JBIC Journal of Biological Inorganic Chemistry

, Volume 23, Issue 7, pp 969–982 | Cite as

The chemical biology and coordination chemistry of putrebactin, avaroferrin, bisucaberin, and alcaligin

  • Rachel CoddEmail author
  • Cho Zin Soe
  • Amalie A. H. Pakchung
  • Athavan Sresutharsan
  • Christopher J. M. Brown
  • William Tieu
Part of the following topical collections:
  1. Alison Butler: Papers in Celebration of Her 2018 ACS Alfred Bader Award in Bioorganic or Bioinorganic Chemistry


Dihydroxamic acid macrocyclic siderophores comprise four members: putrebactin (putH2), avaroferrin (avaH2), bisucaberin (bisH2), and alcaligin (alcH2). This mini-review collates studies of the chemical biology and coordination chemistry of these macrocycles, with an emphasis on putH2. These Fe(III)-binding macrocycles are produced by selected bacteria to acquire insoluble Fe(III) from the local environment. The macrocycles are optimally pre-configured for Fe(III) binding, as established from the X-ray crystal structure of dinuclear [Fe2(alc)3] at neutral pH. The dimeric macrocycles are biosynthetic products of two endo-hydroxamic acid ligands flanked by one amine group and one carboxylic acid group, which are assembled from 1,4-diaminobutane and/or 1,5-diaminopentane as initial substrates. The biosynthesis of alcH2 includes an additional diamine C-hydroxylation step. Knowledge of putH2 biosynthesis supported the use of precursor-directed biosynthesis to generate unsaturated putH2 analogues by culturing Shewanella putrefaciens in medium supplemented with unsaturated diamine substrates. The X-ray crystal structures of putH2, avaH2 and alcH2 show differences in the relative orientations of the amide and hydroxamic acid functional groups that could prescribe differences in solvation and other biological properties. Functional differences have been borne out in biological studies. Although evolved for Fe(III) acquisition, solution coordination complexes have been characterised between putH2 and oxido-V(IV/V), Mo(VI), or Cr(V). Retrosynthetic analysis of 1:1 complexes of [Fe(put)]+, [Fe(ava)]+, and [Fe(bis)]+ that dominate at pH < 5 led to a forward metal-templated synthesis approach to generate the Fe(III)-loaded macrocycles, with apo-macrocycles furnished upon incubation with EDTA. This mini-review aims to capture the rich chemistry and chemical biology of these seemingly simple compounds.

Graphical abstract


Siderophores Hydroxamic acid macrocycles Putrebactin Precursor-directed biosynthesis Metal-templated synthesis 



Alison Butler and Kathleen M. Ledyard are acknowledged for the discovery of putrebactin, which has fuelled a significant amount of research activity in our group and others. Alison Butler is also acknowledged for her generosity in sharing her expertise and passion for siderophore chemistry and her effective style of mentoring and support of scientists in the US and beyond. Alison Butler and Thomas Böttcher are kindly acknowledged for providing the X-ray structure coordinates for putH2 and avaH2, respectively. This work was supported by the Australian Research Council (ARC DP140100092) and the Australian Commonwealth Government (Australian Postgraduate Awards to A.S. and C.J.M.B.). The University of Sydney is acknowledged for funding (co-funded Postgraduate Scholarship to C.Z.S. and to A.A.H.P.).


