Hierarchical control on polyene macrolide biosynthesis: PimR modulates pimaricin production via the PAS-LuxR transcriptional activator pimM

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Santos Aberturas, Javier ^a,b   Vicente, Cláudia M ^b   Payero, Tamara D ^a,b   Martín Sánchez, Lara ^b   Cañibano, Carmen ^b   Martín, Juan F ^b   Aparicio, Jesús F ^a,b  

^a UNIVERSITY OF LEÓN   (Spain)

^b Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MACROLIDE; NATAMYCIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LUXR; TRANSCRIPTION FACTOR PIMR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; POLYENE;

ANTIBIOTIC BIOSYNTHESIS; ARTICLE; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE CLUSTER; GENE EXPRESSION; GENETIC COMPLEMENTATION; HETEROLOGOUS EXPRESSION; NONHUMAN; PIMM GENE; PIMR GENE; PROMOTER REGION; REGULATOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRUCTURAL GENE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; STREPTOMYCES;

ESCHERICHIA COLI; STREPTOMYCES; STREPTOMYCES NATALENSIS;

BACTERIAL PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; MACROLIDES; NATAMYCIN; POLYENES; STREPTOMYCES; TRANSCRIPTION FACTORS;

EID: 84861855586     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038536     Document Type: Article

References (53)

