The siderophore system is essential for viability of Aspergillus nidulans: Functional analysis of two genes encoding L-ornithine N5-monooxygenase (sidA) and a non-ribosomal peptide synthetase (sidC)

Molecular Microbiology

Volumn 49, Issue 2, 2003, Pages 359-375

  Eisendle, Martin ^a   Oberegger, Harald ^a   Zadra, Ivo ^a   Haas, Hubertus ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID DERIVATIVE; ANTIOXIDANT; FERRIC ION; FERRICROCIN; FERROUS ION; FUNGAL PROTEIN; ORNITHINE N5 MONOOXYGENASE; PARAQUAT; PEPTIDE SYNTHASE; SIDEROPHORE; TRIACETYLFUSARININE C; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; ASCOMYCETES; ASPERGILLUS NIDULANS; BIOSYNTHESIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; FUNCTIONAL ASSESSMENT; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS MUTANT; GENE DELETION; GENE FUNCTION; GENE SIDA; GENE SIDC; GENETIC ANALYSIS; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN TRANSPORT; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; ASPERGILLUS NIDULANS; BACTERIAL PROTEINS; CELL SURVIVAL; FERRICHROME; FUNGAL PROTEINS; HERBICIDES; HYDROXAMIC ACIDS; IRON; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PARAQUAT; PEPTIDE SYNTHASES; SEQUENCE ALIGNMENT; SIDEROPHORES;

ASCOMYCOTA; ASPERGILLUS; EMERICELLA NIDULANS; FUNGI;

EID: 0038162590     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03586.x     Document Type: Article

References (67)