  1. 1.
    Ledyard KM, Butler A (1997) Structure of putrebactin, a new dihydroxamate siderophore produced by Shewanella putrefaciens. J Biol Inorg Chem 2:93–97CrossRefGoogle Scholar
  2. 2.
    Codd R, Astashkin AV, Pacheco A, Raitsimring AM, Enemark JH (2002) Pulsed ELDOR spectroscopy of the Mo(V)/Fe(III) state of sulfite oxidase prepared by one-electron reduction with Ti(III) citrate. J Biol Inorg Chem 7:338–350CrossRefGoogle Scholar
  3. 3.
    Baars O, Zhang Z, Morel FMM, Seyedsayamdost MR (2016) The siderophore metabolome of Azotobacter vinelandii. Appl Environ Microbiol 82:27–39CrossRefGoogle Scholar
  4. 4.
    Butler A (2003) Iron acquisition: straight up and on the rocks? Nat Struct Biol 10:240–241CrossRefGoogle Scholar
  5. 5.
    Sandy M, Butler A (2009) Microbial iron acquisition: marine and terrestrial siderophores. Chem Rev 109:4580–4595CrossRefGoogle Scholar
  6. 6.
    Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657CrossRefGoogle Scholar
  7. 7.
    Stintzi A, Raymond KN (2001) Siderophore chemistry. In: Templeton DE (ed) Molecular and cellular iron transport. Marcel Dekker, New York, pp 273–319Google Scholar
  8. 8.
    Dertz EA, Raymond KN (2004) Siderophores and transferrins. In: McCleverty JA, Meyer TJ (eds) Comprehensive Coordination chemistry II. Elsevier Pergamon, Boston, pp 141–168Google Scholar
  9. 9.
    Albrecht-Gary A-M, Crumbliss AL (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release. In: Sigel A, Sigel H (eds) Metal ions in biological systems. Marcel Dekker, Inc., New York, pp 239–327Google Scholar
  10. 10.
    Raymond KN, Dertz EA (2004) Biochemical and physical properties of siderophores. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, DC, pp 3–17CrossRefGoogle Scholar
  11. 11.
    Crosa JH, Walsh CT (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66:223–249CrossRefGoogle Scholar
  12. 12.
    Gram L (1994) Siderophore-mediated iron sequestering by Shewanella putrefaciens. Appl Environ Microbiol 60:2132–2136PubMedPubMedCentralGoogle Scholar
  13. 13.
    Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258CrossRefGoogle Scholar
  14. 14.
    Nealson KH, Scott J (2006) Ecophysiology of the genus Shewanella. In: Dworkin M (ed) The Prokaryotes. Springer, New York, pp 1133–1151CrossRefGoogle Scholar
  15. 15.
    Taillefert M, Beckler JS, Carey E, Burns JL, Fennessey CM, DiChristina TJ (2007) Shewanella putrefaciens produces an Fe(III)-solubilizing organic ligand during anaerobic respiration on insoluble Fe(III) oxides. J Inorg Biochem 101:1760–1767CrossRefGoogle Scholar
  16. 16.
    Fennessey CM, Jones ME, Taillefert M, DiChristina TJ (2010) Siderophores are not involved in Fe(III) solubilization during anaerobic Fe(III) respiration by Shewanella oneidensis MR-1. Appl Environ Microbiol 76:2425–2432CrossRefGoogle Scholar
  17. 17.
    Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451CrossRefGoogle Scholar
  18. 18.
    Miethke M (2013) Molecular strategies of microbial iron assimilation: from high-affinity complexes to cofactor assembly systems. Metallomics 5:15–28CrossRefGoogle Scholar
  19. 19.
    Takahashi A, Nakamura H, Kameyama T, Kurasawa S, Naganawa H, Okami Y, Takeuchi T, Umezawa H (1987) Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage-mediated cytolysis. II. Physico-chemical properties and structure determination. J Antibiot 40:1671–1676CrossRefGoogle Scholar
  20. 20.
    Kameyama T, Takahashi A, Kurasawa S, Ishizuka M, Okami Y, Takeuchi T, 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 40:1664–1670CrossRefGoogle Scholar
  21. 21.
    Winkelmann G, Schmid DG, Nicholson G, Jung G, Colquhoun DJ (2002) Bisucaberin—a dihydroxamate siderophore isolated from Vibrio salmonicida, an important pathogen of farmed Atlantic salmon (Salmo salar). Biometals 15:153–160CrossRefGoogle Scholar
