A new salicylate synthase AmS is identified for siderophores biosynthesis in Amycolatopsis methanolica 239T

Applied Microbiology and Biotechnology

Volumn 99, Issue 14, 2015, Pages 5895-5905

  Xie, Feng ^a,b   Dai, Shengwang ^b,c   Shen, Jinzhao ^b   Ren, Biao ^b,d   Huang, Pei ^b   Wang, Qiushui ^b   Liu, Xueting ^b   Zhang, Buchang ^c   Dai, Huanqin ^b   Zhang, Lixin ^a,b,c  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF MICROBIOLOGY   (China)

^c ANHUI UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

Author keywords

Amycolatopsis; Biochemical properties; Drug target; Salicylate synthase; Siderophore

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; CATALYST ACTIVITY; METABOLITES; SOAPS (DETERGENTS);

AMYCOLATOPSIS; BIOCHEMICAL PROPERTIES; DRUG TARGETS; SALICYLATE SYNTHASE; SIDEROPHORES;

IRON;

AMS PROTEIN; CHORISMIC ACID; CYSTEINE; IRON; METAL ION; ORGANIC SOLVENT; SALICYLIC ACID; SIDEROPHORE; SYNTHETASE; UNCLASSIFIED DRUG; LYASE; SALICYLATE SYNTHETASE; SALICYLIC ACID DERIVATIVE;

AMINO ACID; BACTERIUM; BIOCHEMICAL COMPOSITION; CATALYSIS; CHELATING AGENT; DRUG; ENZYME ACTIVITY; GROWTH RATE; IRON; PHYLOGENETICS; SECONDARY METABOLITE; SIDEROPHORE; TEMPERATURE EFFECT;

ACTINOBACTERIA; AMINO ACID SEQUENCE; AMYCOLATOPSIS METHANOLICA; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL STRAIN; BIOSYNTHESIS; CATALYSIS; CONTROLLED STUDY; ENZYMATIC ASSAY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME SPECIFICITY; ESCHERICHIA COLI; IN VITRO STUDY; MOLECULAR CLONING; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PHYLOGENETIC TREE; REACTION ANALYSIS; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TEMPERATURE; BIOTRANSFORMATION; CHEMISTRY; DNA SEQUENCE; ENZYME STABILITY; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE HOMOLOGY;

AMYCOLATOPSIS; AMYCOLATOPSIS METHANOLICA;

ACTINOBACTERIA; BIOTRANSFORMATION; CHORISMIC ACID; ENZYME STABILITY; HYDROGEN-ION CONCENTRATION; KINETICS; LYASES; MOLECULAR SEQUENCE DATA; PHYLOGENY; SALICYLATES; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SIDEROPHORES; SUBSTRATE SPECIFICITY; TEMPERATURE;

EID: 84932195745     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6370-7     Document Type: Article

References (48)

