002/anie.200801341
3. Chandrayan SK, Wu C-H, McTernan PM, Adams MW (2015) High yield purification of a tagged cytoplasmic [NiFe]-hydrogenase and a catalytically-active nickel-free intermediate form. Protein Expr Purif 107:90–94. doi:10.1016/j.pep.2014.10.018
4. Curran KA, Karim AS, Gupta A, Alper HS (2013) Use of expression-enhancing terminators in Saccharomyces cerevisiae to increase mRNA half-life and improve gene expression control for metabolic engineering applications. Metab Eng 19:88–97. doi:10.1016/j.ymben.2013.07.001
5. Fernández-Lucas J (2015) Multienzymatic synthesis of nucleic acid derivatives: a general perspective. Appl Microbiol Biotechnol 99(11):4615–4627. doi:10.1007/s00253-015-6642-x
6. Fisch KM (2013) Biosynthesis of natural products by microbial iterative hybrid PKS–NRPS. RSC Adv 3(40):18228–18247. doi:10.1039/C3RA42661K
7. Glanemann C, Loos A, Gorret N, Willis L, O’Brien X, Lessard P, Sinskey A (2003) Disparity between changes in mRNA abundance and enzyme activity in Corynebacterium glutamicum: implications for DNA microarray analysis. Appl Microbiol Biotechnol 61(1):61–68 doi:10.1007/s00253-002-1191-5
8. Higgins MK, Demir M, Tate CG (2003) Calnexin co-expression and the use of weaker promoters increase the expression of correctly assembled shaker potassium channel in insect cells. Biochim Biophys Acta Biomem 1610(1):124–132. doi:10.1016/S0005-2736(02)00715-0
9. Jiang W, Fang B (2016) Construction of a tunable multi-enzyme-coordinate expression system for biosynthesis of chiral drug intermediates. Sci Rep 6:30462. doi:10.1038/srep30462
10. Johnston K, Clements A, Venkataramani RN, Trievel RC, Marmorstein R (2000) Coexpression of proteins in bacteria using T7-based expression plasmids: expression of heteromeric cell-cycle and transcriptional regulatory complexes. Protein Expr Purif 20(3):435–443. doi:10.1006/prep.2000.1313
11. Jones KL, Kim S-W, Keasling J (2000) Low-copy plasmids can perform as well as or better than high-copy plasmids for metabolic engineering of bacteria. Metab Eng 2(4):328–338. doi:10.1006/mben.2000.0161
12. Kealey JT, Liu L, Santi DV, Betlach MC, Barr PJ (1998) Production of a polyketide natural product in nonpolyketide-producing prokaryotic and eukaryotic hosts. Proc Natl Acad Sci U S A 95(2):505–509. doi:10.1006/prep.2000.1313
13. Kim KJ, Kim HE, Lee KH, Han W, Yi MJ, Jeong J, Oh BH (2004) Two-promoter vector is highly efficient for overproduction of protein complexes. Protein Sci 13(6):1698–1703. doi:10.1110/ps.04644504
14. Kim S, Lee SB (2006) Rare codon clusters at 5′-end influence heterologous expression of archaeal gene in Escherichia coli. Protein Expr Purif 50(1):49–57. doi:10.1016/j.pep.2006.07.014
15. Lopez-Gallego F, Schmidt-Dannert C (2010) Multi-enzymatic synthesis. Curr Opin Chem Biol 14(2):174–183. doi:10.1016/j.cbpa.2009.11.023
16. Lu W, Ye L, Xu H, Xie W, Gu J, Yu H (2014) Enhanced production of coenzyme Q10 by self-regulating the engineered MEP pathway in Rhodobacter sphaeroides. Biotechnol Bioeng 111(4):761–769. doi:10.1002/bit.25130
17. Lv X, Xu H, Yu H (2013) Significantly enhanced production of isoprene by ordered coexpression of genes dxs, dxr, and idi in Escherichia coli. Appl Microbiol Biotechnol 97(6):2357–2365. doi:10.1007/s00253-012-4485-2
18. Makrides SC (1996) Strategies for achieving high-level expression of genes in Escherichia coli. Microbiol Mol Biol Rev 60(3):512–538
