Unsaturated macrocyclic dihydroxamic acid siderophores produced by shewanella putrefaciens using precursor-directed biosynthesis

ACS Chemical Biology

Volumn 9, Issue 4, 2014, Pages 945-956

  Soe, Cho Z ^a   Codd, Rachel ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 2 BUTENE; ALKENE DERIVATIVE; COORDINATION COMPOUND; DIAMINE; DIHYDROXAMIC ACID; FERRIC ION; LIGAND; MACROCYCLIC COMPOUND; ORNITHINE DECARBOXYLASE; PUTREBACTENE; PUTREBACTIN; PUTRESCINE; SIDEROPHORE; UNCLASSIFIED DRUG; ALCALIGIN; BISUCABERIN; CYCLOPEPTIDE; HYDROXAMIC ACID; SUCCINIC ACID DERIVATIVE;

ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BIOSYNTHESIS; CHEMICAL BOND; CONTROLLED STUDY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SHEWANELLA PUTREFACIENS; SOLUBILITY; ANALOGS AND DERIVATIVES; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM;

CHROMATOGRAPHY, LIQUID; HYDROXAMIC ACIDS; MACROCYCLIC COMPOUNDS; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PEPTIDES, CYCLIC; PUTRESCINE; SHEWANELLA PUTREFACIENS; SIDEROPHORES; SUCCINATES;

EID: 84899047339     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400901j     Document Type: Article

References (70)

