Unsuspected control of siderophore production by N-acetylglucosamine in streptomycetes

Environmental Microbiology Reports

Volumn 4, Issue 5, 2012, Pages 512-521

  Craig, Matthias ^a   Lambert, Stéphany ^a   Jourdan, Samuel ^a   Tenconi, Elodie ^a   Colson, Séverine ^a   Maciejewska, Marta ^a   Ongena, Marc ^a   Martin, Juan Francisco ^b   van Wezel, Gilles ^c   Rigali, Sébastien ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b Institute of Biotechnology INBIOTEC Parque Científico de León   (Spain)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); STREPTOMYCES COELICOLOR; STREPTOMYCETACEAE; STREPTOMYCINEAE;

EID: 84867160523     PISSN: None     EISSN: 17582229     Source Type: Journal    
DOI: 10.1111/j.1758-2229.2012.00354.x     Document Type: Article

References (47)

1. Andrews, S.C., Robinson, A.K., and Rodriguez-Quinones, F. (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27: 215-237.
2. 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.
3. Barona-Gomez, F., Lautru, S., Francou, F.X., Leblond, P., Pernodet, J.L., and Challis, G.L. (2006) Multiple biosynthetic and uptake systems mediate siderophore-dependent iron acquisition in Streptomyces coelicolor A3(2) and Streptomyces ambofaciens ATCC 23877. Microbiology 152: 3355-3366.
4. Bentley, S.D., Chater, K.F., Cerdeno-Tarraga, A.M., Challis, G.L., Thomson, N.R., James, K.D., etal. (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417: 141-147.
5. Bertram, R., Rigali, S., Wood, N., Lulko, A.T., Kuipers, O.P., and Titgemeyer, F. (2011) Regulon of the N-acetylglucosamine utilization regulator NagR in Bacillus subtilis. J Bacteriol 193: 3525-3536.
6. Boelaert, J.R., de Locht, M., Van Cutsem, J., Kerrels, V., Cantinieaux, B., Verdonck, A., etal. (1993) Mucormycosis during deferoxamine therapy is a siderophore-mediated infection. In vitro and in vivo animal studies. J Clin Invest 91: 1979-1986.
7. Boer, W., Folman, L.B., Summerbell, R.C., and Boddy, L. (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29: 795-811.
8. Braun, V. (1997) Avoidance of iron toxicity through regulation of bacterial iron transport. Biol Chem 378: 779-786.
9. Colson, S., Stephan, J., Hertrich, T., Saito, A., van Wezel, G.P., Titgemeyer, F., and Rigali, S. (2007) Conserved cis-acting elements upstream of genes composing the chitinolytic system of streptomycetes are DasR-responsive elements. J Mol Microbiol Biotechnol 12: 60-66.
10. Colson, S., van Wezel, G.P., Craig, M., Noens, E.E., Nothaft, H., Mommaas, A.M., etal. (2008) The chitobiose-binding protein, DasA, acts as a link between chitin utilization and morphogenesis in Streptomyces coelicolor. Microbiology 154: 373-382.
11. Compant, S., Duffy, B., Nowak, J., Clement, C., and Barka, E.A. (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71: 4951-4959.
12. Cornelis, P., Wei, Q., Andrews, S.C., and Vinckx, T. (2011) Iron homeostasis and management of oxidative stress response in bacteria. Metallomics 3: 540-549.
13. Crosa, J.H., and Walsh, C.T. (2002) Genetics and assembly line enzymology of siderophore biosynthesis in bacteria. Microbiol Mol Biol Rev 66: 223-249.
14. Deutscher, J., Francke, C., and Postma, P.W. (2006) How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70: 939-1031.
15. Flores, F.J., and Martin, J.F. (2004) Iron-regulatory proteins DmdR1 and DmdR2 of Streptomyces coelicolor form two different DNA-protein complexes with iron boxes. Biochem J 380: 497-503.
16. Floriano, B., and Bibb, M. (1996) afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 21: 385-396.
17. Galaris, D., and Pantopoulos, K. (2008) Oxidative stress and iron homeostasis: mechanistic and health aspects. Crit Rev Clin Lab Sci 45: 1-23.
18. Greenwood, N.N., and Earnshaw, A. (1997) Chemistry of the Elements. Oxford, UK: Elsevier.
19. Hantke, K. (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4: 172-177.
20. Hiard, S., Maree, R., Colson, S., Hoskisson, P.A., Titgemeyer, F., van Wezel, G.P., etal. (2007) PREDetector: a new tool to identify regulatory elements in bacterial genomes. Biochem Biophys Res Commun 357: 861-864.
21. Hoffmann, T., Schutz, A., Brosius, M., Volker, A., Volker, U., and Bremer, E. (2002) High-salinity-induced iron limitation in Bacillus subtilis. J Bacteriol 184: 718-727.
22. Kieser, T., Bibb, M., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (2000) Practical Streptomyces Genetics. Norwich, UK: John Innes Foundation.
23. Kincade, G.F., Saxton, G.D., Morse, P.W., and Mathisen, A.K. (1948) Streptomycin in the treatment of tuberculosis; a report of its use in a series of 100 cases. Can Med Assoc J 59: 105-112.