  22. 22.
    Senges CHR, Al-Dilaimi A, Marchbank DH, Wibberg D, Winkler A, Haltli B, Nowrousian M, Kalinowski J, Kerr RG, Bandow JE (2018) The secreted metabolome of Streptomyces chartreusis and implications for bacterial chemistry. Proc Natl Acad Sci USA 115:2490–2495CrossRefGoogle Scholar
  23. 23.
    Nishio T, Tanaka N, Hiratake J, Katsube Y, Ishida Y, Oda J (1988) Isolation and structure of the novel dihydroxamate siderophore alcaligin. J Am Chem Soc 110:8733–8734CrossRefGoogle Scholar
  24. 24.
    Brickman TJ, Hansel J-G, Miller MJ, Armstrong SK (1996) Purification, spectroscopic analysis and biological activity of the macrocyclic dihydroxamate siderophore alcaligin produced by Bordetella pertussis and Bordetella bronchiseptica. Biometals 9:191–203CrossRefGoogle Scholar
  25. 25.
    Moore CH, Foster LA, Gerbig DG Jr, Dyer DW, Gibson BW (1995) Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica. J Bacteriol 177:1116–1118CrossRefGoogle Scholar
  26. 26.
    Brickman TJ, Armstrong SK (2010) Iron uptake systems in pathogenic Bordetella. In: Cornelis P, Andrews SC (eds) Iron uptake and homeostasis in microorganisms. Caister Academic Press, UK, pp 65–86Google Scholar
  27. 27.
    Brickman TJ, Anderson MT, Armstrong SK (2007) Bordetella iron transport and virulence. Biometals 20:303–322CrossRefGoogle Scholar
  28. 28.
    Soe CZ, Pakchung AAH, Codd R (2012) Directing the biosynthesis of putrebactin or desferrioxamine B in Shewanella putrefaciens through the upstream inhibition of ornithine decarboxylase. Chem Biodivers 9:1880–1890CrossRefGoogle Scholar
  29. 29.
    Böttcher T, Clardy J (2014) A chimeric siderophore halts swarming Vibrio. Angew Chem Int Ed 53:3510–3513CrossRefGoogle Scholar
  30. 30.
    Watrous JD, Roach P, Heath B, Alexandrov T, Laskin J, Dorrestein PC (2013) Metabolic profiling directly from the Petri dish using nanospray desorption electrospray ionization imaging mass spectrometry. Anal Chem 85:10385–10391CrossRefGoogle Scholar
  31. 31.
    Bowman JP, McCammon SA, Nichols DS, Skerratt JS, Rea SM, Nichols PD, McMeekin TA (1997) Shewanella gelidimarina sp. nov. and Shewanella frigidimarina sp. nov., novel species with the ability to produce eicosapenataenoic acid (20:5w3) and grow anaerobically with dissimilatory Fe(III) reduction. Int J Syst Bacteriol 47:1040–1047CrossRefGoogle Scholar
  32. 32.
    Pakchung AAH, Soe CZ, 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 5:2113–2123CrossRefGoogle Scholar
  33. 33.
    Martinez JS, Zhang GP, Holt PD, Jung PD, Jung H-T, Carrano CJ, Haygood MG, Butler A (2000) Self-assembling amphiphilic siderophores from marine bacteria. Science 287:1245–1247CrossRefGoogle Scholar
  34. 34.
    Xu G, Martinez JS, Groves JT, Butler A (2002) Membrane affinity of the amphiphilic marinobactin siderophores. J Am Chem Soc 124:13408–13415CrossRefGoogle Scholar
  35. 35.
    Martinez JS, Carter-Franklin JN, Mann EL, Martin JD, Haygood MG, Butler A (2003) Structure and membrane affinity of a suite of amphiphilic siderophores produced by a marine bacterium. Proc Natl Acad Sci USA 100:3754–3759CrossRefGoogle Scholar
  36. 36.
    Martin JD, Ito Y, Homann VV, Haygood MG, Butler A (2006) Structure and membrane affinity of new amphiphilic siderophores produced by Ochrobactrum sp. SP18. J Biol Inorg Chem 11:633–641CrossRefGoogle Scholar
  37. 37.
    Zhang G, Amin SA, Küpper FC, Holt PD, Carrano CJ, Butler A (2009) Ferric stability constants of representative marine siderophores: marinobactins, aquachelins, and petrobactin. Inorg Chem 48:11466–11473CrossRefGoogle Scholar
  38. 38.
    Butler A, Theisen RM (2010) Iron(III)-siderophore coordination chemistry: reactivity of marine siderophores. Coord Chem Rev 254:288–296CrossRefGoogle Scholar
  39. 39.