1. Raymond, K. N., Müller, G., and Matzanke, B. F. (1984) Complexation of iron by siderophores. A review of their solution and structural chemistry and biological function, in Structural Chemistry (Boschke, F. L., Ed.) pp 49-102, Springer-Verlag, Berlin.
2. Hider, R. C. and Kong, X. (2010) Chemistry and biology of siderophores Nat. Prod. Rep. 27, 637-657
3. Budzikiewicz, H. (2010) Microbial siderophores, in Progress in the Chemistry of Organic Natural Products (Kinghorn, A. D., Falk, H., and Kobayashi, J., Eds.) pp 1-75, Springer-Verlag, New York.
4. Dhungana, S. and Crumbliss, A. L. (2005) Coordination chemistry and redox processes in siderophore-mediated iron transport Geomicrobiol. J. 22, 87-98
5. Winkelmann, G. and Drechsel, H. (1997) Microbial siderophores, in Products of Secondary Metabolism (Kleinkauf, H. and von Döhren, H., Eds.) pp 199-246, VCH, Weinheim.
6. Neilands, J. B. (1995) Siderophores: structure and function of microbial iron transport compounds J. Biol. Chem. 270, 26723-26726
7. Butler, A. (2003) Iron acquisition: straight up and on the rocks? Nat. Struct. Biol. 10, 240-241
8. Boukhalfa, H. and Crumbliss, A. L. (2002) Chemical aspects of siderophore mediated iron transport BioMetals 15, 325-339
9. Crumbliss, A. L. and Harrington, J. M. (2009) Iron sequestration by small molecules: thermodynamic and kinetic studies of natural siderophores and synthetic model complexes Adv. Inorg. Chem. 61, 179-250
10. Miethke, M. (2013) Molecular strategies of microbial iron assimilation: from high-affinity complexes to cofactor assembly systems Metallomics 5, 15-28
11. Raymond, K. N. and Dertz, E. A. (2004) Biochemical and physical properties of siderophores, in Iron Transport in Bacteria (Crosa, J. H., Mey, A. R., and Payne, S. M., Eds.) pp 3-17, ASM Press, Washington, DC.
12. Schwarzenbach, G. and Schwarzenbach, K. (1963) Hydroxamate complexes. I. The stabilities of the iron(III) complexes of simple hydroxamic acids and desferriferrioxamine B Helv. Chim. Acta 46, 1390-1400
13. Evers, A., Hancock, R. D., Martell, A. E., and Motekaitis, R. J. (1989) Metal ion recognition in ligands with negatively charged oxygen donor groups. Complexation of Fe(III), Ga(III), In(III), Al(III), and other highly charged metal ions Inorg. Chem. 28, 2189-2195
14. Bernhardt, P. V. (2007) Coordination chemistry and biology of chelators for the treatment of iron overload disorders Dalton Trans. 3214-3220
15. Kalinowski, D. S. and Richardson, D. R. (2005) The evolution of iron chelators for the treatment of iron overload disease and cancer Pharmacol. Rev. 57, 547-583
16. Schalk, I. J., Hannauer, M., and Braud, A. (2011) New roles for bacterial siderophores in metal transport and tolerance Environ. Microbiol. 13, 2844-2854
17. Miller, M. J., Zhu, H., Xu, Y., Wu, C., Walz, A. J., Vergne, A., Roosenberg, J. M., Moraski, G., Minnick, A. A., McKee-Dolence, J., Hu, J., Fennell, K., Dolence, E. K., Dong, L., Franzblau, S., Malouin, F., and Mollmann, U. (2009) Utilization of microbial iron assimilation processes for the development of new antibiotics and inspiration for the design of new anticancer agents BioMetals 22, 61-75
18. Girijavallabhan, V. and Miller, M. J. (2004) Therapeutic uses of iron(III) chelators and their antimicrobial conjugates, in Iron Transport in Bacteria (Crosa, J. H., Mey, A. R., and Payne, S. M., Eds.) pp 413-433, ASM Press, Washington, DC.
19. Marmion, C. J., Griffith, D., and Nolan, K. B. (2004) Hydroxamic acids. An intriguing family of enzyme inhibitors and biomedical ligands Eur. J. Inorg. Chem. 3003-3016
20. Codd, R. (2008) Traversing the coordination chemistry and chemical biology of hydroxamic acids Coord. Chem. Rev. 252, 1387-1408
21. Casentini, B. and Pettine, M. (2010) Effects of desferrioxamine-B on the release of arsenic from volcanic rocks Appl. Geochem. 25, 1688-1698
22. Liu, J., Obando, D., Schipanski, L. G., Groebler, L. K., Witting, P. K., Kalinowski, D. S., Richardson, D. R., and Codd, R. (2010) Conjugates of desferrioxamine B (DFOB) with derivatives of adamantane or with orally available chelators as potential agents for treating iron overload J. Med. Chem. 53, 1370-1382
23. Liddell, J. R., Obando, D., Liu, J., Ganio, G., Volitakis, I., Mok, S. S., Crouch, P. J., White, A. R., and Codd, R. (2013) Lipophilic adamantyl- or deferasirox-based conjugates of desferrioxamine B have enhanced neuroprotective capacity: implications for Parkinson disease Free Radical Biol. Med. 60, 147-156
24. Kondani, S., Bicz, J., Song, L., Deeth, R. J., Ohnishi-Kameyama, M., Yoshida, M., Ochi, K., and Challis, G. L. (2013) Structure and biosynthesis of scabichelin, a novel tris-hydroxamate siderophore produced by the plant pathogen Streptomyces scabies 87.22 Org. Biomol. Chem. 11, 4686-4694
25. Zane, H. K. and Butler, A. (2013) Isolation, structure elucidation, and iron-binding properties of lystabactins, siderophores isolated from a marine Pseudoaltermonas sp J. Nat. Prod. 76, 648-654
