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2014 | 61 | 1 | 141-147
Article title

Type II thioesterase ScoT is required for coelimycin production by the modular polyketide synthase Cpk of Streptomyces coelicolor A3(2)

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Abstracts
EN
Type II thioesterases were shown to maintain efficiency of modular type I polyketide synthases and nonribosomal peptide synthetases by removing acyl residues blocking extension modules. We found that thioesterase ScoT from Streptomyces coelicolor A3(2) is required for the production of the yellow-pigmented coelimycin by the modular polyketide synthase Cpk. No production of coelimycin was observed in cultures of scoT disruption mutant. Polyketide production was restored upon complementation with an intact copy of the scoT gene. An enzymatic assay showed that ScoT thioesterase can hydrolyse a 12-carbon acyl chain but the activity is too low to play a role in product release from the polyketide synthase. We conclude that ScoT is an editing enzyme necessary to maintain the activity of polyketide synthase Cpk. We provide a HPLC based method to measure the amount of coelimycin P2 in a culture medium.
Publisher

Year
Volume
61
Issue
1
Pages
141-147
Physical description
Dates
published
2014
received
2013-10-30
revised
2014-01-22
accepted
2014-03-05
(unknown)
2014-03-21
Contributors
  • Ludwik Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wroclaw, Poland
  • Ludwik Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wroclaw, Poland
  • Ludwik Hirszfeld Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wroclaw, Poland
References
  • Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A, Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O'Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
  • Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, Schoner BE (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49.
  • Boettger D, Hertweck C (2013) Molecular diversity sculpted by fungal PKS-NRPS hybrids. Chembiochem 14: 28-42.
  • Butler AR, Bate N, Cundliffe E (1999) Impact of thioesterase activity on tylosin biosynthesis in Streptomyces fradiae. Chem Biol 6: 287-292.
  • Challis GL (2013) Exploitation of the Streptomyces coelicolor A3(2) genome sequence for discovery of new natural products and biosynthetic pathways. J Ind Microbiol Biotechnol 41: 219-232.
  • Chen S, Xue Y, Sherman DH, Reynolds KA (2000) Mechanisms of molecular recognition in the pikromycin polyketide synthase. Chem Biol 7: 907-918.
  • Claxton HB, Akey DL, Silver MK, Admiraal SJ, Smith JL (2009) Structure and functional analysis of RifR, the type II thioesterase from the rifamycin biosynthetic pathway. J Biol Chem 284: 5021-5029.
  • Doi-Katayama Y, Yoon YJ, Choi CY, Yu TW, Floss HG, Hutchinson CR (2000) Thioesterases and the premature termination of polyketide chain elongation in rifamycin B biosynthesis by Amycolatopsis mediterranei S699. J Antibiot. (Tokyo) 53: 484-95.
  • Geoffroy VA, Fetherston JD, Perry RD (2000) Yersinia pestis YbtU and YbtT are involved in synthesis of the siderophore yersiniabactin but have different effects on regulation. Infect Immun 68: 4452-4461.
  • Gómez C, Olano C, Palomino-Schätzlein M, Pineda-Lucena A, Carbajo RJ, Braña AF, Méndez C, Salas JA (2012) Novel compounds produced by Streptomyces lydicus NRRL 2433 engineered mutants altered in the biosynthesis of streptolydigin. J Antibiot (Tokyo) 65: 341-348.
  • Gomez-Escribano JP, Song L, Fox DJ, Yeo V, Bibb MJ, Challis GL (2012) Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chem Sci 3: 2716-2720.
  • Gottelt M, Kol S, Gomez-Escribano JP, Bibb M, Takano E (2010) Deletion of a regulatory gene within the cpk gene cluster reveals novel antibacterial activity in Streptomyces coelicolor A3(2). Microbiology 156: 2343-2353.
  • Heathcote ML, Staunton J, Leadlay PF (2001) Role of type II thioesterases: evidence for removal of short acyl chains produced by aberrant decarboxylation of chain extender units. Chem Biol 8: 207-220.
  • Liu T, You D, Valenzano C, Sun Y, Li J, Yu Q, Zhou X, Cane DE, Deng Z (2006) Identification of NanE as the thioesterase for polyether chain release in nanchangmycin biosynthesis. Chem Biol 13: 945-955.
