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Bisucaberin – A dihydroxamate siderophore isolated from Vibrio salmonicida, an important pathogen of farmed Atlantic salmon (Salmo salar)

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Abstract

A siderophore of the bacterial fish pathogen, Vibrio salmonicida, was isolated from low-iron culture supernatant and structurally characterized as bisucaberin by FTICR- and FAB-MS, NMR and GC-MS analysis of the hydrolysis products. Although the cyclic dihydroxamate bisucaberin has previously been isolated from a marine bacterium, Alteromonas haloplanktis, its involvement in cold-water vibriosis of Atlantic salmon (Salmon salar) is novel. Bisucaberin production in iron-limited media was highest at temperatures around and below 10 °C, correlating well with temperatures at which outbreaks of cold-water vibriosis occur. Due to the very high stability constant of K = 32.2, bisucaberin is a most efficient iron scavenger which may contribute to the virulence of V. salmonicida in Atlantic salmon.

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References

  • Audi G, Wapstra AH. 1995 Update to the atomic mass evaluation. Nucl Phys A, 595, 409-480.

    Google Scholar 

  • Boukhalfa H, Crumbliss AL. 2002 Chemical aspects of siderophore mediated iron transport. BioMetals (in press).

  • 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, 191-203.

    Google Scholar 

  • Brickman TJ, Armstrong SK. 1999 Essential role of the iron-regulated outer membrane receptor FauA in alcaligin siderophore-mediated iron uptake in Bordetella species. J Bacteriol 181, 5958-5966.

    Google Scholar 

  • Caravatti P, Allemann M. 1991 The infinity cell: a new trapped-ion cell with radiofrequency covered trapping electrodes for Fourier transform ion cyclotron resonance mass spectrometry. Org Mass Spectrom 26, 514-518.

    Google Scholar 

  • Colquhoun DJ, Sørum H. 2001 Temperature dependent siderophore production in Vibrio salmonicida. Microbial pathogen 31, 213-219.

    Google Scholar 

  • Colquhoun DJ, Alvheim K, Dommarsnes K, Sørum H. 2002. Relevance of incubation temperature for Vibrio salmonicida vaccine production. J. Appl. Microbiol. (in press).

  • Crosa JH. 1989 Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev 53, 517-530.

    Google Scholar 

  • Drechsel H, Winkelmann G. 1997 Iron chelation and siderophores. In: Winkelmann G and Carrano CJ, eds. Transition Metals in Microbial Metabolism, Harwood Academic Publishers, Amsterdam, pp. 1-49.

    Google Scholar 

  • Deiss K, Hantke K, Winkelmann G. 1998 Molecular recognition of siderophores: A study with cloned ferrioxamine receptors (FoxA) from Erwinia herbicola and Yersinia enterocolitica. BioMetals 11, 131-137.

    Google Scholar 

  • Dhungana S, White PS, Crumbliss AL. 2001 Crystal structure of ferrioxamine B: comparative analysis and implications for molecular recognition. J Biol Inorg Chem 6, 810-818.

    Google Scholar 

  • Egidius E, Wilk R, Andersen K, Hoff KA, Hjeltnes B. 1986 Vibrio salmonicida sp. nov., a new fish pathogen. Int J Syst Bacteriol 36, 518-520.

    Google Scholar 

  • Fouz B, Toranzo AE, Biosca EC, Mazoy R, Amaro C. 1994 Role of iron in the pathogenicity of Vibrio damsela for fish and mammals. FEMS Microbiol Lett 21, 181-188.

    Google Scholar 

  • Gauthier JW, Trautman TR, Jacobson DB. 1991 Sustained off-resonance irradiation for CAD involving FTMS. Anal Chim Acta 246, 211-225.

    Google Scholar 

  • Griffith GL, Sigel S P, Payne SM, Neilands JB. 1984 Vibriobactin, a siderophore from Vibrio cholerae. J Biol Chem 259, 383-385.

    Google Scholar 

  • Haygood MG, Holt PD, Butler A. 1993 Aerobactin production by planktonic marine Vibrio sp. Limol Oceanogr 38, 1091-1097.

    Google Scholar 

  • Hou Z, Raymond KN, O'Sullivan B, Esker TW. 1998 A preorganized siderophore: Thermodynamic and structural characterization of alcaligin and bisucaberin, microbial macrocyclic dihydroxamate chelating agents. Inorg Chem 37, 6630-6637.

    Google Scholar 

  • Jalal MAF, Hossain MB, van der Helm D, Sanders-Loehr J, Actis LA, Crosa JH. 1989 Structure of anguibactin, a unique plasmid-related bacterial siderophore from the fish pathogen Vibrio anguillarum. J Am Chem Soc 111, 292-296.

    Google Scholar 

  • Marshall AG, Hendrickson CL, Jackson GS. 1998 Fourier transform ion cyclotron resonance mass spectrometry: A primer. Mass Spectrom Rev 17, 1-35.

    Google Scholar 

  • Martinez JS, Haygood MG, Butler A. 2001 Identification of a natural desferrioxamine siderophore produced by a marine bacterium. Limnol Oceanogr 46, 420-424.

    Google Scholar 

  • Moore CH, Foster L-A, Gerbig DG Jr., Dyer DW, Gibson BW. 1995 Identification of alcaligin as the siderophore produced by Bordetella pertussis and B. bronchiseptica. J Bacteriol 177, 1116-1118.