1. Allen R, Popat R, Diggle S, Brown S (2014) Targeting virulence: can we make evolution-proof drugs? Nat Rev Microbiol 12(4):300–308
2. Altschul S, Madden T, Schäffer A, Zhang J, Zhang Z, Miller W, Lipman D (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402
3. Andrianantoandro E, Basu S, Karig DK, Weiss R (2006) Synthetic biology: new engineering rules for an emerging discipline. Mol Syst Biol 2:2006.0028. doi:10.1038/msb4100073
4. Ashforth EJ, Fu C, Liu X, Dai H, Song F, Guo H, Zhang L (2010) Bioprospecting for antituberculosis leads from microbial metabolites. Nat Prod Rep 27(11):1709–1719. doi:10.1039/c0np00008f
5. Atsumi S, Hanai T, Liao JC (2008) Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels. Nature 451(7174):86–89. doi:10.1038/nature06450
6. Bedford MR, Ford SJ, Horniblow RD, Iqbal TH, Tselepis C (2013) Iron chelation in the treatment of cancer: a new role for deferasirox? J Clin Pharmacol 53(9):885–891. doi:10.1002/jcph.113
7. Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
8. Cappellini MD (2007) Exjade(R) (deferasirox, ICL670) in the treatment of chronic iron overload associated with blood transfusion. Ther Clin Risk Manag 3(2):291–299
9. Chi G, Manos-Turvey A, O'Connor P, Johnston J, Evans G, Baker E, Payne R, Lott J, Bulloch E (2012) Implications of binding mode and active site flexibility for inhibitor potency against the salicylate synthase from Mycobacterium tuberculosis. Biochemistry 51(24):4868–4879
10. de Boer L, Dijkhuizen L, Grobben G, Goodfellow M, Stackebrandt E, Parlett JH, Whitehead D, Witt D (1990) Amycolatopsis methanolica sp. nov., a facultatively methylotrophic actinomycete. Int J Syst Bacteriol 40(2):194–204
11. Demain A, Zhang L (2005) Natural products: drug discovery and therapeutics medicines. Humana, Totowa
12. Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KL, Keasling JD (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27(8):753–759. doi:10.1038/nbt.1557
13. Endy D (2005) Foundations for engineering biology. Nature 438(7067):449–453. doi:10.1038/nature04342
14. Harrison A, Yu M, Gårdenborg T, Middleditch M, Ramsay R, Baker E, Lott J (2006) The structure of MbtI from Mycobacterium tuberculosis, the first enzyme in the biosynthesis of the siderophore mycobactin, reveals it to be a salicylate synthase. J Bacteriol 188(17):6081–6091
15. Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27(5):637–657. doi:10.1039/b906679a
16. Kerbarh O, Chirgadze D, Blundell T, Abell C (2006) Crystal structures of Yersinia enterocolitica salicylate synthase and its complex with the reaction products salicylate and pyruvate. J Mol Biol 357(2):524–534
17. Kerbarh O, Ciulli A, Howard N, Abell C (2005) Salicylate biosynthesis: overexpression, purification, and characterization of Irp9, a bifunctional salicylate synthase from Yersinia enterocolitica. J Bacteriol 187(15):5061–5066
18. Kieser T, Mervyn J, Bibb MJ (2000) Practical streptomyces genetics. The John Innes Foundation Press, Norwich
19. Kim B, Sahin N, Tan GY, Zakrzewska-Czerwinska J, Goodfellow M (2002) Amycolatopsis eurytherma sp. nov., a thermophilic actinomycete isolated from soil. Int J Syst Evol Microbiol 52(Pt 3):889–894
20. Lawlor M, O'connor C, Miller V (2007) Yersiniabactin is a virulence factor for Klebsiella pneumoniae during pulmonary infection. Infect Immun 75(3):1463–1472
21. Li J, Guo Z, Huang W, Meng X, Ai G, Tang G, Chen Y (2013) Mining of a streptothricin gene cluster from Streptomyces sp. TP-A0356 genome via heterologous expression. Sci China Life Sci 56(7):619–627. doi:10.1007/s11427-013-4504-2
22. Manos-Turvey A, Bulloch E, Rutledge P, Baker E, Lott J, Payne R (2010) Inhibition studies of Mycobacterium tuberculosis salicylate synthase (MbtI). ChemMedChem 5(7):1067–1079
23. Manos-Turvey A, Cergol K, Salam N, Bulloch E, Chi G, Pang A, Britton W, West N, Baker E, Lott J, Payne R (2012) Synthesis and evaluation of M. tuberculosis salicylate synthase (MbtI) inhibitors designed to probe plasticity in the active site. Org Biomol Chem 10(46):9223–9236
24. Marisa CK, Norma JT, Christopher TS, Andrea MS, Paul AB (1995) Chorismate-utilizing enzymes isochorismate synthase, anthranilate synthase, and p-aminobenzoate synthase: mechanistic insight through inhibitor design. J Am Chem Soc 117(8):2128–2140
25. Matthew FT, Mohammad RS, Jon C, Roberto K (2012) Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 86(3):628–644
26. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev: MMBR 71(3):413–451. doi:10.1128/mmbr. 00012-07
