A Streptomyces coelicolor host for the heterologous expression of Type III polyketide synthase genes

Microbial Cell Factories

Volumn 14, Issue 1, 2015, Pages

  Thanapipatsiri, Anyarat ^a,b   Claesen, Jan ^b,c   Gomez Escribano, Juan Pablo ^b   Bibb, Mervyn ^b   Thamchaipenet, Arinthip ^a  

^a KASETSART UNIVERSITY   (Thailand)

^b JOHN INNES CENTRE   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Expression host; Streptomyces; Type III polyketide synthases

Indexed keywords

FLAVIOLIN; METACYCLINE; ORGANIC COMPOUND; POLYKETIDE SYNTHASE; TYPE III POLYKETIDE SYNTHASE; UNCLASSIFIED DRUG; NAPHTHOQUINONE; PYRONE DERIVATIVE;

ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DELETION MUTANT; GCS GENE; GENE; HETEROLOGOUS EXPRESSION; NONHUMAN; PROMOTER REGION; RPPA GENE; SRSA GENE; STREPTOMYCES COELICOLOR; STREPTOMYCES VENEZUELAE; SYNTHESIS; BIOREACTOR; GENETIC ENGINEERING; GENETICS; METABOLISM; MULTIGENE FAMILY; SITE DIRECTED MUTAGENESIS; TRANSGENIC ORGANISM;

BIOREACTORS; GENETIC ENGINEERING; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; NAPHTHOQUINONES; ORGANISMS, GENETICALLY MODIFIED; POLYKETIDE SYNTHASES; PYRONES; STREPTOMYCES COELICOLOR;

EID: 84941778233     PISSN: None     EISSN: 14752859     Source Type: Journal    
DOI: 10.1186/s12934-015-0335-0     Document Type: Article

References (50)

