Improving heterologous polyketide production in Escherichia coli by transporter engineering

Applied Microbiology and Biotechnology

Volumn 99, Issue 20, 2015, Pages 8691-8700

  Yang, Jingya ^a   Xiong, Zhi Qiang ^b   Song, Shu Jie ^a,b   Wang, Jian Feng ^b   Lv, Hua Jun ^b   Wang, Yong ^b  

^a SHANGHAI OCEAN UNIVERSITY   (China)

^b INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

Efflux pump; Escherichia coli; Heterologous production; Polyketide erythromycin; Transcriptional regulator

Indexed keywords

ANTIBIOTICS; ESCHERICHIA COLI;

EFFLUX PUMPS; HETEROLOGOUS PRODUCTION; MICROBIAL CELL FACTORIES; MULTIDRUG EFFLUX PUMPS; POLYKETIDES; PRODUCTION STRAIN; SINGLE COMPONENTS; TRANSCRIPTIONAL REGULATOR;

KETONES;

APRAMYCIN; BACTERIAL PROTEIN; CARBENICILLIN; KANAMYCIN; MULTIDRUG RESISTANCE PROTEIN; POLYKETIDE; POLYKETIDE 6 DEOXYERYTHRONOLIDE B; UNCLASSIFIED DRUG; 6-DEOXYERYTHRONOLIDE B; CARRIER PROTEIN; ERYTHROMYCIN; RECOMBINANT PROTEIN;

BACTERIUM; BIOTECHNOLOGY; FECAL COLIFORM; GENE EXPRESSION; GENETIC ENGINEERING; PROTEIN; SECONDARY METABOLITE;

ARTICLE; ENGINEERING; ESCHERICHIA COLI; NONHUMAN; REGULATORY MECHANISM; TRANSCRIPTION REGULATION; ACTIVE TRANSPORT; ANALOGS AND DERIVATIVES; GENETICS; METABOLIC ENGINEERING; METABOLISM; PROCEDURES;

ESCHERICHIA COLI; LEPIDIUM MEYENII;

BIOLOGICAL TRANSPORT, ACTIVE; ERYTHROMYCIN; ESCHERICHIA COLI; MEMBRANE TRANSPORT PROTEINS; METABOLIC ENGINEERING; POLYKETIDES; RECOMBINANT PROTEINS;

EID: 84941994826     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6718-7     Document Type: Article

References (45)

