Total biosynthesis and diverse applications of the nonribosomal peptide-polyketide siderophore yersiniabactin

Applied and Environmental Microbiology

Volumn 81, Issue 16, 2015, Pages 5290-5298

  Ahmadi, Mahmoud Kamal ^a   Fawaz, Samar ^a   Jones, Charles H ^a   Zhang, Guojian ^a   Pfeifer, Blaine A ^a  

^a the State University of New York   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; ESCHERICHIA COLI; KETONES; PEPTIDES;

BIOLOGICAL SOLUTIONS; DIVERSE APPLICATIONS; NONRIBOSOMAL PEPTIDE; NONRIBOSOMAL PEPTIDE SYNTHETASES; PARALLEL APPLICATION; POLYKETIDE SYNTHASES; POTENTIAL UTILITY; REMOVAL CAPACITY;

BIOSYNTHESIS;

BACTERIUM; BIOTECHNOLOGY; CATALYSIS; CHELATION; COPPER; ENZYME ACTIVITY; IRON; METABOLITE; PATHOGEN; PEPTIDE; SIDEROPHORE;

ESCHERICHIA COLI; YERSINIA PESTIS;

COPPER; IRON; PHENOL DERIVATIVE; THIAZOLE DERIVATIVE; YERSINIABACTIN;

BIOSYNTHESIS; BIOTECHNOLOGY; ESCHERICHIA COLI; GENETICS; METABOLIC ENGINEERING; METABOLISM; PROCEDURES;

BIOSYNTHETIC PATHWAYS; BIOTECHNOLOGY; COPPER; ESCHERICHIA COLI; IRON; METABOLIC ENGINEERING; PHENOLS; THIAZOLES;

EID: 84937899255     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01373-15     Document Type: Article

References (47)