1. Adams, T.H., Wieser, J.K., and Yu, J.H. (1998) Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62: 35-54.
2. Andrews, S.C. (1998) Iron storage in bacteria. Adv Microb Physiol 40: 281-351.
3. Ardon, O., Nudelman, R., Caris, C., Libman, J., Shanzer, A., Chen, Y., and Hadar, Y. (1998) Iron uptake in Ustilago maydis: tracking the iron path. J Bacteriol 180: 2021-2026.
4. Askwith, C., Eide, D., Van Ho, A., Bernard, P.S., Li, L., Davis-Kaplan, S., et al. (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76: 403-410.
5. Bailey, A.M., Kershaw, M.J., Hunt, B.A., Paterson, I.C., Charnley, A.K., Reynolds, S.E., and Clarkson, J.M. (1996) Cloning and sequence analysis of an intron-containing domain from a peptide synthetase-encoding gene of the entomopathogenic fungus Metarhizium anisopliae. Gene 173: 195-197.
6. Ballance, D.J. (1986) Sequences important for gene expression in filamentous fungi. Yeast 2: 229-236.
7. Brakhage, A.A., and Turner, G. (1992) L-lysine repression of penicillin biosynthesis and the expression of penicillin biosynthesis genes acvA and ipnA. Aspergillus nidulans. FEMS Microbiol Lett 77: 123-127.
8. Breuer, W., Epsztejn, S., and Cabantchik, Z.I. (1995a) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron (II). J Biol Chem 270: 24209-24215.
9. Breuer, W., Epsztejn, S., Millgram, P., and Cabantchik, I.Z. (1995b) Transport of iron and other transition metals into cells as revealed by a fluorescent probe. Am J Physiol 268: C1354-C1361.
10. Brody, H., Griffith, J., Cuticchia, A.J., Arnold, J., and Timberlake, W.E. (1991) Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res 19: 3105-3109.
11. Brookman, J.L., and Denning, D.W. (2000) Molecular genetics in Aspergillus fumigatus. Curr Opin Microbiol 3: 468-474.
12. Challis, G.L., Ravel, J., and Townsend, C.A. (2000) Predictive, structure-based model of amino acid recognition by nonribosomal peptide synthetase adenylation domains. Chem Biol 7: 211-224.
13. Charlang, G., Ng, B., Horowitz, N.H., and Horowitz, R.M. (1981) Cellular and extracellular siderophores of Aspergillus nidulans and Penicillium chrysogenum. Mol Cell Biol 1: 94-100.
14. Chen, C.Y., and Morse, S.A. (1999) Neisseria gonorrhoeae bacterioferritin: structural heterogeneity, involvement in iron storage and protection against oxidative stress. Microbiology 145: 2967-2975.
15. Clarke, T.E., Tari, L.W., and Vogel, H.J. (2001) Structural biology of bacterial iron uptake systems. Curr Top Med Chem 1: 7-30.
16. Dancis, A., Roman, D.G., Anderson, G.J., Hinnebusch, A.G., and Klausner, R.D. (1992) Ferric reductase of Saccharomyces cerevisiae: molecular characterization, role in iron uptake, and transcriptional control by iron. Proc Natl Acad Sci USA 89: 3869-3873.
17. Emery, T. (1976) Fungal ornithine esterases: relationship to iron transport. Biochemistry 15: 2723-2728.
18. Fidel, S., Doonan, J.H., and Morris, N.R. (1988) Aspergillus nidulans contains a single actin gene which has unique intron locations and encodes a gamma-actin. Gene 70: 283-293.
19. Fischer, R., and Timberlake, W.E. (1995) Aspergillus nidulans apsA (anucleate primary sterigmata) encodes a coiled-coil protein required for nuclear positioning and completion of asexual development. J Cell Biol 128: 485-498.
20. Foster, L.A. (2002) Utilization and cell-surface binding of hemin by Histoplasma capsulatum. Can J Microbiol 48: 437-442.
21. Georgatsou, E., and Alexandraki, D. (1994) Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 14: 3065-3073.
22. Guerinot, M.L. (1994) Microbial iron transport. Annu Rev Microbiol 48: 743-772.
23. Haas, H., Zadra, I., and Stoffler, G., and Angermayr, K. (1999) The Aspergillus nidulans GATA factor SREA is involved in regulation of siderophore biosynthesis and control of iron uptake. J Biol Chem 274: 4613-4619.
24. Haas, H., Schoeser, M., Lesuisse, E., Ernst, J.F., Parson, W., Abt, B., et al. (2002) Characterisation of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem J 371: 505-513.
25. Haber, F., and Weiss, J. (1934) The catalytic decomposition of hydrogen peroxide by iron salts. Proc R Soc Series A 147: 332-333.
26. Halliwell, B., and Gutteridge, J.M. (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219: 1-14.
27. Harrison, P.M., and Arosio, P. (1996) The ferritins: molecular properties, iron storage function and cellular regulation. Biochim Biophys Acta 1275: 161-203.
28. Herrero, M., de Lorenzo, V., and Neilands, J.B. (1988) Nucleotide sequence of the iucD gene of the pCoIV-K30 aerobactin operon and topology of its product studied with phoA and lacZ gene fusions. J Bacteriol 170: 56-64.
29. Heymann, P., Gerads, M., Schaller, M., Dromer, F., Winkelmann, G., and Ernst, J.F. (2002) The siderophore iron transporter of Candida albicans (Sit1p/Arn1p) mediates uptake of ferrichrome-type siderophores and is required for epithelial invasion. Infect Immun 70: 5246-5255.
30. Horowitz, N.H., Charlang, G., Horn, G., and Williams, N.P. (1976) Isolation and identification of the conidial germination factor of Neurospora crassa. J Bacteriol 127: 135-140.
31. Hu, C.J., Bai, C., Zheng, X.D., Wang, Y.M., and Wang, Y. (2002) Characterization and functional analysis of the siderophore-Fe transporter CaArn1p in Candida albicans. J Biol Chem 11: 11.
32. Kleinkauf, H., and Von Dohren, H. (1996) A nonribosomal system of peptide biosynthesis. Eur J Biochem 236: 335-351.
33. Konetschny-Rapp, S., Huschka, H.G., Winkelmann, G., and Jung, G. (1988) High-performance liquid chromatography of siderophores from fungi. Biol Met 1: 9-17.
34. Latge, J.P. (1999) Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12: 310-350.