    Challis GL (2005) A widely distributed bacterial pathway for siderophore biosynthesis independent of nonribosomal peptide synthetases. ChemBioChem 6:601–611CrossRefGoogle Scholar
  40. 40.
    Rütschlin S, Gunesch S, Böttcher T (2017) One enzyme, three metabolites: Shewanella algae controls siderophore production via the cellular substrate pool. Cell Chem Biol 24:598–604CrossRefGoogle Scholar
  41. 41.
    Rütschlin S, Gunesch S, Böttcher T (2018) One enzyme to build them all: ring-size engineered siderophores inhibit the swarming motility of Vibrio. ACS Chem Biol 13:1153–1158CrossRefGoogle Scholar
  42. 42.
    Barona-Gómez F, Wong U, Giannakopulos AE, Derrick PJ, Challis GL (2004) Identification of a cluster of genes that directs desferrioxamine biosynthesis in Streptomyces coelicolor M145. J Am Chem Soc 126:16282–16283CrossRefGoogle Scholar
  43. 43.
    Kadi N, Oves-Costales D, Barona-Gómez F, Challis GL (2007) A new family of ATP-dependent oligomerization-macrocyclization biocatalysts. Nat Chem Biol 3:652–656CrossRefGoogle Scholar
  44. 44.
    Oves-Costales D, Kadi N, Challis GL (2009) The long-overlooked enzymology of a nonribosomal peptide synthetase-independent pathway for virulence-conferring siderophore biosynthesis. Chem Commun. CrossRefGoogle Scholar
  45. 45.
    Kadi N, Arbache S, Song L, Oves-Costales D, Challis GL (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 130:10458–10459CrossRefGoogle Scholar
  46. 46.
    Kadi N, Song L, Challis GL (2008) Bisucaberin biosynthesis: an adenylating domain of the BibC multi-enzyme catalyzes cyclodimerization of N-hydroxy-N-succinylcadaverine. Chem Commun. CrossRefGoogle Scholar
  47. 47.
    Giardina PC, Foster LA, Toth SI, Roe BA, Dyer DW (1995) Identification of alcA, a Bordetella bronchiseptica gene necessary for alcaligin production. Gene 167:133–136CrossRefGoogle Scholar
  48. 48.
    Kang HY, Brickman TJ, Beaumont FC, Armstrong SK (1996) Identification and characterization of iron-regulated Bordetella pertussis alcaligin biosynthesis genes. J Bacteriol 178:4877–4884CrossRefGoogle Scholar
  49. 49.
    Brickman TJ, Armstrong SK (1996) The ornithine decarboxylase gene odc is required for alcaligin siderophore biosynthesis in Bordetella spp.: putrescine is a precursor of alcaligin. J Bacteriol 178:54–60CrossRefGoogle Scholar
  50. 50.
    Giardina PC, Foster L-A, Toth SI, Roe BA, Dyer DW (1997) Analysis of the alcABC operon encoding alcaligin biosynthesis enzymes in Bordetella bronchiseptica. Gene 194:19–24CrossRefGoogle Scholar
  51. 51.
    Kang HY, Armstrong SK (1998) Transcriptional analysis of the Bordetella alcaligin siderophore biosyntheiss operon. J Bacteriol 180:855–861PubMedPubMedCentralGoogle Scholar
  52. 52.
    Li B, Lowe-Power T, Kurihara S, Gonzales S, Naidoo J, MacMillan JB, Allen C, Michael AJ (2016) Functional identification of putrescine C- and N-hydroxylases. ACS Chem Biol 11:2782–2789CrossRefGoogle Scholar
  53. 53.
    Soe CZ, Codd R (2014) Unsaturated macrocyclic dihydroxamic acid siderophores produced by Shewanella putrefaciens using precursor-directed biosynthesis. ACS Chem Biol 9:945–956CrossRefGoogle Scholar
  54. 54.
    Soe CZ, Telfer TJ, Levina A, Lay PA, Codd R (2016) Simultaneous biosynthesis of putrebactin, avaroferrin and bisucaberin by Shewanella putrefaciens and characterisation of complexes with iron(III), molybdenum(VI) or chromium(V). J Inorg Biochem 162:207–215CrossRefGoogle Scholar
  55. 55.
    Hirschmann M, Grundmann F, Bode HB (2017) Identification and occurrence of the hydroxamate siderophores aerobactin, putrebactin, avaroferrin and ochrobactin C as virulence factors from entomopathogenic bacteria. Environ Microbiol 19:4080–4090CrossRefGoogle Scholar
  56. 56.
    Fujita MJ, Kimura N, Yokose H, Otsuka M (2012) Heterologous production of bisucaberin using a biosynthetic gene cluster cloned from a deep sea metagenome. Mol BioSyst 8:482–485CrossRefGoogle Scholar
