Evaluation of Streptomyces coelicolor A3(2) as a heterologous expression host for the cyanobacterial protein kinase C activator lyngbyatoxin A

FEBS Journal

Volumn 279, Issue 7, 2012, Pages 1243-1251

  Jones, Adam C ^a   Ottilie, Sabine ^a   Eustáquio, Alessandra S ^a   Edwards, Daniel J ^b   Gerwick, Lena ^a   Moore, Bradley S ^a,c   Gerwick, William H ^a,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

gene cluster; heterologous expression; marine cyanobacteria; natural product; Streptomyces

Indexed keywords

BACTERIAL RNA; COMPLEMENTARY DNA; CYTOCHROME P450; CYTOSINE; GUANINE; LEUCINE; LYNGBYATOXIN A; PEPTIDE SYNTHASE; PROTEIN LTXB; PROTEIN LTXC; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BIOSYNTHESIS; CODON; CONTROLLED STUDY; CYANOBACTERIUM; GENE CLUSTER; IN VITRO STUDY; LTXA GENE; LTXB GENE; LTXC GENE; MOLECULAR CLONING; MOOREA PRODUCTA; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA EXTRACTION; STREPTOMYCES COELICOLOR; STREPTOMYCES COELICOLOR A3(2);

BACTERIAL PROTEINS; BIOLOGICAL AGENTS; CYANOBACTERIA; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LYNGBYA TOXINS; MOLECULAR STRUCTURE; MULTIGENE FAMILY; OPEN READING FRAMES; PROTEIN KINASE C; STREPTOMYCES COELICOLOR;

CYANOBACTERIA; LYNGBYA MAJUSCULA; STREPTOMYCES; STREPTOMYCES COELICOLOR;

EID: 84859111197     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08517.x     Document Type: Article

References (37)