1. Braun V, Killmann H. 1999. Bacterial solutions to the iron-supply problem. Trends Biochem Sci 24:104-109. http://dx.doi.org/10.1016/S0968-0004(99)01359-6.
2. Miethke M, Marahiel MA. 2007. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413-451. http://dx.doi.org /10.1128/MMBR.00012-07.
3. Ratledge C, Dover LG. 2000. Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881-941. http://dx.doi.org/10.1146/annurev.micro.54.1.881.
4. Caza M, Kronstad JW. 2013. Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol 3:80. http://dx.doi.org/10.3389/fcimb.2013.00080.
5. Haas H, Eisendle M, Turgeon BG. 2008. Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46:149-187. http://dx.doi .org/10.1146/annurev.phyto.45.062806.094338.
6. Garenaux A, Caza M, Dozois CM. 2011. The ins and outs of siderophore mediated iron uptake by extra-intestinal pathogenic Escherichia coli. Vet Microbiol 153:89-98. http://dx.doi.org/10.1016/j.vetmic.2011.05.023.
7. Muller SI, Valdebenito M, Hantke K. 2009. Salmochelin, the longoverlooked catecholate siderophore of Salmonella. Biometals 22:691-695. http://dx.doi.org/10.1007/s10534-009-9217-4.
8. Drechsel H, Stephan H, Lotz R, Haag H, Zahner H, Hantke K, Jung G. 1995. Structural elucidation of yersiniabactin, a siderophore from highly virulent Yersinia strains. Liebigs Ann 10:1727-1733.
9. Haag H, Hantke K, Drechsel H, Stojiljkovic I, Jung G, Zahner H. 1993. Purification of yersiniabactin: a siderophore and possible virulence factor of Yersinia enterocolitica. J Gen Microbiol 139:2159-2165. http://dx.doi .org/10.1099/00221287-139-9-2159.
10. Perry RD, Balbo PB, Jones HA, Fetherston JD, DeMoll E. 1999. Yersiniabactin from Yersinia pestis: biochemical characterization of the siderophore and its role in iron transport and regulation. Microbiology 145:1181-1190. http://dx.doi.org/10.1099/13500872-145-5-1181.
11. Wallner A, Blatzer M, Schrettl M, Sarg B, Lindner H, Haas H. 2009. Ferricrocin, a siderophore involved in intra-and transcellular iron distribution in Aspergillus fumigatus. Appl Environ Microbiol 75:4194-4196. http://dx.doi.org/10.1128/AEM.00479-09.
12. Crosa JH, Walsh CT. 2002. Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223-249. http://dx.doi.org/10.1128/MMBR.66.2.223-249.2002.
13. Cane DE, Walsh CT, Khosla C. 1998. Harnessing the biosynthetic code:combinations, permutations, and mutations. Science 282:63-68. http://dx.doi.org/10.1126/science.282.5386.63.
14. Du L, Sanchez C, Shen B. 2001. Hybrid peptide-polyketide natural products: biosynthesis and prospects toward engineering novel molecules. Metab Eng 3:78-95. http://dx.doi.org/10.1006/mben.2000.0171.
15. Menzella HG, Reeves CD. 2007. Combinatorial biosynthesis for drug development. Curr Opin Microbiol 10:238-245. http://dx.doi.org/10.1016/j.mib.2007.05.005.
16. Zhang H, Boghigian BA, Armando J, Pfeifer BA. 2011. Methods and options for the heterologous production of complex natural products. Nat Prod Rep 28:125-151. http://dx.doi.org/10.1039/C0NP00037J.
17. Ongley SE, Bian X, Neilan BA, Muller R. 2013. Recent advances in the heterologous expression of microbial natural product biosynthetic pathways. Nat Prod Rep 30:1121-1138. http://dx.doi.org/10.1039/c3np70034h.
18. Pfeifer BA, Wang CC, Walsh CT, Khosla C. 2003. Biosynthesis of Yersiniabactin, a complex polyketide-nonribosomal peptide, using Escherichia coli as a heterologous host. Appl Environ Microbiol 69:6698-6702. http://dx.doi.org/10.1128/AEM.69.11.6698-6702.2003.
19. de Carvalho CC, Marques MP, Fernandes P. 2011. Recent achievements on siderophore production and application. Recent Pat Biotechnol 5:183-198. http://dx.doi.org/10.2174/187220811797579114.
20. Ahmed E, Holmstrom SJ. 2014. Siderophores in environmental research:roles and applications. Microb Biotechnol 7:196-208. http://dx.doi.org /10.1111/1751-7915.12117.
21. Schalk IJ, Hannauer M, Braud A. 2011. New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844-2854. http://dx.doi.org/10.1111/j.1462-2920.2011.02556.x.
22. Braud A, Hannauer M, Mislin GL, Schalk IJ. 2009. The Pseudomonas aeruginosa pyochelin-iron uptake pathway and its metal specificity. J Bacteriol 191:3517-3525. http://dx.doi.org/10.1128/JB.00010-09.
23. Chaturvedi KS, Hung CS, Crowley JR, Stapleton AE, Henderson JP. 2012. The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat Chem Biol 8:731-736. http://dx.doi.org/10.1038/nchembio.1020.
24. Chaturvedi KS, Hung CS, Giblin DE, Urushidani S, Austin AM, Dinauer MC, Henderson JP. 2014. Cupric yersiniabactin is a virulenceassociated superoxide dismutase mimic. ACS Chem Biol 9:551-561. http://dx.doi.org/10.1021/cb400658k.
25. Reynolds HV, Talekar CR, Bellapart J, Leggett BA, Boots RJ. 2014. Copper removal strategies for Wilson's disease crisis in the ICU. Anaesth Intensive Care 42:253-257.
26. Gateau C, Delangle P. 2014. Design of intrahepatocyte copper(I) chelators as drug candidates for Wilson's disease. Ann N Y Acad Sci 1315:30-36. http://dx.doi.org/10.1111/nyas.12379.