1. Ajikumar PK, Xiao WH, Tyo KE, Wang Y, Simeon F, Leonard E, Mucha O, Phon TH, Pfeifer B, Stephanopoulos G (2010) Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli. Science 330(6000):70–74
2. Alper H, Moxley J, Nevoigt E, Fink GR, Stephanopoulos G (2006) Engineering yeast transcription machinery for improved ethanol tolerance and production. Science 314(5805):1565–1568
3. Ambudkar SV, Dey S, Hrycyna CA, Ramachandra M, Pastan I, Gottesman MM (1999) Biochemical, cellular, and pharmacological aspects of the multidrug transporter. Annu Rev Pharmacol Toxicol 39:361–398
4. Boghigian BA, Zhang H, Pfeifer BA (2011) Multi-factorial engineering of heterologous polyketide production in Escherichia coli reveals complex pathway interactions. Biotechnol Bioeng 108(6):1360–1371
5. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97(12):6640–6645
6. Dayem LC, Carney JR, Santi DV, Pfeifer BA, Khosla C, Kealey JT (2002) Metabolic engineering of a methylmalonyl-CoA mutase-epimerase pathway for complex polyketide biosynthesis in Escherichia coli. Biochemistry 41(16):5193–5201
7. Deeley RG, Cole SP (1997) Function, evolution and structure of multidrug resistance protein (MRP). Semin Cancer Biol 8(3):193–204
8. Doshi R, Nguyen T, Chang G (2013) Transporter-mediated biofuel secretion. Proc Natl Acad Sci U S A 110(19):7642–7647
9. Du D, Wang Z, James NR, Voss JE, Klimont E, Ohene-Agyei T, Venter H, Chiu W, Luisi BF (2014) Structure of the AcrAB-TolC multidrug efflux pump. Nature 509(7501):512–515
10. Dunlop MJ, Dossani ZY, Szmidt HL, Chu HC, Lee TS, Keasling JD, Hadi MZ, Mukhopadhyay A (2011) Engineering microbial biofuel tolerance and export using efflux pumps. Mol Syst Biol 7(1):487
11. Eguchi Y, Oshima T, Mori H, Aono R, Yamamoto K, Ishihama A, Utsumi R (2003) Transcriptional regulation of drug efflux genes by EvgAS, a two-component system in Escherichia coli. Microbiology 149(10):2819–2828
12. Fisher MA, Boyarskiy S, Yamada MR, Kong N, Bauer S, Tullman-Ercek D (2014) Enhancing tolerance to short-chain alcohols by engineering the Escherichia coli AcrB efflux pump to secrete the non-native substrate n-butanol. ACS Synth Biol 3(1):30–40
13. Grkovic S, Brown MH, Skurray RA (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66(4):671–701
14. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
15. Hirakawa H, Inazumi Y, Senda Y, Kobayashi A, Hirata T, Nishino K, Yamaguchi A (2006) N-acetyl-d-glucosamine induces the expression of multidrug exporter genes, mdtEF, via catabolite activation in Escherichia coli. J Bacteriol 188(16):5851–5858
16. Hirakawa H, Nishino K, Yamada J, Hirata T, Yamaguchi A (2003) Beta-lactam resistance modulated by the overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Antimicrob Chemother 52(4):576–582
17. 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
18. Keeney D, Ruzin A, McAleese F, Murphy E, Bradford PA (2008) MarA-mediated overexpression of the AcrAB efflux pump results in decreased susceptibility to tigecycline in Escherichia coli. J Antimicrob Chemother 61(1):46–53
19. Kinoshita K, Pfeifer BA, Khosla C, Cane DE (2003) Precursor-directed polyketide biosynthesis in Escherichia coli. Bioorg Med Chem Lett 13(21):3701–3704
20. Krummenacher P, Narberhaus F (2000) Two genes encoding a putative multidrug efflux pump of the RND/MFP family are cotranscribed with an rpoH gene in Bradyrhizobium japonicum. Gene 241(2):247–254
21. Li XZ, Nikaido H, Poole K (1995) Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother 39(9):1948–1953
22. Lu S, Zgurskaya HI (2012) Role of ATP binding and hydrolysis in assembly of MacAB-TolC macrolide transporter. Mol Microbiol 86(5):1132–1143
23. Mutka SC, Carney JR, Liu Y, Kennedy J (2006) Heterologous production of epothilone C and D in Escherichia coli. Biochemistry 45(4):1321–1330
24. Nishino K, Senda Y, Hayashi-Nishino M, Yamaguchi A (2009) Role of the AraC-XylS family regulator YdeO in multi-drug resistance of Escherichia coli. J Antibiot 62(5):251–257
25. Nonaka G, Blankschien M, Herman C, Gross CA, Rhodius VA (2006) Regulon and promoter analysis of the E. coli heat-shock factor, sigma32, reveals a multifaceted cellular response to heat stress. Genes Dev 20(13):1776–1789