1. Moore BS, Hopke JN. Discovery of a new bacterial polyketide biosynthetic pathway. Chembiochem. 2001;2:35-8.
2. Hertweck C. The biosynthetic logic of polyketide diversity. Angew Chem Int Ed Engl. 2009;48:4688-716.
3. Pfeifer V, Nicholson GJ, Ries J, Recktenwald J, Schefer AB, Shawky RM, et al. A polyketide synthase in glycopeptide biosynthesis: the biosynthesis of the non-proteinogenic amino acid (S)-3,5-dihydroxyphenylglycine. J Biol Chem. 2001;276:38370-7.
4. Saxena P, Yadav G, Mohanty D, Gokhale RS. A new family of Type III polyketide synthases in Mycobacterium tuberculosis. J Biol Chem. 2003;278:44780-90.
5. Song L, Barona-Gomez F, Corre C, Xiang L, Udwary DW, Austin MB, et al. Type III polyketide synthase beta-ketoacyl-ACP starter unit and ethylmalonyl-CoA extender unit selectivity discovered by Streptomyces coelicolor genome mining. J Am Chem Soc. 2006;128:14754-5.
6. Funa N, Funabashi M, Ohnishi Y, Horinouchi S. Biosynthesis of hexahydroxyperylenequinone melanin via oxidative aryl coupling by cytochrome P-450 in Streptomyces griseus. J Bacteriol. 2005;187:8149-55.
7. Yu D, Xu F, Zeng J, Zhan J. Type III polyketide synthases in natural product biosynthesis. IUBMB Life. 2012;64:285-95.
8. Izumikawa M, Shipley PR, Hopke JN, O'Hare T, Xiang L, Noel JP, et al. Expression and characterization of the Type III polyketide synthase 1,3,6,8-tetrahydroxynaphthalene synthase from Streptomyces coelicolor A3(2). J Ind Microbiol Biotechnol. 2003;30:510-5.
9. Austin MB, Izumikawa M, Bowman ME, Udwary DW, Ferrer JL, Moore BS, et al. Crystal structure of a bacterial Type III polyketide synthase and enzymatic control of reactive polyketide intermediates. J Biol Chem. 2004;279:45162-74.
10. Funa N, Funabashi M, Yoshimura E, Horinouchi S. A novel quinone-forming monooxygenase family involved in modification of aromatic polyketides. J Biol Chem. 2005;280:14514-23.
11. Zhao B, Guengerich FP, Bellamine A, Lamb DC, Izumikawa M, Lei L, et al. Binding of two flaviolin substrate molecules, oxidative coupling, and crystal structure of Streptomyces coelicolor A3(2) cytochrome P450 158A2. J Biol Chem. 2005;280:11599-607.
12. Funabashi M, Funa N, Horinouchi S. Phenolic lipids synthesized by Type III polyketide synthase confer penicillin resistance on Streptomyces griseus. J Biol Chem. 2008;283:13983-91.
13. Chen H, Tseng CC, Hubbard BK, Walsh CT. Glycopeptide antibiotic biosynthesis: enzymatic assembly of the dedicated amino acid monomer (S)-3,5-dihydroxyphenylglycine. Proc Natl Acad Sci USA. 2001;98:14901-6.
14. Pelzer S, Sussmuth R, Heckmann D, Recktenwald J, Huber P, Jung G, et al. Identification and analysis of the balhimycin biosynthetic gene cluster and its use for manipulating glycopeptide biosynthesis in Amycolatopsis mediterranei DSM5908. Antimicrob Agents Chemother. 1999;43:1565-73.
15. Horbal L, Kobylyanskyy A, Truman AW, Zaburranyi N, Ostash B, Luzhetskyy A, et al. The pathway-specific regulatory genes, tei15*and tei16*, are the master switches of teicoplanin production in Actinoplanes teichomyceticus. Appl Microbiol Biotechnol. 2014;98:9295-309.
16. Wenzel SC, Bode HB, Kochems I, Muller R. A Type I/Type III polyketide synthase hybrid biosynthetic pathway for the structurally unique ansa compound kendomycin. Chembiochem. 2008;9:2711-21.
17. Olano C, Carmaen M, José AS. Streptomyces: Molecular Biology and Biotechnology. Gene clusters for bioactive natural products in actinomycetes and their use in combinatorial biosynthesis. Norfolk: Caister Academic Press; 2011.
18. Baltz RH. Streptomyces and Saccharopolyspora hosts for heterologous expression of secondary metabolite gene clusters. J Ind Microbiol Biotechnol. 2010;37:759-72.
19. Omura S, Ikeda H, Ishikawa J, Hanamoto A, Takahashi C, Shinose M, et al. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc Natl Acad Sci USA. 2001;98:12215-20.
20. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, et al. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol. 2003;21:526-31.
21. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature. 2002;417:141-7.
22. Komatsu M, Uchiyama T, Omura S, Cane DE, Ikeda H. Genome-minimized Streptomyces host for the heterologous expression of secondary metabolism. Proc Natl Acad Sci USA. 2010;107:2646-51.
23. Komatsu M, Komatsu K, Koiwai H, Yamada Y, Kozone I, Izumikawa M, et al. Engineered Streptomyces avermitilis host for heterologous expression of biosynthetic gene cluster for secondary metabolites. ACS Synth Biol. 2013;2:384-96.
24. Gomez-Escribano JP, Bibb MJ. Engineering Streptomyces coelicolor for heterologous expression of secondary metabolite gene clusters. Microb Biotechnol. 2011;4:207-15.
25. Gomez-Escribano JP, Bibb MJ. Streptomyces coelicolor as an expression host for heterologous gene clusters. Methods Enzymol. 2012;517:279-300.
