The major facilitator superfamily-type transporter YmfE and the multidrug-efflux activator Mta mediate bacillibactin secretion in Bacillus subtilis

Journal of Bacteriology

Volumn 190, Issue 15, 2008, Pages 5143-5152

  Miethke, Marcus ^a,b   Schmidt, Sarah ^a   Marahiel, Mohamed A ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; BACILLIBACTIN; CARRIER PROTEIN; CATECHOL DERIVATIVE; FERRIC ION; FERRIC UPTAKE REGULATOR; IRON; MULTIDRUG EFFLUX ACTIVATOR MTA; PROTEIN YMFE; REGULATOR PROTEIN; SIDEROPHORE; TRANSCRIPTION FACTOR;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIUM CULTURE; BACTERIUM MUTANT; GENE EXPRESSION REGULATION; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; YMFE GENE;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CULTURE MEDIA; ESTERS; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; HYDROXYBENZOIC ACIDS; IRON; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OLIGOPEPTIDES; OPERON; PROTEIN STRUCTURE, SECONDARY; TRANS-ACTIVATORS;

BACILLUS SUBTILIS;

EID: 48149100258     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00464-08     Document Type: Article

References (38)

1. Allard, K. A., V. K. Viswanathan, and N. P. Cianciotto. 2006. lbtA and lbtB are required for production of the Legionella pneumophila siderophore legiobactin. J. Bacteriol. 188:1351-1363.
2. Baichoo, N., and J. D. Helmann. 2002. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J. Bacteriol. 184:5826-5832.
3. Baichoo, N., T. Wang, R. Ye, and J. D. Helmann. 2002. Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol. Microbiol. 45:1613-1629.
4. Baranova, N. N., A. Danchin, and A. A. Neyfakh. 1999. Mta, a global MerR-type regulator of the Bacillus subtilis multidrug-efflux transporters. Mol. Microbiol. 31:1549-1559.
5. Bleuel, C., C. Grosse, N. Taudte, J. Scherer, D. Wesenberg, G. J. Krauss, D. H. Nies, and G. Grass. 2005. TolC is involved in enterobactin efflux across the outer membrane of Escherichia coli. J. Bacteriol. 187:6701-6707.
6. Brickman, T. J., and S. K. Armstrong. 2005. Bordetella AlcS transporter functions in alcaligin siderophore export and is central to inducer sensing in positive regulation of alcaligin system gene expression. J. Bacteriol. 187: 3650-3661.
7. Brickman, T. J., H. Y. Kang, and S. K. Armstrong. 2001. Transcriptional activation of Bordetella alcaligin siderophore genes requires the AlcR regulator with alcaligin as inducer. J. Bacteriol. 183:483-489.
8. Caguiat, J. J., A. L. Watson, and A. O. Summers. 1999. Cd(II)-responsive and constitutive mutants implicate a novel domain in MerR. J. Bacteriol. 181:3462-3471.
9. Crouch, M. L., M. Castor, J. E. Karlinsey, T. Kalhorn, and F. C. Fang. 2008. Biosynthesis and IroC-dependent export of the siderophore salmochelin are essential for virulence of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 67:971-983.
10. Franza, T., B. Mahe, and D. Expert. 2005. Erwinia chrysanthemi requires a second iron transport route dependent of the siderophore achromobactin for extracellular growth and plant infection. Mol. Microbiol. 55:261-275.
11. Furrer, J. L., D. N. Sanders, I. G. Hook-Barnard, and M. A. McIntosh. 2002. Export of the siderophore enterobactin in Escherichia coli: involvement of a 43 kDa membrane exporter. Mol. Microbiol. 44:1225-1234.
12. Gaballa, A., and J. D. Helmann. 2007. Substrate induction of siderophore transport in Bacillus subtilis mediated by a novel one-component regulator. Mol. Microbiol. 66:164-173.
13. Godsey, M. H., N. N. Baranova, A. A. Neyfakh, and R. G. Brennan. 2001. Crystal structure of MtaN, a global multidrug transporter gene activator. J. Biol. Chem. 276:47178-47184.
14. Godsey, M. H., N. N. Baranova, A. A. Neyfakh, and R. G. Brennan. 2000. Crystallization and preliminary X-ray diffraction studies on the DNA-binding domain of the multidrug transporter activation protein (MtaN) from Bacillus subtilis. Acta Crystallogr. D 56:1456-1458.