26. Ongley SE, Bian X, Neilan BA, Muller R (2013) Recent advances in the heterologous expression of microbial natural product biosynthetic pathways. Nat Prod Rep 30(8):1121–1138
27. Ostash I, Rebets Y, Ostash B, Kobylyanskyy A, Myronovskyy M, Nakamura T, Walker S, Fedorenko V (2008) An ABC transporter encoding gene lndW confers resistance to landomycin E. Arch Microbiol 190(1):105–109
28. Paddon CJ, Westfall PJ, Pitera DJ, Benjamin K, Fisher K, McPhee D, Leavell MD, Tai A, Main A, Eng D, Polichuk DR, Teoh KH, Reed DW, Treynor T, Lenihan J, Fleck M, Bajad S, Dang G, Dengrove D, Diola D, Dorin G, Ellens KW, Fickes S, Galazzo J, Gaucher SP, Geistlinger T, Henry R, Hepp M, Horning T, Iqbal T, Jiang H, Kizer L, Lieu B, Melis D, Moss N, Regentin R, Secrest S, Tsuruta H, Vazquez R, Westblade LF, Xu L, Yu M, Zhang Y, Zhao L, Lievense J, Covello PS, Keasling JD, Reiling KK, Renninger NS, Newman JD (2013) High-level semi-synthetic production of the potent antimalarial artemisinin. Nature 496(7446):528–532
29. Papadopoulos CJ, Carson CF, Chang BJ, Riley TV (2008) Role of the MexAB-OprM efflux pump of Pseudomonas aeruginosa in tolerance to tea tree (Melaleuca alternifolia) oil and its monoterpene components terpinen-4-ol, 1,8-cineole, and alpha-terpineol. Appl Environ Microbiol 74(6):1932–1935
30. Pfeifer B, Hu Z, Licari P, Khosla C (2002) Process and metabolic strategies for improved production of Escherichia coli-derived 6-deoxyerythronolide B. Appl Environ Microbiol 68(7):3287–3292
31. Pfeifer BA, Admiraal SJ, Gramajo H, Cane DE, Khosla C (2001) Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 291(5509):1790–1792
32. Qiu J, Zhuo Y, Zhu D, Zhou X, Zhang L, Bai L, Deng Z (2011) Overexpression of the ABC transporter AvtAB increases avermectin production in Streptomyces avermitilis. Appl Microbiol Biotechnol 92(2):337–345
33. Salmon K, Hung SP, Mekjian K, Baldi P, Hatfield GW, Gunsalus RP (2003) Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J Biol Chem 278(32):29837–29855
34. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York
35. Shah AA, Wang C, Chung YR, Kim JY, Choi ES, Kim SW (2013) Enhancement of geraniol resistance of Escherichia coli by MarA overexpression. J Biosci Bioeng 115(3):253–258
36. Stevens DC, Conway KR, Pearce N, Villegas-Penaranda LR, Garza AG, Boddy CN (2013a) Alternative sigma factor over-expression enables heterologous expression of a type II polyketide biosynthetic pathway in Escherichia coli. PLoS One 8(5):e64858
37. Stevens DC, Hari TP, Boddy CN (2013b) The role of transcription in heterologous expression of polyketides in bacterial hosts. Nat Prod Rep 30(11):1391–1411
38. Tikhonova EB, Zgurskaya HI (2004) AcrA, AcrB, and TolC of Escherichia coli form a stable intermembrane multidrug efflux complex. J Biol Chem 279(31):32116–32124
39. Touze T, Eswaran J, Bokma E, Koronakis E, Hughes C, Koronakis V (2004) Interactions underlying assembly of the Escherichia coli AcrAB-TolC multidrug efflux system. Mol Microbiol 53(2):697–706
40. Wang JF, Xiong ZQ, Li SY, Wang Y (2013) Enhancing isoprenoid production through systematically assembling and modulating efflux pumps in Escherichia coli. Appl Microbiol Biotechnol 97(18):8057–8067
41. Yamanaka Y, Ishihama A, Yamamoto K (2012) Induction of YdeO, a regulator for acid resistance genes, by ultraviolet irradiation in Escherichia coli. Biosci Biotechnol Biochem 76(6):1236–1238
42. You C, Zhang XZ, Zhang YH (2012) Simple cloning via direct transformation of PCR product (DNA multimer) to Escherichia coli and Bacillus subtilis. Appl Environ Microbiol 78(5):1593–1595
43. Zakeri B, Lu TK (2013) Synthetic biology of antimicrobial discovery. ACS Synth Biol 2(7):358–372
44. Zhang H, Boghigian BA, Pfeifer BA (2010) Investigating the role of native propionyl-CoA and methylmalonyl-CoA metabolism on heterologous polyketide production in Escherichia coli. Biotechnol Bioeng 105(3):567–573
45. Zhao K, Liu M, Burgess RR (2005) The global transcriptional response of Escherichia coli to induced sigma 32 protein involves sigma 32 regulon activation followed by inactivation and degradation of sigma 32 in vivo. J Biol Chem 280(18):17758–17768