  • Liu T, Lin X, Zhou X, Deng Z, Cane DE (2008) Mechanism of thioesterase-catalyzed chain release in the biosynthesis of the polyether antibiotic nanchangmycin. Chem Biol 15: 449-458.
  • Kalaitzis JA, Cheng Q, Meluzzi D, Xiang L, Izumikawa M, Dorrestein PC, Moore BS (2011) Policing starter unit selection of the enterocin type II polyketide synthase by the type II thioesterase EncL. Bioorg Med Chem 19: 6633-6638.
  • Kelley LA, Sternberg MJ (2009) Protein structure prediction on the web: a case study using the Phyre server. Nature Protocols 4: 363-371.
  • Kim BS, Cropp TA, Beck BJ, Sherman DH, Reynolds KA (2002) Biochemical evidence for an editing role of thioesterase II in the biosynthesis of the polyketide pikromycin. J Biol Chem 277: 48028-48034
  • Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces Genetics. The John Innes Foundation, Norwich, UK.
  • Koglin A, Walsh CT (2009) Structural insights into nonribosomal peptide enzymatic assembly lines. Nat Prod Rep 26: 987-1000.
  • Kotowska M, Pawlik K, Butler AR, Cundliffe E, Takano E, Kuczek K (2002) Type II thioesterase from Streptomyces coelicolor A3(2). Microbiology 148: 1777-1783.
  • Kotowska M, Pawlik K, Smulczyk-Krawczyszyn A, Bartosz-Bechowski H, Kuczek K (2009) Type II thioesterase ScoT, associated with Streptomyces coelicolor A3(2) modular polyketide synthase Cpk, hydrolyzes acyl residues and has a preference for propionate. Appl Environ Microbiol 75: 887-896.
  • Olano C, Méndez C, Salas JA (2009) Antitumor compounds from actinomycetes: from gene clusters to new derivatives by combinatorial biosynthesis. Nat Prod Rep 26: 628-660.
  • Oliynyk M, Stark CB, Bhatt A, Jones MA, Hughes-Thomas ZA, Wilkinson C, Oliynyk Z, Demydchuk Y, Staunton J, Leadlay PF (2003) Analysis of the biosynthetic gene cluster for the polyether antibiotic monensin in Streptomyces cinnamonensis and evidence for the role of monB and monC genes in oxidative cyclization. Mol Microbiol 49: 1179-1190.
  • Pawlik K, Kotowska M, Chater KF, Kuczek K, Takano E (2007) A cryptic type I polyketide synthase (cpk) gene cluster in Streptomyces coelicolor A3(2). Arch Microbiol 187: 87-99.
  • Pawlik K, Kotowska M, Kolesiński P (2010) Streptomyces coelicolor A3(2) produces a new yellow pigment associated with the polyketide synthase Cpk. J Mol Microbiol Biotechnol 19: 147-151.
  • Rui Z, Petrícková K, Skanta F, Pospísil S, Yang Y, Chen CY, Tsai SF, Floss HG, Petrícek M, Yu TW (2010) Biochemical and genetic insights into asukamycin biosynthesis. J Biol Chem 285: 24915-24924.
  • Sambrook J, Russel DW (2001) Molecular Cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor New York.
  • Schneider A, Marahiel MA (1998) Genetic evidence for a role of thioesterase domains, integrated in or associated with peptide synthetases, in non-ribosomal peptide biosynthesis in Bacillus subtilis. Arch Microbiol 169: 404-410.
  • Shen Y, Huang H, Zhu L, Luo M, Chen D (2012) Type II thioesterase gene (ECO-orf27) from Amycolatopsis orientalis influences production of the polyketide antibiotic, ECO-0501 (LW01). Biotechnol Lett 34: 2087-2091.
  • Schwarzer D, Mootz HD, Linne U, Marahiel MA (2002) Regeneration of misprimed nonribosomal peptide synthetases by type II thioesterases. Proc Natl Acad Sci USA 99: 14083-14088.
  • Staunton J, Weissman KJ (2001) Polyketide biosynthesis: a millennium review. Nat Prod Rep 18: 380-416
  • Wong FT, Khosla C (2012) Combinatorial biosynthesis of polyketides - a perspective. Curr Opin Chem Biol 16: 117-123.
  • Yeh E, Kohli RM, Bruner SD, Walsh CT (2004) Type II thioesterase restores activity of a NRPS module stalled with an aminoacyl-S-enzyme that cannot be elongated. Chembiochem 5: 1290-1293.
  • Yu FM, Qiao B, Zhu F, Wu JC, Yuan YJ (2006) Functional analysis of type II thioesterase of Streptomyces lydicus AS 4.2501. Appl Biochem Biotechnol 135: 145-158.
  • Zhou Y, Meng Q, You D, Li J, Chen S, Ding D, Zhou X, Zhou H, Bai L, Deng Z (2008) Selective removal of aberrant extender units by a type II thioesterase for efficient FR-008/candicidin biosynthesis in Streptomyces sp. strain FR-008. Appl Environ Microbiol 74: 7235-7242.
Document Type
Publication order reference
Identifiers
YADDA identifier
bwmeta1.element.bwnjournal-article-abpv61p141kz
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