26. Ejje, N., Soe, C. Z., Gu, J., and Codd, R. (2013) The variable hydroxamic acid siderophore metabolome of the marine actinomycete Salinispora tropica CNB-440 Metallomics 5, 1519-1528
27. D'Onofrio, A., Crawford, J. M., Stewart, E. J., Witt, K., Gavrish, E., Epstein, S., Clardy, J., and Lewis, K. (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria Chem. Biol. 17, 254-264
28. Yang, Y.-L., Xu, Y., Kersten, R. D., Liu, W.-T., Meehan, M. J., Moore, B. S., Bandeira, N., and Dorrestein, P. C. (2011) Connecting chemotypes and phenotypes of cultured marine microbial assemblages by imaging mass spectrometry Angew. Chem., Int. Ed. 50, 5839-5942
29. Sidebottom, A. M., Johnson, A. R., Karty, J. A., Trader, D. J., and Carlson, E. E. (2013) Integrated metabolomics approach facilitates discovery of an unpredicted natural product suite from Streptomyces coelicolor M145 ACS Chem. Biol. 8, 2009-2016
30. Gauglitz, J. M. and Butler, A. (2013) Amino acid variability in the peptide composition of a suite of amphiphilic peptide siderophores from an open ocean Vibrio species J. Biol. Inorg. Chem. 18, 489-497
31. Meiwes, J., Fiedler, H.-P., Zähner, H., Konetschny-Rapp, S., and Jung, G. (1990) Production of desferrioxamine E and new analogues by directed fermentation and feeding fermentation Appl. Microbiol. Biotechnol. 32, 505-510
32. Feistner, G. J. (1995) Proferrioxamine synthesis in Erwinia amylovora in response to precursor or hydroxylysine feeding: metabolic profiling with liquid chromatography-electrospray mass spectrometry BioMetals 8, 318-327
33. Tschierske, M., Drechsel, H., Jung, G., and Zähner, H. (1996) Production of rhizoferrin and new analogues obtained by directed fermentation Appl. Microbiol. Biotechnol. 45, 664-670
34. Konetschny-Rapp, S., Jung, G., Raymond, K. N., Meiwes, J., and Zaehner, H. (1992) Solution thermodynamics of the ferric complexes of new desferrioxamine siderophores obtained by directed fermentation J. Am. Chem. Soc. 114, 2224-2230
35. Venkateswaran, K., Moser, D. P., Dollhopf, M. E., Lies, D. P., Saffarini, D. A., MacGregor, B. J., Ringelberg, D. B., White, D. C., Nishijima, M., Sano, H., Burghardt, J., Stackebrandt, E., and Nealson, K. H. (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov Int. J. Syst. Bacteriol. 49, 705-724
36. Fredrickson, J. K., Romine, M. F., Beliaev, A. S., Auchtung, J. M., Driscoll, M. E., Gardner, T. S., Nealson, K. H., Osterman, A. L., Pinchuk, G., Reed, J. L., Rodionov, D. A., Rodrigues, J. L. M., Saffarini, D. A., Serres, M. H., Spormann, A. M., Zhulin, I. B., and Tiedje, J. M. (2008) Towards environmental systems biology of Shewanella Nat. Rev. Microbiol. 6, 592-603
37. Konstantinidis, K. T., Serres, M. H., Romine, M. F., Rodrigues, J. L. M., Auchtung, J., McCue, L.-A., Lipton, M. S., Obraztsova, A., Giometti, C. S., Nealson, K. H., Fredrickson, J. K., and Tiedje, J. M. (2009) Comparative systems biology across an evolutionary gradient within the Shewanella genus Proc. Natl. Acad. Sci. U.S.A. 106, 15909-15914
38. Bagge, D., Hjelm, M., Johansen, C., Huber, I., and Gram, L. (2001) Shewanella putrefaciens Adhesion and biofilm formation on food processing surfaces Appl. Environ. Microbiol. 67, 2319-2325
39. Tiedje, J. M. (2002) Shewanella-the environmentally versatile genome Nat. Biotechnol. 20, 1093-1095
40. Ledyard, K. M. and Butler, A. (1997) Structure of putrebactin, a new dihydroxamate siderophore produced by Shewanella putrefaciens J. Biol. Inorg. Chem. 2, 93-97
41. Pakchung, A. A. H., Soe, C. Z., and Codd, R. (2008) Studies of iron-uptake mechanisms in two bacterial species of the Shewanella genus adapted to middle-range (Shewanella putrefaciens) or Antarctic (Shewanella gelidimarina) temperatures Chem. Biodivers. 5, 2113-2123
42. Pakchung, A. A. H., Soe, C. Z., Lifa, T., and Codd, R. (2011) Complexes formed in solution between vanadium(IV)/(V) and the cyclic dihydroxamic acid putrebactin or linear suberodihydroxamic acid Inorg. Chem. 50, 5978-5989
43. Soe, C. Z., Pakchung, A. A. H., and Codd, R. (2012) Directing the biosynthesis of putrebactin or desferrioxamine B in Shewanella putrefaciens through the upstream inhibition of ornithine decarboxylase Chem. Biodivers. 9, 1880-1890
44. Takahashi, A., Nakamura, H., Kameyama, T., Kurasawa, S., Naganawa, H., Okami, Y., Takeuchi, T., and Umezawa, H. (1987) Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. II. Physico-chemical properties and structure determination J. Antibiot. 40, 1671-1676
45. Kameyama, T., Takahashi, A., Kurasawa, S., Ishizuka, M., Okami, Y., Takeuchi, T., and Umezawa, H. (1987) Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. I. Taxonomy of the producing organism, isolation and biological properties J. Antibiot. 40, 1664-1670
46. Winkelmann, G., Schmid, D. G., Nicholson, G., Jung, G., and Colquhoun, D. J. (2002) Bisucaberin-a dihydroxamate siderophore isolated from Vibrio salmonicida, an important pathogen of farmed Atlantic salmon (Salmo salar) BioMetals 15, 153-160