35. Leong, S.A., and Winkelmann, G. (1998) Molecular biology of iron transport in fungi. Met Ions Biol Syst 35: 147-186.
36. Lesuisse, E., and Labbe, P. (1989) Reductive and non-reductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J Gen Microbiol 135: 257-263.
37. Matzanke, B.F., Bill, E., Trautwein, A.X., and Winkelmann, G. (1987a) Role of siderophores in iron storage in spores of Neurospora crassa and Aspergillus ochraceus. J Bacteriol 169: 5873-5876.
38. 57Fe-labeled coprogen in Neurospora crassa. An in vivo Mossbauer study. Eur J Biochem 162: 643-650.
39. Mei, B., Budde, A.D., and Leong, S.A. (1993) sid1, a gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron, and role in phytopathogenicity. Proc Natl Acad Sci USA 90: 903-907.
40. Neilands, J.B., Konopka, K., Schwyn, B., Coy, M., Francis, R.T., Paw, B.H., and Bagg, A. (1987) Comparative biochemistry of microbial iron assimilation. In Iron Transport in Microbes, Plants and Animals. Winkelmann, G. van der Helm, D., and Neilands, J.B. (eds). New York: Weinheim, VCH, pp. 3-34.
41. Oberegger, H., Zadra, I., Schoeser, M., and Haas, H. (2000) Iron starvation leads to increased expression of Cu/Zn-superoxide dismutase in Aspergillus. FEBS Lett 485: 113-116.
42. Oberegger, H., Schoeser, M., Zadra, I., Abt, B., and Haas, H. (2001) SREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans. Mol Microbiol 41: 1077-1089.
43. Oberegger, H., Schoeser, M., Zadra, I., Schrettl, M., Parson, W., and Haas, H. (2002a) Regulation of freA, acoA, lysF and cycA expression by iron availability in Aspergillus nidulans. Appl Environ Microbiol 68: 5769-5772.
44. Oberegger, H., Zadra, I., Schoeser, M., Abt, B., Parson, W., and Haas, H. (2002b) Identification of members of the Aspergillus nidulans SREA regulon: genes involved in siderophore biosynthesis and utilization. Biochem Soc T 30: 781-783.
45. Payne, S.M. (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol 235: 329-344.
46. Plattner, H.J., and Diekmann, H. (1994) Enzymology of siderophore biosynthesis in fungi. In Metal Ions in Fungi. Winkelmann, G., and Winge, D.R. (eds). New York, New York: Marcel Decker, pp. 99-117.
47. Pontecorvo, G., Roper, J.A., Hemmons, L.M., MacDonald, K.D., and Bufton, A.W.J. (1953) The genetics of Aspergillus nidulans. Adv Genet 5: 141-238.
48. Ratledge, C., and Dover, L.G. (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
49. Roosenberg, J.M., Lin, Y.M., Lu, Y., and Miller, M.J. (2000) Studies and syntheses of siderophores, microbial iron chelators, and analogs as potential drug delivery agents. Curr Med Chem 7: 159-197.
50. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
51. Stachelhaus, T., Mootz, H.D., and Marahiel, M.A. (1999) The specificity-conferring code of adenylation domains in non-ribosomal peptide synthetases. Chem Biol 6: 493-505.
52. Stearman, R., Yuan, D.S., Yamaguchi-Iwai, Y., Klausner, R.D., and Dancis, A. (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271: 1552-1557.
53. Stehr, M., Diekmann, H., Smau, L., Seth, O., Ghisla, S., Singh, M., and Macheroux, P. (1998) A hydrophobic sequence motif common to N-hydroxylating enzymes. Trends Biochem Sci 23: 56-57.
54. Suntres, Z.E. (2002) Role of antioxidants in paraquat toxicity. Toxicology 180: 65-77.
55. Tilburn, J., Sarkar, S., Widdick, D.A., Espeso, E.A., Orejas, M., Mungroo, J., et al. (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J 14: 779-790.
56. Tudzynski, P., Holter, K., Correia, T., Arntz, C., Grammel, N., and Keller, U. (1999) Evidence for an ergot alkaloid gene cluster in Claviceps purpurea. Mol Gen Genet 261: 133-141.
57. Upshall, A., Gilbert, T., Saari, G., O'Hara, P.J., Weglenski, P., Berse, B., et al. (1986) Molecular analysis of the argB gene of Aspergillus nidulans. Mol Gen Genet 204: 349-354.
58. Visca, P., Ciervo, A., and Orsi, N. (1994) Cloning and nucleotide sequence of the pvdA gene encoding the pyoverdin biosynthetic enzyme L-ornithine N5-oxygenase in Pseudomonas aeruginosa. J Bacteriol 176: 1128-1140.
59. Weber, T., and Marahiel, M.A. (2001) Exploring the domain structure of modular nonribosomal peptide synthetases. Structure (Camb) 9: R3-R9.
60. Weinberg, E.D. (1999) The role of iron in protozoan and fungal infectious diseases. J Eukaryot Microbiol 46: 231-238.
61. Weissman, Z., Shemer, R., and Kornitzer, D. (2002) Deletion of the copper transporter CaCCC2 reveals two distinct pathways for iron acquisition in Candida albicans. Mol Microbiol 44: 1551-1560.
62. Winkelmann, G. (1993) Kinetics, energetics, and mechanisms of siderophore iron transport in fungi. In Iron Chelation in Plants and Soil Microorganisms. Barton, L.L., and Hemmings, B.C. (eds). New York: New York Academic Press, pp. 219-239.
63. Winkelmann, G. (2001) Siderophore transport in Fungi. In Microbial Transport Systems. Winkelmann, G. (ed.). Weinheim: Wiley-VCH, pp. 463-479.
64. Yuan, W.M., Gentil, G.D., Budde, A.D., and Leong, S.A. (2001) Characterization of the Ustilago maydis sid2 gene, encoding a multidomain peptide synthetase in the ferrichrome biosynthetic gene cluster. J Bacteriol 183: 4040-4051.
65. Yun, C.W., Ferea, T., Rashford, J., Ardon, O., Brown, P.O., Botstein, D., et al. (2000) Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae. Evidence for two pathways of iron uptake. J Biol Chem 275: 10709-10715.
66. Yun, C.W., Bauler, M., Moore, R.E., Klebba, P.E., and Philpott, C.C. (2001) The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cerevisiae. J Biol Chem 276: 10218-10223.
67. Zadra, I., Abt, B., Parson, W., and Haas, H. (2000) xylP promoter-based expression system and its use for anti-sense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl Environ Microbiol 66: 4810-4816.