1. Wilkinson B, &, Micklefield J, (2007) Mining and engineering natural-product biosynthetic pathways. Nat Chem Biol 3, 379-386.
2. Lane AL, &, Moore BS, (2010) A sea of biosynthesis: marine natural products meet the molecular age. Nat Prod Rep 28, 411-428.
3. Gust B, Challis GL, Fowler K, Kieser T, &, Chater KF, (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100, 1541-1546.
4. Rachid S, Gerth K, Kochems I, &, Müller R, (2007) Deciphering regulatory mechanisms for secondary metabolite production in the myxobacterium Sorangium cellulosum So ce56. Mol Microbiol 63, 1783-1796.
5. Watanabe K, Hotta K, Praseuth AP, Koketsu K, Migita A, Boddy CN, Wang CCC, Oguri H, &, Oikawa H, (2006) Total biosynthesis of antitumor nonribosomal peptides in Escherichia coli. Nat Chem Biol 2, 423-428.
6. Eustáquio AS, Gust B, Galm U, Li S-M, Chater KF, &, Heide L, (2005) Heterologous expression of novobiocin and chlorobiocin biosynthetic gene clusters. Appl Environ Microbiol 71, 2452-2459.
7. Heide L, (2009) Aminocoumarins: mutasynthesis, chemoenzymatic synthesis, and metabolic engineering. Methods Enzymol 459, 437-455.
8. Rossi JV, Roberts MA, Yoo H-D, &, Gerwick WH, (1997) Pilot scale culture of the marine cyanobacterium Lyngbya majuscula for its pharmaceutically useful natural metabolite curacin A. J Appl Phycol 9, 195-204.
9. Suyama TL, &, Gerwick WH, (2008) Stereospecific total synthesis of somocystinamide A. Org Lett 10, 4449-4452.
10. Engene N, Rottacker EC, Kastovsky J, Byrum T, Choi H, Ellisman MH, Komárek J, &, Gerwick WH, (2011) Moorea producta gen. nov., sp. nov. and Moorea bouillonii comb. nov., tropical marine cyanobacteria rich in bioactive secondary metabolites. Int J Syst Evol Microbiol doi:.
11. Esquenazi E, Jones AC, Byrum T, Dorrestein PC, &, Gerwick WH, (2011) Temporal dynamics of natural product biosynthesis in marine cyanobacteria. Proc Natl Acad Sci USA 108, 5226-5231.
12. Jones AC, Monroe EA, Podell S, Hess WR, Klages S, Esquenazi E, Niessen S, Hoover H, Rothmann M, Lasken RS, et al. (2011) Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula. Proc Natl Acad Sci USA 108, 8815-8820.
13. Simmons TL, Coates RC, Clark BR, Engene N, Gonzalez D, Esquenazi E, Dorrestein PC, &, Gerwick WH, (2008) Biosynthetic origin of natural products isolated from marine microorganism-invertebrate assemblages. Proc Natl Acad Sci USA 105, 4587-4594.
14. Grindberg RV, Ishoey T, Brinza D, Esquenazi E, Coates RC, Liu W-T, Gerwick L, Dorrestein PC, Pevzner P, Lasken R, et al. (2011) Single cell genome amplification accelerates identification of the apratoxin biosynthetic pathway from a complex microbial assemblage. PLoS One 6, e18565.
15. Baltz RH, (2008) Renaissance in antibacterial discovery from actinomycetes. Curr Opin Pharmacol 8, 557-563.
16. Nett M, Ikeda H, &, Moore BS, (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26, 1362-1384.
17. Kieser T, Bibb MJ, Buttner MJ, Chater KF, &, Hopwood DA, (2000) Practical Streptomyces Genetics, 2nd edn. John Innes Foundation, Norwich, UK.
18. Bentley SD, Chater KF, Cerdeño-Tárraga A-M, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, et al. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature, 417, 141-147.
19. Leskiw BK, Bibb MJ, &, Chater KF, (1991) The use of a rare codon specifically during development? Mol Microbiol 5, 2861-2867.
20. Takano E, Tao M, Long F, Bibb MJ, Wang L, Li W, Buttner MJ, Bibb MJ, Deng ZX, &, Chater KF, (2003) A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol Microbiol 50, 475-486.
21. Chater KF, &, Chandra G, (2008) The use of the rare UUA codon to define 'expression space' for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces. J Microbiol 46, 1-11.
22. Edwards DJ, &, Gerwick WH, (2004) Lyngbyatoxin biosynthesis: sequence of biosynthetic gene cluster and identification of a novel aromatic prenyltransferase. J Am Chem Soc 126, 11432-11433.
23. Basu A, Kozikowski AP, &, Lazo JS, (1992) Structural requirements of lyngbyatoxin A for activation and downregulation of protein kinase C. Biochemistry 31, 3824-3830.
24. Cardellina JH II, Marner FJ, &, Moore RE, (1979) Seaweed dermatitis: structure of lyngbyatoxin A. Science 204, 193-195.
25. Fujiki H, Mori M, Nakayasu M, Terada M, Sugimura T, &, Moore RE, (1981) Indole alkaloids: dihydroteleocidin B, teleocidin, and lyngbyatoxin A as members of a new class of tumor promoters. Proc Natl Acad Sci USA 78, 3872-3876.
26. Read JA, &, Walsh CT, (2007) The lyngbyatoxin biosynthetic assembly line: chain release by four-electron reduction of a dipeptidyl thioester to the corresponding alcohol. J Am Chem Soc 129, 15762-15763.
27. Huynh MU, Elston MC, Hernandez NM, Ball DB, Kajiyama S-i, Irie K, Gerwick WH, &, Edwards DJ, (2010) Enzymatic production of (-)-indolactam V by LtxB, a cytochrome P450 monooxygenase. J Nat Prod 73, 71-74.
28. Herai S, Hashimoto Y, Higashibata H, Maseda H, Ikeda H, Amura S, &, Kobayashi M, (2004) Hyper-inducible expression system for Streptomycetes. Proc Natl Acad Sci USA 101, 14031-14035.
29. Nagasawa T, Nakamura T, &, Yamada H, (1990) μ-Caprolactam, a new powerful inducer for the formation of Rhodococcus rhodochrous J1 nitrilase. Arch Microbiol 155, 13-17.
30. Flinspach K, Westrich L, Kaysser L, Siebenberg S, Gomez-Escribano JP, Bibb MJ, Gust B, &, Heide L, (2010) Heterologous expression of the biosynthetic gene clusters of coumermycin A1, chlorobiocin and caprazamycins in genetically modified Streptomyces coelicolor strains. Biopolymers 93, 823-832.
31. Jones AC, Monroe EA, Eisman EB, Gerwick L, Sherman DH, &, Gerwick WH, (2010) The unique mechanistic transformations involved in the biosynthesis of modular natural products from marine cyanobacteria. Nat Prod Rep 27, 1048-1065.
32. Chang Z, Sitachitta N, Rossi JV, Roberts MA, Flatt PM, Jia J, Sherman DH, &, Gerwick WH, (2004) Biosynthetic pathway and gene cluster analysis of curacin A, an antitubulin natural product from the tropical marine cyanobacterium Lyngbya majuscula. J Nat Prod 67, 1356-1367.
33. 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.
34. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, &, MacNeil T, (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111, 61-68.
35. Dekleva ML, Titus JA, &, Strohl WR, (1985) Nutrient effects on anthracycline production by Streptomyces peucetius in a defined medium. Can J Microbiol 31, 287-294.
36. Irie K, Nakagawa Y, Tomimatsu S, &, Ohigashi H, (1998) Biosynthesis of the monoterpenoid moiety of teleocidins via the non-mevalonate pathway in Streptomyces. Tetrahedron Lett 39, 7929-7930.
37. Ramaswamy AV, Sorrels CM, &, Gerwick WH, (2007) Cloning and biochemical characterization of the hectochlorin biosynthetic gene cluster from the marine cyanobacterium Lyngbya majuscula. J Nat Prod 70, 1977-1986.