47. Nishio, T., Tanaka, N., Hiratake, J., Katsube, Y., Ishida, Y., and Oda, J. (1988) Isolation and structure of the novel dihydroxamate siderophore alcaligin J. Am. Chem. Soc. 110, 8733-8734
48. Nishio, T. and Ishida, Y. (1990) Production of dihydroxamate siderophore alcaligin by Alcaligenes denitrificans subsp. xylosoxydans Agric. Biol. Chem. 54, 1837-1839
49. Moore, C. H., Foster, L. A., Gerbig, D. G., Jr., Dyer, D. W., and Gibson, B. W. (1995) Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica J. Bacteriol. 177, 1116-1118
50. Bentley, S. D., Chater, K. F., Cerdec̃o-Tárraga, A.-M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H., Harper, D., Bateman, A., Brown, S., Chandra, G., Chen, C. W., Collins, M., Cronin, A., Fraser, A., Goble, A., Hidalgo, J., Hornsby, T., Howarth, S., Huang, C.-H., Kieser, T., Larke, L., Murphy, L., Oliver, K., O'Neil, S., Rabbinowitsch, E., Rajandream, M.-A., Rutherford, K., Rutter, S., Seeger, K., Saunders, D., Sharp, S., Squares, R., Squares, S., Taylor, K., Warren, T., Wietzorrek, A., Woodward, J., Barrell, B. G., Parkhill, J., and Hopwood, D. A. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) Nature 417, 141-147
51. Challis, G. L. (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases ChemBioChem 6, 601-611
52. Barry, S. M. and Challis, G. L. (2009) Recent advances in siderophore biosynthesis Curr. Opin. Chem. Biol. 13, 205-215
53. Oves-Costales, D., Kadi, N., and Challis, G. L. (2009) The long-overlooked enzymology of a nonribosomal peptide synthetase-independent pathway for virulence-conferring siderophore biosynthesis Chem. Commun. 6530-6541
54. Barona-Gomez, F., Wong, U., Giannakopulos, A. E., Derrick, P. J., and Challis, G. L. (2004) Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145 J. Am. Chem. Soc. 126, 16282-16283
55. Kadi, N., Oves-Costales, D., Barona-Gomez, F., and Challis, G. L. (2007) A new family of ATP-dependent oligomerization-macrocyclization biocatalysts Nat. Chem. Biol. 3, 652-656
56. Kadi, N., Arbache, S., Song, L., Oves-Costales, D., and Challis, G. L. (2008) Identification of a gene cluster that directs putrebactin biosynthesis in Shewanella species: PubC catalyzes cyclodimerization of N -hydroxy- N -succinylputrescine J. Am. Chem. Soc. 130, 10458-10459
57. Kadi, N., Song, L., and Challis, G. L. (2008) Bisucaberin biosynthesis: an adenylating domain of the BibC multi-enzyme catalyzes cyclodimerization of N-hydroxy-N-succinylcadaverine Chem. Commun. 5119-5121
58. Brickman, T. J. and Armstrong, S. K. (1996) The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: Putrescine is a precursor of alcaligin J. Bacteriol. 178, 54-60
59. Weeks, C. E., Herrmann, A. L., Nelson, F. R., and Slaga, T. J. (1982) α-Difluoromethylornithine, an irreversible inhibitor of ornithine decarboxylase, inhibits tumor promotor-induced polyamine accumulation and carcinogenesis in mouse skin Proc. Natl. Acad. Sci. U.S.A. 79, 6028-6032
60. Bergeron, R. J. and McManis, J. S. (1989) The total synthesis of bisucaberin Tetrahedron 45, 4939-4944
61. Bergeron, R. J., McManis, J. S., Perumal, P. T., and Algee, S. E. (1991) The total synthesis of alcaligin J. Org. Chem. 56, 5560-5563
62. Braich, N. and Codd, R. (2008) Immobilized metal affinity chromatography for the capture of hydroxamate-containing siderophores and other Fe(III)-binding metabolites from bacterial culture supernatants Analyst 133, 877-880
63. Schwyn, B. and Neilands, J. B. (1987) Universal chemical assay for the detection and determination of siderophores Anal. Biochem. 160, 47-56
64. Shah, P. and Swiatlo, E. (2008) A multifaceted role for polyamines in bacterial pathogens Mol. Microbiol. 68, 4-16
65. Crumbliss, A. L. (1991) Aqueous solution equilibrium and kinetic studies of iron siderophore and model siderophore complexes, in Handbook of Microbial Iron Chelates (Winkelmann, G., Ed.) pp 172-233, CRC, Boca Raton.
66. Spasojevic, I., Boukhalfa, H., Stevens, R. D., and Crumbliss, A. L. (2001) Aqueous solution speciation of Fe(III) complexes with dihydroxamate siderophores alcaligin and rhodotorulic acid and synthetic analogues using electrospray ionization mass spectrometry Inorg. Chem. 40, 49-58
67. Pakchung, A. A. H., Lifa, T., and Codd, R. (2013) Solution species of Fe(III), Ga(III), In(III) or Ln(III) and suberodihydroxamic acid from electrospray ionization mass spectrometry RSC Adv. 3, 16051-16059
68. Hou, Z., Sunderland, C. J., Nishio, T., and Raymond, K. N. (1996) Preorganization of ferric alcaligin, Fe2L3. The first structure of a ferric dihydroxamate siderophore J. Am. Chem. Soc. 118, 5148-5149
69. Salamci, E., Seçen, H., Sütbeyaz, Y., and Balci, M. (1997) A concise and convenient synthesis of DL- proto -quercitol and DL- gala -quercitol via ene reaction of singlet oxygen combined with [2 + 4] cycloaddition to cyclohexadiene J. Org. Chem. 62, 2453-2457
70. Bataille, C. J. R. and Donohoe, T. J. (2011) Osmium-free direct syn -dihydroxylation of alkenes Chem. Soc. Rev. 40, 114-128