Multiplexed integrating plasmids for engineering of the erythromycin gene cluster for expression in Streptomyces spp. and combinatorial biosynthesis

Applied and Environmental Microbiology

Volumn 81, Issue 24, 2015, Pages 8402-8413

  Fayed, Bahgat ^a,b   Ashford, David A ^a   Hashem, Amal M ^b   Amin, Magdy A ^c   El Gazayerly, Omaima N ^c   Gregory, Matthew A ^d   Smith, Margaret C M ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

^b NATIONAL RESEARCH CENTRE   (Egypt)

^c CAIRO UNIVERSITY   (Egypt)

^d Isomerase Therapeutics Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; GENES; KETONES; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLITES; MULTIPLEXING;

ANTIBIOTIC ACTIVITY; COMBINATORIAL BIOSYNTHESIS; ENGINEERING EXPRESSION; GENOME SEQUENCING; LIQUID CHROMATOGRAPHY - MASS SPECTROMETRIES; POLYKETIDE SYNTHASE GENES; POLYKETIDE SYNTHASES; SECONDARY METABOLITES;

GENE EXPRESSION;

ANTIMICROBIAL ACTIVITY; BACTERIUM; GENE EXPRESSION; GENETIC ENGINEERING; METABOLITE; PLASMID;

STREPTOMYCES;

6-DEOXYERYTHRONOLIDE B; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; ERYTHROMYCIN; ERYTHRONOLIDE B; MULTIENZYME COMPLEX;

ANALOGS AND DERIVATIVES; BIOSYNTHESIS; GENETIC ENGINEERING; GENETICS; GLYCOSYLATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; MULTIGENE FAMILY; PLASMID; STREPTOMYCES;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; ERYTHROMYCIN; GENETIC ENGINEERING; GLYCOSYLATION; MASS SPECTROMETRY; MULTIENZYME COMPLEXES; MULTIGENE FAMILY; PLASMIDS; STREPTOMYCES;

EID: 84949643508     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02403-15     Document Type: Article

References (45)