15. Higgins, C. F. 2007. Multiple molecular mechanisms for multidrug resistance transporters. Nature 446:749-757.
16. Hoch, J. A. 1991. Genetic analysis in Bacillus subtilis. Methods Enzymol. 204:305-320.
17. Homuth, G., S. Masuda, A. Mogk, Y. Kobayashi, and W. Schumann. 1997. The dnaK operon of Bacillus subtilis is heptacistronic. J. Bacteriol. 179:1153-1164.
18. Kobayashi, K., et al. 2003. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 100:4678-4683.
19. Li, X. Z., H. Nikaido, and K. Poole. 1995. Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 39:1948-1953.
20. May, J. J., T. M. Wendrich, and M. A. Marahiel. 2001. The dhb operon of Bacillus subtilis encodes the biosynthetic template for the catecholic siderophore 2,3-dihydroxybenzoate-glycine-threonine trimeric ester bacillibactin. J. Biol. Chem. 276:7209-7217.
21. Miethke, M., O. Klotz, U. Linne, J. J. May, C. L. Beckering, and M. A. Marahiel. 2006. Ferri-bacillibactin uptake and hydrolysis in Bacillus subtilis. Mol. Microbiol. 61:1413-1427.
22. Miethke, M., and M. A. Marahiel. 2007. Siderophore-based iron acquisition and pathogen control. Microbiol. Mol. Biol. Rev. 71:413-451.
23. Ollinger, J., K. B. Song, H. Antelmann, M. Hecker, and J. D. Helmann. 2006. Role of the Fur regulon in iron transport in Bacillus subtilis. J. Bacteriol. 188:3664-3673.
24. Page, W. J., E. Kwon, A. S. Cornish, and A. E. Tindale. 2003. The csbX gene of Azotobacter vinelandii encodes an MFS efflux pump required for catecholate siderophore export. FEMS Microbiol. Lett. 228:211-216.
25. Poole, K., D. E. Heinrichs, and S. Neshat. 1993. Cloning and sequence analysis of an EnvCD homologue in Pseudomonas aeruginosa: regulation by iron and possible involvement in the secretion of the siderophore pyoverdine. Mol. Microbiol. 10:529-544.
26. Quadri, L. E. 2007. Strategic paradigm shifts in the antimicrobial drug discovery process of the 21st century. Infect. Disord. Drug Targets 7:230-237.
27. Rowland, B. M., T. H. Grossman, M. S. Osburne, and H. W. Taber. 1996. Sequence and genetic organization of a Bacillus subtilis operon encoding 2,3-dihydroxybenzoate biosynthetic enzymes. Gene 178:119-123.
28. Rowland, B. M., and H. W. Taber. 1996. Duplicate isochorismate synthase genes of Bacillus subtilis: regulation and involvement in the biosyntheses of menaquinone and 2,3-dihydroxybenzoate. J. Bacteriol. 178:854-861.
29. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
31. Shewchuk, L. M., J. D. Helmann, W. Ross, S. J. Park, A. O. Summers, and C. T. Walsh. 1989. Transcriptional switching by the MerR protein: activation and repression mutants implicate distinct DNA and mercury(II) binding domains. Biochemistry 28:2340-2344.
32. Stergiopoulos, I., L.-H. Zwiers, and M. A. De Waard. 2002. Secretion of natural and synthetic toxic compounds from filamentous fungi by membrane transporters of the ATP-binding cassette and major facilitator superfamily. Eur. J. Plant Pathol. 108:719-734.
33. Stülke, J., R. Hanschke, and M. Hecker. 1993. Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J. Gen. Microbiol. 139:2041-2045.
34. Tanabe, T., H. Nakao, T. Kuroda, T. Tsuchiya, and S. Yamamoto. 2006. Involvement of the Vibrio parahaemolyticus pvsC gene in export of the siderophore vibrioferrin. Microbiol. Immunol. 50:871-876.
35. Tusnady, G. E., and I. Simon. 2001. The HMMTOP transmembrane topology prediction server. Bioinformatics 17:849-850.
36. Tusnady, G. E., and I. Simon. 1998. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283:489-506.
37. Wach, A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae. Yeast 12:259-265.
38. Zhu, W., J. E. Arceneaux, M. L. Beggs, B. R. Byers, K. D. Eisenach, and M. D. Lundrigan. 1998. Exochelin genes in Mycobacterium smegmatis: identification of an ABC transporter and two nonribosomal peptide synthetase genes. Mol. Microbiol. 29:629-639.