1. Aparicio JF, Mendes MV, Antón N, Recio E, Martín JF, (2004) Polyene macrolide antibiotic biosynthesis. Curr Med Chem 11: 1645-1656.
2. Caffrey P, Aparicio JF, Malpartida F, Zotchev SB, (2008) Biosynthetic engineering of polyene macrolides towards generation of improved antifungal and antiparasitic agents. Curr Top Med Chem 8: 639-653.
3. Bibb MJ, (2005) Regulation of secondary metabolism in Streptomycetes. Curr Opin Microbiol 8: 208-215.
4. Antón N, Mendes MV, Martín JF, Aparicio JF, (2004) Identification of PimR as a positive regulator of pimaricin biosynthesis in Streptomyces natalensis. J Bacteriol 186: 2567-2575.
5. Martín JF, Aparicio JF, (2009) Enzymology of the Polyenes Pimaricin and Candicidin Biosynthesis. Methods Enzymol 459: 215-242.
6. Mendes MV, Recio E, Fouces R, Luiten R, Martín JF, et al. (2001) Engineered biosynthesis of novel polyenes: a pimaricin derivative produced by targeted gene disruption in Streptomyces natalensis. Chem Biol 8: 635-644.
7. Mendes MV, Antón N, Martín JF, Aparicio JF, (2005) Characterization of the polyene macrolid P450 epoxidase from Streptomyces natalensis that converts de-epoxypimaricin into pimaricin. Biochem J 386: 57-62.
8. Mendes MV, Recio E, Antón N, Guerra SM, Santos-Aberturas J, et al. (2007) Cholesterol oxidases act as signalling proteins for the biosynthesis of the polyene macrolide pimaricin. Chem Biol 14: 279-290.
9. Aparicio JF, Martín JF, (2008) Microbial cholesterol oxidases: Bioconversion enzymes or signal proteins? Mol Biosyst 4: 804-809.
10. Vicente CM, Santos-Aberturas J, Guerra SM, Payero TD, Martín JF, et al. (2009) PimT, an amino acid exporter controls polyene production via secretion of the quorum sensing pimaricin-inducer PI-factor in Streptomyces natalensis. Microb Cell Fact 8: 33.
11. Kells PM, Ouellet H, Santos-Aberturas J, Aparicio JF, Podust LM, (2010) Structure of cytochrome P450 PimD suggests epoxidation of the polyene macrolide pimaricin occurs via a hydroperoxoferric intermediate. Chem Biol 17: 841-851.
12. Recio E, Colinas A, Rumbero A, Aparicio JF, Martín JF, (2004) PI factor, a novel type quorum-sensing inducer elicits pimaricin production in Streptomyces natalensis. J Biol Chem 279: 41586-41593.
13. Beites T, Pires SDS, Santos CL, Osório H, Moradas-Ferreira P, et al. (2011) Crosstalk between ROS homeostasis and secondary metabolism in S. natalensis ATCC27448: Modulation of pimaricin production by intracellular ROS. PLoS One 6: e27472.
14. Wietzorrek A, Bibb M, (1997) A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold. Mol Microbiol 25: 1177-1184.
15. De Schrijver A, De Mot R, (1999) A subfamily of MalT-related ATP-dependent regulators in the LuxR family. Microbiology 145: 1287-1288.
16. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, et al. (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21: 526-531.
17. Liu G, Tian Y, Yang H, Tan H, (2005) A pathway-specific transcriptional regulatoy gene for nikkomycin biosynthesis in Streptomyces ansochromogenes that also influences coloy development. Mol Microbiol 55: 1855-1866.
18. Li R, Xie Z, Tian Y, Yang H, Chen W, et al. (2009) polR, a pathway-specific transcriptional regulatory gene, positively controls polyoxin biosynthesis in Streptomyces cacaoi subsp. asoensis. Microbiology 155: 1819-1831.
19. Li R, Liu G, Xie Z, He X, Chen W, et al. (2010) PolY, a transcriptional regulator with ATPase activity, directly activates transcription of polR in polyoxin biosynthesis in Streptomyces cacaoi. Mol Microbiol 75: 349-364.
20. Mizuno T, Tanaka I, (1997) Structure of the DNA-binding domain of the OmpR family of response regulators. Mol Microbiol 24: 665-667.
21. Pérez-Rueda E, Collado-Vides J, (2000) The repertoire of DNA-binding transcriptional regulators in Escherichia coli K-12. Nucleic Acids Res 28: 1838-1847.
22. Sekurova ON, Brautaset T, Sletta H, Borgos SEF, Jakobsen OM, et al. (2004) In vivo analysis of the regulatory genes in the nystatin biosynthetic gene cluster of Streptomyces noursei ATCC 11455 reveals their differential control over antibiotic biosynthesis. J Bacteriol 186: 1345-1354.
23. Carmody M, Byrne B, Murphy B, Breen C, Lynch S, et al. (2004) Analysis and manipulation of amphotericin biosynthetic genes by means of modified phage KC515 transduction techniques. Gene 343: 107-115.
24. Guerra SM, Rodriguez-García A, Santos-Aberturas J, Vicente CM, Payero TD, et al. (2012) LAL regulators SCO0877 and SCO7173 as pleiotropic modulators of phosphate starvation response and actinorhodin biosynthesis in Streptomyces coelicolor. PLoS One 7: e31475.
25. Antón N, Santos-Aberturas J, Mendes MV, Guerra SM, Martín JF, et al. (2007) PimM, a PAS domain positive regulator of pimaricin biosynthesis in Streptomyces natalensis. Microbiology 53: 3174-3183.
26. Hefti MH, Francoijs K-J, de Vries SC, Dixon R, Vervoort J, (2004) The PAS fold. A redefinition of the PAS domain based upon structural prediction. Eur J Biochem 271: 1198-1208.