19. Mantis J, Tague BW (2000) Comparing the utility of β-glucuronidase and green fluorescent protein for detection of weak promoter activity in Arabidopsis thaliana. Plant Mol Biol Rep 18(4):319–330. doi:10.1007/BF02825059
20. Myung S, Rollin J, You C, Sun F, Chandrayan S, Adams MW, Zhang Y-HP (2014) In vitro metabolic engineering of hydrogen production at theoretical yield from sucrose. Metab Eng 24:70–77. doi:10.1016/j.ymben.2014.05.006
21. Naoumkina MA, Modolo LV, Huhman DV, Urbanczyk-Wochniak E, Tang Y, Sumner LW, Dixon RA (2010) Genomic and coexpression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell 22(3):850–866. doi:10.1105/tpc.109.073270
22. Neumann D, Woods A, Carling D, Wallimann T, Schlattner U (2003) Mammalian AMP-activated protein kinase: functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli. Protein Expr Purif 30(2):230–237. doi:10.1016/S1046-5928(03)00126-8
23. Ninh PH, Honda K, Sakai T, Okano K, Ohtake H (2015) Assembly and multiple gene expression of thermophilic enzymes in Escherichia coli for in vitro metabolic engineering. Biotechnol Bioeng 112(1):189–196. doi:10.1002/bit.25338
24. Nogueira T, Springer M (2000) Post-transcriptional control by global regulators of gene expression in bacteria. Curr Opin Microbiol 3(2):154–158. doi:10.1016/S1369-5274(00)00068-0
25. Opgenorth PH, Korman TP, Bowie JU (2016) A synthetic biochemistry module for production of bio-based chemicals from glucose. Nat Chem Biol:393–395 doi: 10.1038/nchembio.2062
26. Otte KB, Kittelberger J, Kirtz M, Nestl BM, Hauer B (2014) Whole-cell one-pot biosynthesis of azelaic acid. ChemCatChem 6(4):1003–1009. doi:10.1002/cctc.201300787
27. Rollin JA, Tam TK, Zhang Y-HP (2013) New biotechnology paradigm: cell-free biosystems for biomanufacturing. Green Chem 15(7):1708–1719. doi:10.1039/C3GC40625C
28. Romier C, Ben Jelloul M, Albeck S, Buchwald G, Busso D, Celie PH, Christodoulou E, De Marco V, Van Gerwen S, Knipscheer P (2006) Co-expression of protein complexes in prokaryotic and eukaryotic hosts: experimental procedures, database tracking and case studies. Acta Crystallogr, Sect D: Biol Crystallogr 62(10):1232–1242. doi:10.1107/S0907444906031003
29. Salis HM, Mirsky EA, Voigt CA (2009) Automated design of synthetic ribosome binding sites to control protein expression. Nat Biotechnol 27(10):946–950. doi:10.1038/nbt.1568
30. Santacoloma PA, Gr S, Gernaey KV, Woodley JM (2010) Multienzyme-catalyzed processes: next-generation biocatalysis. Org Proc Res Dev 15(1):203–212. doi:10.1021/op1002159
31. Sørensen HP, Mortensen KK (2005) Advanced genetic strategies for recombinant protein expression in Escherichia coli. J Biotechnol 115(2):113–128. doi:10.1016/j.jbiotec.2004.08.004
32. Sun J, Hopkins RC, Jenney FE Jr, McTernan PM, Adams MW (2010) Heterologous expression and maturation of an NADP-dependent [NiFe]-hydrogenase: a key enzyme in biofuel production. PLoS One 5(5):e10526. doi:10.1371/journal.pone.0010526
33. Tan S (2001) A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr Purif 21(1):224–234. doi:10.1006/prep.2000.1363
34. Taniguchi Y, Choi PJ, Li G-W, Chen H, Babu M, Hearn J, Emili A, Xie XS (2010) Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329(5991):533–538. doi:10.1126/science.1188308
35. Tolia NH, Joshua-Tor L (2006) Strategies for protein coexpression in Escherichia coli. Nat Meth 3(1):55–64. doi:10.1038/nmeth0106-55