27. Brewer GJ. 2012. Metals in the causation and treatment of Wilson's disease and Alzheimer's disease, and copper lowering therapy in medicine. Inorg Chim Acta 393:135-141. http://dx.doi.org/10.1016/j.ica.2012.06.014.
28. Pfeifer BA, Admiraal SJ, Gramajo H, Cane DE, Khosla C. 2001. Biosynthesis of complex polyketides in a metabolically engineered strain of E. coli. Science 291:1790-1792. http://dx.doi.org/10.1126/science.1058092.
29. Pelludat C, Brem D, Heesemann J. 2003. Irp9, encoded by the highpathogenicity island of Yersinia enterocolitica, is able to convert chorismate into salicylate, the precursor of the siderophore yersiniabactin. J Bacteriol 185:5648-5653. http://dx.doi.org/10.1128/JB.185.18.5648-5653.2003.
30. Jones AM, Lindow SE, Wildermuth MC. 2007. Salicylic acid, yersiniabactin, and pyoverdin production by the model phytopathogen Pseudomonas syringae pv. tomato DC3000: synthesis, regulation, and impact on tomato and Arabidopsis host plants. J Bacteriol 189:6773-6786. http://dx.doi.org/10.1128/JB.00827-07.
31. Sabel CE, Neureuther JM, Siemann S. 2010. A spectrophotometric method for the determination of zinc, copper, and cobalt ions in metalloproteins using Zincon. Anal Biochem 397:218-226. http://dx.doi.org/10.1016/j.ab.2009.10.037.
32. Jones CH, Ravikrishnan A, Chen M, Reddinger R, Kamal Ahmadi M, Rane S, Hakansson AP, Pfeifer BA. 2014. Hybrid biosynthetic gene therapy vector development and dual engineering capacity. Proc Natl Acad Sci U S A 111:12360-12365. http://dx.doi.org/10.1073/pnas .1411355111.
33. Kerbarh O, Chirgadze DY, Blundell TL, Abell C. 2006. Crystal structures of Yersinia enterocolitica salicylate synthase and its complex with the reaction products salicylate and pyruvate. J Mol Biol 357:524-534. http://dx .doi.org/10.1016/j.jmb.2005.12.078.
34. Kerbarh O, Ciulli A, Howard NI, Abell C. 2005. Salicylate biosynthesis:overexpression, purification, and characterization of Irp9, a bifunctional salicylate synthase from Yersinia enterocolitica. J Bacteriol 187:5061-5066. http://dx.doi.org/10.1128/JB.187.15.5061-5066.2005.
35. Neres J, Wilson DJ, Celia L, Beck BJ, Aldrich CC. 2008. Aryl acid adenylating enzymes involved in siderophore biosynthesis: fluorescence polarization assay, ligand specificity, and discovery of non-nucleoside inhibitors via high-throughput screening. Biochemistry 47:11735-11749. http://dx.doi.org/10.1021/bi801625b.
36. Wurst JM, Drake EJ, Theriault JR, Jewett IT, VerPlank L, Perez JR, Dandapani S, Palmer M, Moskowitz SM, Schreiber SL, Munoz B, Gulick AM. 2014. Identification of inhibitors of PvdQ, an enzyme involved in the synthesis of the siderophore pyoverdine. ACS Chem Biol 9:1536-1544. http://dx.doi.org/10.1021/cb5001586.
37. Oh SJ, Cook DC, Townsend HE. 1998. Characterization of iron oxides commonly formed as corrosion products on steel. Hyperfine Interact 112:59-65. http://dx.doi.org/10.1023/A:1011076308501.
38. Argo J. 1981. A qualitative test for iron corrosion products. Stud Conserv 26:140-142.
39. Cervini-Silva J, Sposito G. 2002. Steady-state dissolution kinetics of aluminum-goethite in the presence of desferrioxamine-B and oxalate ligands. Environ Sci Technol 36:337-342. http://dx.doi.org/10.1021/es010901n.
40. Reichard PU, Kraemer SM, Frazier SW, Kretzschmar R. 2005. Goethite dissolution in the presence of phytosiderophores: rates, mechanisms, and the synergistic effect of oxalate. Plant Soil 276:115-132. http://dx.doi.org /10.1007/s11104-005-3504-9.
41. Dhungana S, Anthony CR, Hersman LE. 2007. Effect of exogenous reductant on growth and iron mobilization from ferrihydrite by the Pseudomonas mendocina ymp strain. Appl Environ Microbiol 73:3428-3430. http://dx.doi.org/10.1128/AEM.02586-06.
42. Dehner CA, Awaya JD, Maurice PA, DuBois JL. 2010. Roles of siderophores, oxalate, and ascorbate in mobilization of iron from hematite by the aerobic bacterium Pseudomonas mendocina. Appl Environ Microbiol 76:2041-2048. http://dx.doi.org/10.1128/AEM.02349-09.
43. Flora SJ, Pachauri V. 2010. Chelation in metal intoxication. Int J Environ Res Public Health 7:2745-2788. http://dx.doi.org/10.3390/ijerph7072745.
44. Agarwal S, Ferreira AE, Santos SMC, Reis MTA, Ismael MRC, Correia MJN, Carvalho JMR. 2010. Separation and recovery of copper from zinc leach liquor by solvent extraction using Acorga M5640. Int J Miner Process 97:85-91. http://dx.doi.org/10.1016/j.minpro.2010.08.009.
45. Zhu Z, Zhang W, Pranolo Y, Cheng CY. 2012. Separation and recovery of copper, nickel, cobalt and zinc in chloride solutions by synergistic solvent extraction. Hydrometallurgy 127:1-7.
46. Zhang XJ, Li XG, Cao HB, Zhang Y. 2010. Separation of copper, iron (III), zinc and nickel from nitrate solution by solvent extraction using LK-C2. Sep Purif Technol 70:306-313. http://dx.doi.org/10.1016/j.seppur.2009.10.012.
47. Seelig MS. 1982. Auto-immune complications of D-penicillamine-a possible result of zinc and magnesium depletion and of pyridoxine inactivation. JAmColl Nutr 1:207-214. http://dx.doi.org/10.1080/07315724.1982.10718989.