27. Niu G, Tan H (2013) Biosynthesis and regulation of secondary metabolites in microorganisms. Sci China Life Sci 56(7):581–583. doi:10.1007/s11427-013-4501-5
28. Pan W, Kang Q, Wang L, Bai L, Deng Z (2013) Asm8, a specific LAL-type activator of 3-amino-5-hydroxybenzoate biosynthesis in ansamitocin production. Sci China Life Sci 56(7):601–608. doi:10.1007/s11427-013-4502-4
29. Payne R, Kerbarh O, Miguel R, Abell A, Abell C (2005) Inhibition studies on salicylate synthase. Org Biomol Chem 3(10):1825–1827
30. Quadri L (2007) Strategic paradigm shifts in the antimicrobial drug discovery process of the 21st century. Infect Disord Drug Targets 7(3):230–237
31. Ratledge C (2004) Iron, mycobacteria and tuberculosis. Tuberculosis 84:110–130
32. Ratledge C, Dover L (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941
33. Saha R, Saha N, Donofrio RS, Bestervelt LL (2013) Microbial siderophores: a mini review. J Basic Microbiol 53(4):303–317. doi:10.1002/jobm.201100552
34. Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Lab Press, Cold Spring Harbor
35. Seyedsayamdost M, Traxler M, Zheng S, Kolter R, Clardy J (2011) Structure and biosynthesis of amychelin, an unusual mixed-ligand siderophore from Amycolatopsis sp. AA4. J Am Chem Soc 133(30):11434–11437
36. Skaar E (2010) The battle for iron between bacterial pathogens and their vertebrate hosts. PLoS Pathog 6(8):e1000949
37. Sridharan S, Howard N, Kerbarh O, Błaszczyk M, Abell C, Blundell T (2010) Crystal structure of Escherichia coli enterobactin-specific isochorismate synthase (EntC) bound to its reaction product isochorismate: implications for the enzyme mechanism and differential activity of chorismate-utilizing enzymes. J Mol Biol 397(1):290–300
38. Staunton J, Wilkinson B (2001) Combinatorial biosynthesis of polyketides and nonribosomal peptides. Curr Opin Chem Biol 5(2):159–164
39. Traxler MF, Watrous JD, Alexandrov T, Dorrestein PC, Kolter R (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. mBio 4(4) doi:10.1128/mBio.00459-13
40. Vasan M, Neres J, Williams J, Wilson D, Teitelbaum A, Remmel R, Aldrich C (2010) Inhibitors of the salicylate synthase (MbtI) from Mycobacterium tuberculosis discovered by high-throughput screening. ChemMedChem 5(12):2079–2087
41. Xu L, Huang H, Wei W, Zhong Y, Tang B, Yuan H, Zhu L, Huang W, Ge M, Yang S, Zheng H, Jiang W, Chen D, Zhao GP, Zhao W (2014) Complete genome sequence and comparative genomic analyses of the vancomycin-producing Amycolatopsis orientalis. BMC Genomics 15:363. doi:10.1186/1471-2164-15-363
42. Zhang L, Yan K, Zhang Y, Huang R, Bian J, Zheng C, Sun H, Chen Z, Sun N, An R, Min F, Zhao W, Zhuo Y, You J, Song Y, Yu Z, Liu Z, Yang K, Gao H, Dai H, Zhang X, Wang J, Fu C, Pei G, Liu J, Zhang S, Goodfellow M, Jiang Y, Kuai J, Zhou G, Chen X (2007) High-throughput synergy screening identifies microbial metabolites as combination agents for the treatment of fungal infections. Proc Natl Acad Sci U S A 104(11):4606–4611. doi:10.1073/pnas.0609370104
43. Zhang T, Zhuo Y, Jia X, Liu J, Gao H, Song F, Liu M, Zhang L (2013) Cloning and characterization of the gene cluster required for beauvericin biosynthesis in Fusarium proliferatum. Sci China Life Sci 56(7):628–637. doi:10.1007/s11427-013-4505-1
44. Zhao W, Zhong Y, Yuan H, Wang J, Zheng H, Wang Y, Cen X, Xu F, Bai J, Han X, Lu G, Zhu Y, Shao Z, Yan H, Li C, Peng N, Zhang Z, Zhang Y, Lin W, Fan Y, Qin Z, Hu Y, Zhu B, Wang S, Ding X, Zhao GP (2010) Complete genome sequence of the rifamycin SV-producing Amycolatopsis mediterranei U32 revealed its genetic characteristics in phylogeny and metabolism. Cell Res 20(10):1096–1108. doi:10.1038/cr.2010.87
45. Zhong X, Tian Y, Niu G, Tan H (2013) Assembly and features of secondary metabolite biosynthetic gene clusters in Streptomyces ansochromogenes. Sci China Life Sci 56(7):609–618. doi:10.1007/s11427-013-4506-0
46. Zhuo Y, Liu L, Wang Q, Liu X, Ren B, Liu M, Ni P, Cheng YQ, Zhang L (2012) Revised genome sequence of Burkholderia thailandensis MSMB43 with improved annotation. J Bacteriol 194(17):4749–4750. doi:10.1128/jb.00931-12
47. Ziebart K, Toney M (2010) Nucleophile specificity in anthranilate synthase, aminodeoxychorismate synthase, isochorismate synthase, and salicylate synthase. Biochemistry 49(13):2851–2859
48. Zwahlen J, Kolappan S, Zhou R, Kisker C, Tonge P (2007) Structure and mechanism of MbtI, the salicylate synthase from Mycobacterium tuberculosis. Biochemistry 46(4):954–964