36. Vind J, Sørensen MA, Rasmussen MD, Pedersen S (1993) Synthesis of proteins in Escherichia coli is limited by the concentration of free ribosomes: expression from reporter genes does not always reflect functional mRNA levels. J Mol Biol 231(3):678–688. doi:10.1006/jmbi.1993.1319
37. Wakagi T, Oshima T, Imamura H, Matsuzawa H (1998) Cloning of the gene for inorganic pyrophosphatase from a thermoacidophilic archaeon, Sulfolobus sp. strain 7, and overproduction of the enzyme by coexpression of tRNA for arginine rare codon. Biosci Biotechnol Biochem 62(12):2408–2414. doi:10.1271/bbb.62.2408
38. Wang Y, Huang W, Sathitsuksanoh N, Zhu Z, Zhang Y-HP (2011) Biohydrogenation from biomass sugar mediated by in vitro synthetic enzymatic pathways. Chem Biol 18(3):372–380. doi:10.1016/j.chembiol.2010.12.019
39. Wenzel SC, Gross F, Zhang Y, Fu J, Stewart AF, Müller R (2005) Heterologous expression of a myxobacterial natural products assembly line in Pseudomonads via red/ET recombineering. Chem Biol 12(3):349–356. doi:10.1016/j.chembiol.2004.12.012
40. Woodyer R, Simurdiak M, van der Donk WA, Zhao H (2005) Heterologous expression, purification, and characterization of a highly active xylose reductase from Neurospora crassa. Appl Environ Microbiol 71(3):1642–1647. doi:10.1128/AEM.71.3.1642-1647.2005
41. Wu S, Chen Y, Xu Y, Li A, Xu Q, Glieder A, Li Z (2014) Enantioselective trans-dihydroxylation of aryl olefins by cascade biocatalysis with recombinant Escherichia coli coexpressing monooxygenase and epoxide hydrolase. ACS Catal 4(2):409–420. doi:10.1021/cs400992z
42. You C, Zhang X-Z, Zhang Y-HP (2012) Simple cloning via direct transformation of PCR product (DNA multimer) to Escherichia coli and Bacillus subtilis. Appl Environ Microbiol 78(5):1593–1595. doi:10.1128/AEM.07105-11
43. Zha W, Rubin-Pitel SB, Shao Z, Zhao H (2009) Improving cellular malonyl-CoA level in Escherichia coli via metabolic engineering. Metab Eng 11(3):192–198. doi:10.1016/j.ymben.2009.01.005
44. Zhang Y-HP (2015) Production of biofuels and biochemicals by in vitro synthetic biosystems: opportunities and challenges. Biotechnol Adv 33(7):1467–1483. doi:10.1016/j.biotechadv.2014.10.009
45. Zhang Y-HP, Lynd LR (2005) Regulation of cellulase synthesis in batch and continuous cultures of Clostridium thermocellum. J Bacteriol 187(1):99–106. doi:10.1128/JB.187.1.99-106.2005
46. Zhong C, Wei P, Zhang Y-HP (2016) Enhancing functional expression of codon-optimized heterologous enzymes in Escherichia coli BL21(DE3) by selective introduction of synonymous rare codons. Biotechnol Bioeng. doi:10.1002/bit.26238
47. Zhou W, You C, Ma H, Ma Y, Zhang Y-HP (2016) One-pot biosynthesis of high-concentration α-glucose 1-phosphate from starch by sequential addition of three hyperthermophilic enzymes. J Agr Food Chem 64:1777–1783. doi:10.1021/acs.jafc.5b05648
48. Zhu Y, Li H, Liu P, Yang J, Zhang X, Sun Y (2015) Construction of allitol synthesis pathway by multi-enzyme coexpression in Escherichia coli and its application in allitol production. J Ind Microbiol Biotechnol 42(5):661–669. doi:10.1007/s10295-014-1578-1
49. Zhu Z, Sun F, Zhang X, Zhang Y-HP (2012) Deep oxidation of glucose in enzymatic fuel cells through a synthetic enzymatic pathway containing a cascade of two thermostable dehydrogenase. Biosens Bioelectron 36(1):110–115. doi:10.1016/j.bios.2012.04.001
50. Zhu Z, Tam TK, Sun F, You C, Zhang Y-HP (2014) A high-energy-density sugar biobattery based on a synthetic enzymatic pathway. Nat Commun 5:3026. doi:10.1038/ncomms4026