    Google Scholar 

  • Murakami K, Fuse H, Takimura O, Kamimura K, Yamaoka Y. 1998 Phylogenetic analysis of marine environmental strains of Vibrio that produce aerobactin. J Mar Biotechnol 6, 76-79.

    Google Scholar 

  • Nishio T, Tanaka N, Hiratake J, Katsube Y, Ishida Y, Oda J. 1988 Isolation and structure of the novel dihydroxamate siderophore alcaligin. J Chem Soc 110, 8733-8734.

    Google Scholar 

  • Nishio T, Ishida Y. 1990 Production of dihydroxamate siderophore alcaligin by Alcaligenes denitrificans subsp. xylosoxydans. Agric Biol Chem 54, 1837-1839.

    Google Scholar 

  • Okujo N, Saito M, Yamamoto S, Yoshida T, Miyoshi S, Shinoda S. 1994 Structure of vulnibactin, a new polyamine-containing siderophore from Vibrio vulnificus. BioMetals 7, 109-116.

    Google Scholar 

  • Rabsch W, Winkelmann G. 1991 The specificity of bacterial siderophore receptors probed by bioassays. BioMetals 4, 244-250.

    Google Scholar 

  • Register KB, Ducey TF, Brockmeier SL, Dyer DW. 2001 Reduced virulence of a Bordetella bronchiseptica siderophore mutant in neonatal swine. Infect Immun 69, 2137-2143.

    Google Scholar 

  • Reissbrodt R, Rabsch W, Chapeaurouge A, Jung G, Winkelmann G. 1990 Isolation and identification of ferrioxamine G and E in Hafnia alvei. BioMetals 3, 54-60.

    Google Scholar 

  • Schwyn B & Neilands JB 1987 Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160, 47-56.

    Google Scholar 

  • Sebulsky MT, Hohnstein D, Hunter MD, Heinrichs DE. 2000 Identification and characterization of membrane permease involved in iron-hydroxamate transport in Staphylococcus aureus. J Bacteriol 182, 4394-4400.

    Google Scholar 

  • 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 electropsray ionization mass spectrometry. Inorg Chem 40, 49-58.

    Google Scholar 

  • Takahashi A, Nakamura H, Kameyama T, Kurasawa S, Naganawa H, Okami Y, Takeuchi S, Umezawa H. 1987 Bisucaberin, a new siderophore, sensitizing tumor cells to macrophage mediated cytolysis. II Physico-chemical properties and structure determination. J Antibiotics 40, 1671-1676.

    Google Scholar 

  • Wertheimer AM, Verweij W, Chen Q, Crosa LM, Nagasawa M, Tolmasky ME, Actis LA, Crosa JH. 1999 Characterization of the angR gene of Vibrio anguillarum: Essential role in virulence. Infect Immun 67, 6496-6509.

    Google Scholar 

  • Wolf MK, Crosa JH. 1986 Evidence for a role of a siderophore in promoting Vibrio anguillarum infection. J Gen Microbiol 132, 2949-2952.

    Google Scholar 

  • Yamamoto S, Fujita Y, Okujo N, Matsuura S, Shinoda S. 1992 Isolation and partial characterization of a compound with siderophore activity from V. parahaemolyticus. FEMS Microbiol Lett 94, 181-186.

    Google Scholar 

  • Yamamoto S, Okujo N, Fujita Y, Saito M, Yoshida T, Shinoda, S. 1993a Structures of two polyamine containing catecholate siderophores from Vibrio fluvialis. J Biochem 113, 538-544.

    Google Scholar 

  • Yamamoto S, Okujo N, Yoshida T, Matsuura S, Shinoda, S. 1993b Structure and iron transport activity of vibrioferrin, a new siderophore of Vibrio parahaemolyticus. J Biochem 115, 868-874.

    Google Scholar 

  • Yamamoto S, Okuio N, Sakakibara Y. 1994 Isolation and structure elucidation of acinetobactin, a novel siderophore from Acinetobacter baumannii. Arch Microbiol 162, 249-254.

    Google Scholar 

  • Young IG, Gibson F. 1979 Isolation of enterochelin from Escherichia coli. Methods Enzymol 56, 394-398.

    Google Scholar 

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Authors and Affiliations

  1. Institut für Mikrobiologie und Biotechnologie, Universität Tübingen, Auf der Morgenstelle 28, D-72076, Tübingen, Germany

    Günther Winkelmann

  2. Institut für Organische Chemie, Universität Tübingen, Auf der Morgenstelle 28, D-72076, Tübingen, Germany

    Dietmar G. Schmid, Graeme Nicholson & Günther Jung

  3. National Veterinary Institute, Post Box 8156 Dep., 0033, Oslo, Norway

    Duncan J. Colquhoun

Authors
  1. Günther Winkelmann
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  2. Dietmar G. Schmid
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  3. Graeme Nicholson
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  4. Günther Jung
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  5. Duncan J. Colquhoun
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Winkelmann, G., Schmid, D.G., Nicholson, G. et al. Bisucaberin – A dihydroxamate siderophore isolated from Vibrio salmonicida, an important pathogen of farmed Atlantic salmon (Salmo salar). Biometals 15, 153–160 (2002). https://doi.org/10.1023/A:1015206419613

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