1. Brotz-Oesterhelt H, Sass P. 2010. Postgenomic strategies in antibacterial drug discovery. Future Microbiol 5:1553-1579. http://dx.doi.org/10.2217/fmb.10.119.
2. Monciardini P, Iorio M, Maffioli S, Sosio M, Donadio S. 2014. Discovering new bioactive molecules from microbial sources. Microb Biotechnol 7:209-220. http://dx.doi.org/10.1111/1751-7915.12123.
3. Medema MH, Breitling R, Bovenberg R, Takano E. 2011. Exploiting plug-and-play synthetic biology for drug discovery and production in microorganisms. Nat Rev Microbiol 9:131-137. http://dx.doi.org/10.1038/nrmicro2478.
4. Ongley SE, Bian X, Neilan BA, Muller R. 2013. Recent advances in the heterologous expression of microbial natural product biosynthetic pathways. Nat Prod Rep 30:1121-1138. http://dx.doi.org/10.1039/c3np70034h.
5. Yamanaka K, Reynolds KA, Kersten RD, Ryan KS, Gonzalez DJ, Nizet V, Dorrestein PC, Moore BS. 2014. Direct cloning and refactoring of a silent lipopeptide biosynthetic gene cluster yields the antibiotic taromycin A. Proc Natl Acad Sci U S A 111:1957-1962. http://dx.doi.org/10.1073/pnas.1319584111.
6. Baltz RH. 2012. Streptomyces temperate bacteriophage integration systems for stable genetic engineering of actinomycetes (and other organisms). J Ind Microbiol Biotechnol 39:661-672. http://dx.doi.org/10.1007/s10295-011-1069-6.
7. Fogg PC, Colloms S, Rosser S, Stark WM, Smith MCM. 2014. New applications for phage integrases. J Mol Biol 426:2703-2716. http://dx.doi.org/10.1016/j.jmb.2014.05.014.
8. Smith MCM. 2015. Phage-encoded serine integrases and other large serine recombinases, p 253-272. In Craig NL, Chandler M, Gellert M, Lambowitz AM, Rice PA, Sandmeyer S (ed), Mobile DNA, 3rd ed. American Society for Microbiology, Washington, DC.
9. Khaleel T, Younger E, McEwan AR, Varghese AS, Smith MCM. 2011. A phage protein that binds φC31 integrase to switch its directionality. Mol Microbiol 80:1450-1463. http://dx.doi.org/10.1111/j.1365-2958.2011.07696.x.
10. Gregory MA, Till R, Smith MCM. 2003. Integration site for Streptomyces phage fBT1 and the development of novel site-specific integrating vectors. J Bacteriol 185:5320-5323. http://dx.doi.org/10.1128/JB.185.17.5320-5323.2003.
11. Fayed B, Younger E, Taylor G, Smith MCM. 2014. A novel Streptomyces spp. integration vector derived from the S. venezuelae phage, SV1. BMC Biotechnol 14:51. http://dx.doi.org/10.1186/1472-6750-14-51.
12. Morita K, Yamamoto T, Fusada N, Komatsu M, Ikeda H, Hirano N, Takahashi H. 2009. The site-specific recombination system of actinophage TG1. FEMS Microbiol Lett 297:234-240. http://dx.doi.org/10.1111/j.1574-6968.2009.01683.x.
13. Wilson DN. 2014. Ribosome-targeting antibiotics and mechanisms of bacterial resistance. Nat Rev Microbiol 12:35-48.
14. Staunton J, Wilkinson B. 1997. Biosynthesis of erythromycin and rapamycin. Chem Rev 97:2611-2630. http://dx.doi.org/10.1021/cr9600316.
15. Andersen JF, Tatsuta K, Gunji H, Ishiyama T, Hutchinson CR. 1993. Substrate specificity of 6-deoxyerythronolide B hydroxylase, a bacterial cytochrome P450 of erythromycin A biosynthesis. Biochemistry 32:1905-1913.http://dx.doi.org/10.1021/bi00059a004.
16. Summers RG, Donadio S, Staver MJ, Wendt-Pienkowski E, Hutchinson CR, Katz L. 1997. Sequencing and mutagenesis of genes from the erythromycin biosynthetic gene cluster of Saccharopolyspora erythraea that are involved in L-mycarose and D-desosamine production. Microbiology 143(Pt 10):3251-3262.
17. Stassi D, Donadio S, Staver MJ, Katz L. 1993. Identification of a Saccharopolyspora erythraea gene required for the final hydroxylation step in erythromycin biosynthesis. J Bacteriol 175:182-189.
18. Haydock SF, Dowson JA, Dhillon N, Roberts GA, Cortes J, Leadlay PF. 1991. Cloning and sequence analysis of genes involved in erythromycin biosynthesis in Saccharopolyspora erythraea: sequence similarities between EryG and a family of S-adenosylmethionine-dependent methyltransferases. Mol Gen Genet 230:120-128. http://dx.doi.org/10.1007/BF00290659.
19. Oliynyk M, Samborskyy M, Lester JB, Mironenko T, Scott N, Dickens S, Haydock SF, Leadlay PF. 2007. Complete genome sequence of the erythromycin-producing bacterium Saccharopolyspora erythraea NRRL23338. Nat Biotechnol 25:447-453. http://dx.doi.org/10.1038/nbt1297.
20. Zhang H, Wang Y, Wu J, Skalina K, Pfeifer BA. 2010. Complete biosynthesis of erythromycinAand designed analogs using Escherichia coli as a heterologous host. Chem Biol 17:1232-1240. http://dx.doi.org/10.1016/j.chembiol.2010.09.013.
21. Kao CM, Katz L, Khosla C. 1994. Engineered biosynthesis of a complete macrolactone in a heterologous host. Science 265:509-512. http://dx.doi.org/10.1126/science.8036492.