  57. 57.
    Fujita MJ, Sakai R (2014) Production of avaroferrin and putrebactin by heterologous expression of a deep-sea metagenomic DNA. Mar Drugs 12:4799–4809CrossRefGoogle Scholar
  58. 58.
    Hou Z, Sunderland CJ, Nishio T, Raymond KN (1996) Preorganization of ferric alcaligin, Fe2L3. The first structure of a ferric dihydroxamate siderophore. J Am Chem Soc 118:5148–5149CrossRefGoogle Scholar
  59. 59.
    Hou Z, Raymond KN, O’Sullivan B, Esker TW, Nishio T (1998) A preorganized siderophore: thermodynamic and structural characterization of alcaligin and bisucaberin, microbial macrocyclic dihydroxamate chelating agents. Inorg Chem 37:6630–6637CrossRefGoogle Scholar
  60. 60.
    Carrano CJ, Raymond KN (1978) Coordination chemistry of microbial iron transport compounds. 10. Characterization of the complexes of rhodotorulic acid, a dihydroxamate siderophore. J Am Chem Soc 100:5371–5374CrossRefGoogle Scholar
  61. 61.
    Carrano CJ, Cooper SR, Raymond KN (1979) Coordination chemistry of microbial iron transport compounds. 11. Solution equilibriums and electrochemistry of ferric rhodotorulate complexes. J Am Chem Soc 101:599–604CrossRefGoogle Scholar
  62. 62.
    Boukhalfa H, Brickman TJ, Armstrong SK, Crumbliss AL (2000) Kinetics and mechanism of iron(III) dissociation from the dihydroxamic siderophores alcaligin and rhodotorulic acid. Inorg Chem 39:5591–5602CrossRefGoogle Scholar
  63. 63.
    Springer SD, Butler A (2015) Magnetic susceptibility of Mn(III) complexes of hydroxamate siderophores. J Inorg Biochem 148:22–26CrossRefGoogle Scholar
  64. 64.
    Kouzuma A, Hashimoto KKW (2012) Roles of siderophore in manganese-oxide reduction by Shewanella oneidensis MR-1. FEMS Microbiol Lett 326:91–98CrossRefGoogle Scholar
  65. 65.
    Lin H, Szeinbaum NH, DiChristina TJ, Taillefert M (2012) Microbial Mn(IV) reduction requires an initial one-electron reductive solubilization step. Geochim Cosmochim Acta 99:179–192CrossRefGoogle Scholar
  66. 66.
    Duckworth OW, Sposito G (2005) Siderophore-manganese(III) interactions. II. Manganite dissolution promoted by desferrioxamine B. Environ Sci Technol 39:6045–6051CrossRefGoogle Scholar
  67. 67.
    Saal LB, Duckworth OW (2010) Synergistic dissolution of manganese oxides as promoted by sideorphores and small organic acids. Soil Sci Soc Am J 74:2021–2031CrossRefGoogle Scholar
  68. 68.
    Faulkner KM, Stevens RD, Fridovich I (1994) Characterization of Mn(III) complexes of linear and cyclic desferrioxamines as mimics of superoxide dismutase activity. Arch Biochem Biophys 310:341–346CrossRefGoogle Scholar
  69. 69.
    Duckworth OW, Sposito G (2005) Siderophore-manganese(III) interactions. I. Air-oxidation of manganese(II) promoted by desferrioxamine B. Environ Sci Technol 39:6037–6044CrossRefGoogle Scholar
  70. 70.
    Spasojevic I, Boukhalfa H, Stevens RD, Crumbliss AL (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 40:49–58CrossRefGoogle Scholar
  71. 71.
    Sresutharsan A, Tieu W, Richardson-Sanchez T, Soe CZ, Codd R (2017) Dimeric and trimeric homo- and heteroleptic hydroxamic acid macrocycles formed using mixed-ligand Fe(III)-based metal-templated synthesis. J Inorg Biochem 177:344–351CrossRefGoogle Scholar
  72. 72.
    Abbasi S (1976) Extraction and spectrophotometric determination of vanadium(V) with N-[p-(N, N-dimethylanilino)-3-methoxy-2-naphtho]hydroxamic acid. Anal Chem 48:714–717CrossRefGoogle Scholar
  73. 73.
    Pande KR, Tandon SG (1980) A novel method for the isolation of oxo-vanadium(V) complexes of hydroxamic acids. Studies on oxo-chloro-bis-N-phenylbenzohydroxamato-vanadium(V). J Inorg Nucl Chem 42:1509Google Scholar
  74. 74.