27. Santos-Aberturas J, Vicente CM, Guerra SM, Payero TD, Martín JF, et al. (2011) Molecular control of polyene macrolide biosynthesis: direct binding of the regulator PimM to eight promoters of pimaricin genes and identification of binding boxes. J Biol Chem 286: 9150-9161.
28. Santos-Aberturas J, Payero TD, Vicente CM, Guerra SM, Cañibano C, et al. (2011) Functional conservation of PAS-LuxR transcriptional regulators in polyene macrolide biosynthesis. Metab Eng 13: 756-767.
29. He X, Li R, Pan Y, Liu G, Tan H, (2010) SanG, a transcriptional activator, controls nikkomycin biosynthesis through binding to the sanN-sanO intergenic region in Streptomyces ansochromogenes. Microbiology 156: 828-837.
30. Bourn WR, Babb B, (1995) Computer assisted identification and classification of streptomycete promoters. Nucleic Acids Res 23: 3696-3703.
31. Tang L, Grimm A, Zhang YX, Hutchinson CR, (1996) Purification and characterization of the DNA-binding protein DnrI, a transcriptional factor of daunorubicin biosynthesis in Streptomyces peucetius. Mol Microbiol 22: 801-813.
32. Arias P, Fernández-Moreno MA, Malpartida F, (1999) Characterization of the pathway-specific positive transcriptional regulator for actinorhodin biosynthesis in Streptomyces coelicolor A3 (2) as a DNA-binding protein. J Bacteriol 181: 6958-6968.
33. Tanaka A, Takano Y, Ohnishi Y, Horinouchi S, (2007) AfsR recruits RNA polymerase to the afsS promoter: a model for transcriptional activation by SARPs. J Mol Biol 369: 322-333.
34. Wilkinson CJ, Hughes-Thomas ZA, Martin CJ, Böhm I, Mironenko T, et al. (2002) Increasing the efficiency of heterologous promoters in actinomycetes. J Mol Microbiol Biotechnol 4: 417-426.
35. Browning DF, Busby SJ, (2004) The regulation of bacterial transcription initiation. Nat Rev Microbiol 2: 57-65.
36. Bate N, Stratigopoulos G, Cundliffe E, (2002) Differential roles of two SARP-encoding regulatory genes during tylosin biosynthesis. Mol Microbiol 43: 449-458.
37. Jang BY, Hwang YI, Choi SU, (2011) Effects of pimM and pimR on the Increase of Natamycin Production in Streptomyces natalensis. J Korean Soc Appl Bi 54: 141-144.
38. Du YL, Li SZ, Zhou Z, Chen SF, Fan WM, et al. (2011) The pleitropic regulator AdpAch is required for natamycin biosynthesis and morphological differentiation in Streptomyces chattanoogensis. Microbiology 157: 1300-1311.
39. Aparicio JF, Colina AJ, Ceballos E, Martín JF, (1999) The biosynthetic gene cluster for the 26-membered ring polyene macrolide pimaricin: A new polyketide synthase organization encoded by two subclusters separated by functionalization genes. J Biol Chem 274: 10133-10139.
40. Bierman M, Logan R, O'Brien K, Seno ET, Rao RN, et al. (1992) Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43-49.
41. Sambrook J, Russell DW, (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor, N. Y. Cold Spring Harbor Laboratory Press.
42. Enríquez LL, Mendes MV, Antón N, Tunca S, Guerra SM, et al. (2006): An efficient gene transfer system for the pimaricin producer Streptomyces natalensis. FEMS Microbiol Lett 257: 312-318.
43. 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.
44. Recio E, Aparicio JF, Rumbero A, Martín JF, (2006) Glycerol, ethylene glycol and propanediol elicit pimaricin biosynthesis in the PI-factor defective strain Streptomyces natalensis npi287 and increase polyene production in several wild type actinomycetes. Microbiology 152: 3147-3156.
45. Mendes MV, Tunca S, Antón N, Recio E, Sola-Landa A, et al. (2007) The two-component phoR-phoP system of Streptomyces natalensis: Inactivation or deletion of phoP reduces the negative phosphate regulation of pimaricin biosynthesis. Metab Eng 9: 217-227.
46. Hertz GZ, Stormo GD, (1999) Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15: 563-577.
47. van Helden J, (2003) Regulatory sequence analysis tools. Nucleic Acids Res 31: 3593-3596.
48. Tunca S, Barreiro C, Coque JJ, Martín JF, (2009) Two overlapping antiparallel genes encoding the iron regulator DmdR1 and the Adm proteins control siderophore and antibiotic biosynthesis in Streptomyces coelicolor A3(2). FEBS J 276: 4814-4827.
49. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, et al. (2006) The RIN: an RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7: 3.
50. Rozen S, Skaletsky HJ, (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics Methods and Protocols: Methods in Molecular Biology Humana Press, Totowa, NJ pp. 365-386.
51. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
52. Pfaffl MW, Horgan GW, Dempfle L, (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36.
53. Rasmussen R, (2000) Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K, editors. Rapid Cycle Real-Time PCR, Methods and Applications Springer Press, Heidelberg pp. 21-34.