26. Li T, Du Y, Cui Q, Zhang J, Zhu W, Hong K, et al. Cloning, characterization and heterologous expression of the indolocarbazole biosynthetic gene cluster from marine-derived Streptomyces sanyensis FMA. Mar Drugs. 2013;11:466-88.
27. Niu G, Li L, Wei J, Tan H. Cloning, heterologous expression, and characterization of the gene cluster required for gougerotin biosynthesis. Chem Biol. 2013;20:34-44.
28. Flinspach K, Westrich L, Kaysser L, Siebenberg S, Gomez-Escribano JP, Bibb M, et al. Heterologous expression of the biosynthetic gene clusters of coumermycin A(1), clorobiocin and caprazamycins in genetically modified Streptomyces coelicolor strains. Biopolymers. 2010;93:823-32.
29. Flinspach K, Kapitzke C, Tocchetti A, Sosio M, Apel AK. Heterologous expression of the thiopeptide antibiotic GE2270 from Planobispora rosea ATCC 53733 in Streptomyces coelicolor requires deletion of ribosomal genes from the expression construct. PLoS One. 2014. doi: 10.1371/journal.pone.0090499 .
30. Robles-Reglero V, Santamarta I, Alvarez-Alvarez R, Martin JF, Liras P. Transcriptional analysis and proteomics of the holomycin gene cluster in overproducer mutants of Streptomyces clavuligerus. J Biotechnol. 2013;163:69-76.
31. Jankowitsch F, Schwarz J, Ruckert C, Gust B, Szczepanowski R, Blom J, et al. Genome sequence of the bacterium Streptomyces davawensis JCM 4913 and heterologous production of the unique antibiotic roseoflavin. J Bacteriol. 2012;194:6818-27.
32. Ikeda H, Kazuo SY, Omura S. Genome mining of the Streptomyces avermitilis genome and development of genome-minimized hosts for heterologous expression of biosynthetic gene clusters. J Ind Microbiol Biotechnol. 2014;41:233-50.
33. Challis GL, Hopwood DA. Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA. 2003;100(Suppl 2):14555-61.
34. Gruschow S, Buchholz TJ, Seufert W, Dordick JS, Sherman DH. Substrate profile analysis and ACP-mediated acyl transfer in Streptomyces coelicolor Type III polyketide synthases. Chembiochem. 2007;8:863-8.
35. Gust B, Chandra G, Jakimowicz D, Yuqing T, Bruton CJ, Chater KF. Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces. Adv Appl Microbiol. 2004;54:107-28.
36. Sambrook J, Russell DW. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press; 2001.
37. Beltran-Garcia MJ, Prado FM, Oliveira MS, Ortiz-Mendoza D, Scalfo AC, Pessoa A Jr, et al. Singlet molecular oxygen generation by light-activated DHN-melanin of the fungal pathogen Mycosphaerella fijiensis in black Sigatoka disease of bananas. PLoS One. 2014. doi: 10.1371/journal.pone.0091616 .
38. Ghimire GP, Oh TJ, Liou K, Sohng JK. Identification of a cryptic Type III polyketide synthase (1,3,6,8-tetrahydroxynaphthalene synthase) from Streptomyces peucetius ATCC 27952. Mol Cells. 2008;26:362-7.
39. Funa N, Ohnishi Y, Ebizuka Y, Horinouchi S. Properties and substrate specificity of RppA, a chalcone synthase-related polyketide synthase in Streptomyces griseus. J Biol Chem. 2002;277:4628-35.
40. Lim YR, Hong MK, Kim JK, Doan TT, Kim DH, Yun CH, et al. Crystal structure of cytochrome P450 CYP105N1 from Streptomyces coelicolor, an oxidase in the coelibactin siderophore biosynthetic pathway. Arch Biochem Biophys. 2012;528:111-7.
41. Gust B, Challis GL, Fowler K, Kieser T, Chater KF. PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA. 2003;100:1541-6.
42. Joshi MV, Mann SG, Antelmann H, Widdick DA, Fyans JK, Chandra G, et al. The twin arginine protein transport pathway exports multiple virulence proteins in the plant pathogen Streptomyces scabies. Mol Microbiol. 2010;77:252-71.
43. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA. Practical Streptomyces Genetics. Norwich Research Park, Colney, Norwich: John Innes Foundation; 2000.
44. Shima J, Hesketh A, Okamoto S, Kawamoto S, Ochi K. 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. 1996;178:7276-84.
45. Cherepanov PP, Wackernagel W. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene. 1995;158:9-14.
46. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA. 2000;97:6640-5.
47. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, MacNeil T. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene. 1992;111:61-8.
48. Healy FG, Eaton KP, Limsirichai P, Aldrich JF, Plowman AK, King RR. Characterization of gamma-butyrolactone autoregulatory signaling gene homologs in the angucyclinone polyketide WS5995B producer Streptomyces acidiscabies. J Bacteriol. 2009;191:4786-97.
49. Claesen J. Cloning and analysis of the cypemycin biosynthetic gene cluster. University of East Anglia; 2010.
50. Paget MS, Chamberlin L, Atrih A, Foster SJ, Buttner MJ. Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J Bacteriol. 1999;181:204-11.