22. Oliynyk M, Brown MJ, Cortes J, Staunton J, Leadlay PF. 1996. A hybrid modular polyketide synthase obtained by domain swapping. Chem Biol 3:833-839. http://dx.doi.org/10.1016/S1074-5521(96)90069-1.
23. Cortes J, Wiesmann KE, Roberts GA, Brown MJ, Staunton J, Leadlay PF. 1995. Repositioning of a domain in a modular polyketide synthase to promote specific chain cleavage. Science 268:1487-1489. http://dx.doi.org/10.1126/science.7770773.
24. Pfeifer BA, Khosla C. 2001. Biosynthesis of polyketides in heterologous hosts. Microbiol Mol Biol Rev 65:106-118. http://dx.doi.org/10.1128/MMBR.65.1.106-118.2001.
25. McDaniel R, Thamchaipenet A, Gustafsson C, Fu H, Betlach M, Ashley G. 1999. Multiple genetic modifications of the erythromycin polyketide synthase to produce a library of novel "unnatural" natural products. Proc Natl Acad Sci U S A 96:1846-1851. http://dx.doi.org/10.1073/pnas.96.5.1846.
26. Xue Q, Ashley G, Hutchinson CR, Santi DV. 1999. A multiplasmid approach to preparing large libraries of polyketides. Proc Natl Acad Sci U S A 96:11740-11745. http://dx.doi.org/10.1073/pnas.96.21.11740.
27. Gust B, Kieser T, Chater KF. 2002. REDIRECT technology: PCRtargeting system in Streptomyces coelicolor. John Innes Centre, Norwich, United Kingdom.
28. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press., Cold Spring Harbor, NY.
29. MacNeil DJ. 1988. Characterization of a unique methyl-specific restriction system in Streptomyces avermitilis. J Bacteriol 170:5607-5612.
30. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. 2000. Practical Streptomyces genetics. The John Innes Foundation, Norwich, United Kingdom.
31. Bedford DJ, Laity C, Buttner MJ. 1995. Two genes involved in the phase-variable φC31 resistance mechanism of Streptomyces coelicolor A3(2). J Bacteriol 177:4681-4689.
32. Floriano B, Bibb M. 1996. afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 21:385-396. http://dx.doi.org/10.1046/j.1365-2958.1996.6491364.x.
33. Gomez-Escribano JP, Bibb MJ. 2011. Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb Biotechnol 4:207-215. http://dx.doi.org/10.1111/j.1751-7915.2010.00219.x.
34. Lee J, Lee HJ, Shin MK, Ryu WS. 2004. Versatile PCR-mediated insertion or deletion mutagenesis. Biotechniques 36:398-400.
35. Rowe CJ, Cortes J, Gaisser S, Staunton J, Leadlay PF. 1998. Construction of new vectors for high-level expression in actinomycetes. Gene 216: 215-223. http://dx.doi.org/10.1016/S0378-1119(98)00327-8.
36. Schell U, Haydock SF, Kaja AL, Carletti I, Lill RE, Read E, Sheehan LS, Low L, Fernandez MJ, Grolle F, McArthur HA, Sheridan RM, Leadlay PF, Wilkinson B, Gaisser S. 2008. Engineered biosynthesis of hybrid macrolide polyketides containing D-angolosamine and D-mycaminose moieties. Org Biomol Chem 6:3315-3327. http://dx.doi.org/10.1039/b807914e.
37. Minas W. 2005. Production of erythromycin with Saccharopolyspora erythraea, vol 18. Humana Press, Inc, New York, NY.
38. Hu H, Zhang Q, Ochi K. 2002. Activation of antibiotic biosynthesis by specified mutations in the rpoB gene (encoding the RNA polymerase beta subunit) of Streptomyces lividans. J Bacteriol 184:3984-3991. http://dx.doi.org/10.1128/JB.184.14.3984-3991.2002.
39. Okamoto-Hosoya Y, Sato TA, Ochi K. 2000. Resistance to paromomycin is conferred by rpsL mutations, accompanied by an enhanced antibiotic production in Streptomyces coelicolor A3(2). J Antibiot 53:1424-1427. http://dx.doi.org/10.7164/antibiotics.53.1424.
40. Shima J, Hesketh A, Okamoto S, Kawamoto S, Ochi K. 1996. Induction of actinorhodin production by rpsL (encoding ribosomal protein S12) mutations that confer streptomycin resistance in Streptomyces lividans and Streptomyces coelicolor A3(2). J Bacteriol 178:7276-7284.
41. Baltz RH. 2010. Streptomyces and Saccharopolyspora hosts for heterologous expression of secondary metabolite gene clusters. J Ind Microbiol Biotechnol 37:759-772. http://dx.doi.org/10.1007/s10295-010-0730-9.
42. Omura S, Tanaka H. 1984. Production and antimicrobial activity of macrolides, p 3-36. In Omura S (ed), Macrolide antibiotics: chemistry, biology, and practice. Academic Press, Orlando, FL.
43. Borisova SA, Zhao L, Melancon IC, Kao CL, Liu HW. 2004. Characterization of the glycosyltransferase activity of desVII: analysis of and implications for the biosynthesis of macrolide antibiotics. J Am Chem Soc 126:6534-6535. http://dx.doi.org/10.1021/ja049967j.
44. Butler AR, Bate N, Kiehl DE, Kirst HA, Cundliffe E. 2002. Genetic engineering of aminodeoxyhexose biosynthesis in Streptomyces fradiae. Nat Biotechnol 20:713-716. http://dx.doi.org/10.1038/nbt0702-713.
45. Gaisser S, Reather J, Wirtz G, Kellenberger L, Staunton J, Leadlay PF. 2000. A defined system for hybrid macrolide biosynthesis in Saccharopolyspora erythraea. Mol Microbiol 36:391-401. http://dx.doi.org/10.1046/j.1365-2958.2000.01856.x.