    Butler A, Parsons SM, Yamagata SK, de la Rosa RI (1989) Reactivation of vanadate-inhibited enzymes with desferrioxamine B, a vanadium(V) chelator. Inorg Chim Acta 163:1–3CrossRefGoogle Scholar
  75. 75.
    Pakchung AAH, Soe CZ, Lifa T, Codd R (2011) Complexes formed in solution between vanadium(IV)/(V) and the cyclic dihydroxamic acid putrebactin or linear suberodihydroxamic acid. Inorg Chem 50:5978–5989CrossRefGoogle Scholar
  76. 76.
    Caudle MT, Stevens RD, Crumbliss AL (1994) A monomer-to-dimer shift in a series of 1:1 ferric dihydroxamates probed by electrospray mass spectrometry. Inorg Chem 33:6111–6115CrossRefGoogle Scholar
  77. 77.
    Soe CZ, Pakchung AAH, Codd R (2014) Dinuclear [VVO(putrebactin))2(μ-OCH3)2] formed in solution as established from LC–MS measurements using 50V-enriched V2O5. Inorg Chem 53:5852–5861CrossRefGoogle Scholar
  78. 78.
    Fisher DC, Barclay-Peet SJ, Balfe CA, Raymond KN (1989) Synthesis and characterization of vanadium(V) and -(IV) hydroxamate complexes. X-ray crystal structures of oxochlorobis(benzohydroxamato)vanadium(V) and oxoisopropoxo(N, N’-dihydroxy-N, N’-diisopropylheptanediamido)vanadium(V). Inorg Chem 28:4399–4406CrossRefGoogle Scholar
  79. 79.
    Haratake M, Fukunaga M, Ono M, Nakayama M (2005) Synthesis of vanadium(IV, V) hydroxamic acid complexes and in vivo assessment of their insulin-like activity. J Biol Inorg Chem 10:250–258CrossRefGoogle Scholar
  80. 80.
    Rehder D (2013) The future of/for vanadium. Dalton Trans 42:11749–11761CrossRefGoogle Scholar
  81. 81.
    Emerson SR, Huested SS (1991) Ocean anoxia and the concentrations of molybdenum and vanadium in seawater. Mar Chem 34:177–196CrossRefGoogle Scholar
  82. 82.
    Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–210CrossRefGoogle Scholar
  83. 83.
    Springer SD, Butler A (2016) Microbial ligand coordination: consideration of biological significance. Coord Chem Rev 306:628–635CrossRefGoogle Scholar
  84. 84.
    Bergeron RJ, McManis JS (1989) The total synthesis of bisucaberin. Tetrahedron 45:4939–4944CrossRefGoogle Scholar
  85. 85.
    Bergeron RJ, McManis JS, Perumal PT, Algee SE (1991) The total synthesis of alcaligin. J Org Chem 56:5560–5563CrossRefGoogle Scholar
  86. 86.
    Kachadourian R, Chuilon S, Mérienne C, Kunesch G, Deroussent A (1997) A new total synthesis of ferrioxamine E through metal-templated cyclic trimerization. Supramol Chem 8:301–308CrossRefGoogle Scholar
  87. 87.
    Lifa T, Tieu W, Hocking RK, Codd R (2015) Forward and reverse (retro) iron(III)- or gallium(III)-desferrioxamine E and ring-expanded analogs prepared using metal-templated synthesis from endo-hydroxamic acid monomers. Inorg Chem 54:3573–3583CrossRefGoogle Scholar
  88. 88.
    Guérard F, Lee Y-S, Tripier R, Szajek LP, Deschamps JR, Brechbiel MW (2013) Investigation of Zr(IV) and 89Zr(IV) complexation with hydroxamates: progress towards designing a better chelator than desferrioxamine B for immuno-PET imaging. Chem Commun 49:1002–1004CrossRefGoogle Scholar
  89. 89.
    Holland JP, Vasdev N (2014) Charting the mechanism and reactivity of zirconium oxalate with hydroxamate ligands using density functional theory: implications in new chelate design. Dalton Trans 43:9872–9884CrossRefGoogle Scholar
  90. 90.
    Tieu W, Lifa T, Katsifis A, Codd R (2017) Octadentate zirconium(IV)-loaded macrocycles with varied stoichiometry assembled from hydroxamic acid monomers using metal-templated synthesis. Inorg Chem 56:3719–3728CrossRefGoogle Scholar

Copyright information

© SBIC 2018

Authors and Affiliations

  • Rachel Codd
    • 1
    Email author
  • Cho Zin Soe
    • 1
  • Amalie A. H. Pakchung
    • 1
  • Athavan Sresutharsan
    • 1
  • Christopher J. M. Brown
    • 1
  • William Tieu
    • 1
  1. 1.School of Medical Sciences (Pharmacology) and Bosch InstituteThe University of SydneySydneyAustralia

Personalised recommendations