24. Korgaonkar, A.K., and Whiteley, M. (2011) Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan. J Bacteriol 193: 909-917.
25. Lautru, S., Deeth, R.J., Bailey, L.M., and Challis, G.L. (2005) Discovery of a new peptide natural product by Streptomyces coelicolor genome mining. Nat Chem Biol 1: 265-269.
26. Lee, J.W., and Helmann, J.D. (2007) Functional specialization within the Fur family of metalloregulators. Biometals 20: 485-499.
27. Manteca, A., Fernandez, M., and Sanchez, J. (2005) A death round affecting a young compartmentalized mycelium precedes aerial mycelium dismantling in confluent surface cultures of Streptomyces antibioticus. Microbiology 151: 3689-3697.
28. Manteca, A., Fernandez, M., and Sanchez, J. (2006) Cytological and biochemical evidence for an early cell dismantling event in surface cultures of Streptomyces antibioticus. Res Microbiol 157: 143-152.
29. Matzanke, B.F., Bill, E., Trautwein, A.X., and Winkelmann, G. (1987) Role of siderophores in iron storage in spores of Neurospora crassa and Aspergillus ochraceus. J Bacteriol 169: 5873-5876.
30. Miethke, M., and Marahiel, M.A. (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71: 413-451.
31. Miguelez, E.M., Hardisson, C., and Manzanal, M.B. (1999) Hyphal death during colony development in Streptomyces antibioticus: morphological evidence for the existence of a process of cell deletion in a multicellular prokaryote. J Cell Biol 145: 515-525.
32. Nielsen, A.K., Breuner, A., Krzystanek, M., Andersen, J.T., Poulsen, T.A., Olsen, P.B., etal. (2010) Global transcriptional analysis of Bacillus licheniformis reveals an overlap between heat shock and iron limitation stimulon. J Mol Microbiol Biotechnol 18: 162-173.
33. Nothaft, H., Dresel, D., Willimek, A., Mahr, K., Niederweis, M., and Titgemeyer, F. (2003a) The phosphotransferase system of Streptomyces coelicolor is biased for N-acetylglucosamine metabolism. J Bacteriol 185: 7019-7023.
34. Nothaft, H., Parche, S., Kamionka, A., and Titgemeyer, F. (2003b) In vivo analysis of HPr reveals a fructose-specific phosphotransferase system that confers high-affinity uptake in Streptomyces coelicolor. J Bacteriol 185: 929-937.
35. Nothaft, H., Rigali, S., Boomsma, B., Swiatek, M., McDowall, K.J., van Wezel, G.P., and Titgemeyer, F. (2010) The permease gene nagE2 is the key to N-acetylglucosamine sensing and utilization in Streptomyces coelicolor and is subject to multi-level control. Mol Microbiol 75: 1133-1144.
36. Ratledge, C., and Dover, L.G. (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54: 881-941.
37. Rigali, S., Schlicht, M., Hoskisson, P., Nothaft, H., Merzbacher, M., Joris, B., and Titgemeyer, F. (2004) Extending the classification of bacterial transcription factors beyond the helix-turn-helix motif as an alternative approach to discover new cis/trans relationships. Nucleic Acids Res 32: 3418-3426.
38. Rigali, S., Nothaft, H., Noens, E.E., Schlicht, M., Colson, S., Muller, M., etal. (2006) The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol Microbiol 61: 1237-1251.
39. Rigali, S., Titgemeyer, F., Barends, S., Mulder, S., Thomae, A.W., Hopwood, D.A., and van Wezel, G.P. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675.
40. Schrempf, H. (2001) Recognition and degradation of chitin by streptomycetes. Antonie Van Leeuwenhoek 79: 285-289.
41. Schwyn, B., and Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
42. Swiatek, M.A., Tenconi, E., Rigali, S., and van Wezel, G.P. (2012) Functional analysis of the N-acetylglucosamine metabolic genes of Streptomyces coelicolor and role in control of development and antibiotic production. J Bacteriol 194: 1136-1144.
43. Touati, D. (2000) Iron and oxidative stress in bacteria. Arch Biochem Biophys 373: 1-6.
44. Tunca, S., Barreiro, C., Sola-Landa, A., Coque, J.J., and Martin, J.F. (2007) Transcriptional regulation of the desferrioxamine gene cluster of Streptomyces coelicolor is mediated by binding of DmdR1 to an iron box in the promoter of the desA gene. FEBS J 274: 1110-1122.
45. Wandersman, C., and Delepelaire, P. (2004) Bacterial iron sources: from siderophores to hemophores. Annu Rev Microbiol 58: 611-647.
46. Yamanaka, K., Oikawa, H., Ogawa, H.O., Hosono, K., Shinmachi, F., Takano, H., etal. (2005) Desferrioxamine E produced by Streptomyces griseus stimulates growth and development of Streptomyces tanashiensis. Microbiology 151: 2899-2905.
47. Young, G.M., and Postle, K. (1994) Repression of tonB transcription during anaerobic growth requires Fur binding at the promoter and a second factor binding upstream. Mol Microbiol 11: 943-954.