Iron acquisition mechanisms of the Burkholderia cepacia complex

Biology of Metals - Tập 20 - Trang 431-452 - 2007
Mark S. Thomas1
1Unit of Infection and Immunity, School of Medicine and Biomedical Sciences, University of Sheffield, Beech Hill Road, UK

Tóm tắt

The Burkholderia cepacia complex (Bcc) is comprised of at least 10 closely related species of Gram-negative proteobacteria that are associated with infections in certain groups of immunocompromised individuals, particularly those with cystic fibrosis. Infections in humans tend to occur in the lungs, which present an iron-restricted environment to a prospective pathogen, and accordingly members of the Bcc appear to possess efficient mechanisms for iron capture. These bacteria specify up to four different types of siderophore (ornibactin, pyochelin, cepabactin and cepaciachelin) that employ the full repertoire of iron-binding groups present in most naturally occurring siderophores. Members of the Bcc are also capable of utilising some exogenous siderophores that they are not able to synthesise. In addition to siderophore-mediated mechanisms of iron uptake, the Bcc possess mechanisms for acquiring iron from haem and from ferritin. The Bcc therefore appear to be well-equipped for life in an iron-poor environment.

Tài liệu tham khảo

Adilakshmi T, Ayling PD, Ratledge C (2000) Mutational analysis of a role for salicylic acid in iron metabolism of Mycobacterium smegmatis. J Bacteriol 182:264–271 Agnoli K, Lowe CA, Farmer KL, Husnain I, Thomas MS (2006) The ornibactin biosynthesis and transport genes of Burkholderia cenocepacia are regulated by an ECF σ factor which is a part of the Fur regulon. J Bacteriol 188:3631–3644 Alice AF, Lopez CS, Lowe CA, Ledesma MA, Crosa JH (2006) Genetic and transcriptional analysis of the siderophore malleobactin biosynthesis and transport genes in the human pathogen Burkholderia pseudomallei K96243. J Bacteriol 188:1551–1566 Alisi C, Lasinio GJ, Dalmastri C, et al (2005) Metabolic profiling of Burkholderia cenocepacia, Burkholderia ambifaria, and Burkholderia pyrrocinia isolates from maize rhizosphere. Microb Ecol 50:385–395 Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Lett 27:215–237 Ankenbauer RG (1992) Cloning of the outer membrane high-affinity Fe(III)–pyochelin receptor of Pseudomonas aeruginosa. J Bacteriol 174:4401–4409 Ankenbauer RG, Cox CD (1988) Isolation and characterisation of Pseudomonas aeruginosa mutants requiring salicylic acid for pyochelin biosynthesis. J Bacteriol 170:5364–5367 Ankenbauer RG, Quan HN (1994) FptA, the Fe(III)–pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J Bacteriol 176:307–319 Ankenbauer RG, Sriyosachati S, Cox CD (1985) Effects of siderophores on the growth of Pseudomonas aeruginosa in human serum and transferrin. Infect Immun 49:312–140 Ankenbauer RG, Toyokuni T, Staley A, Rinehart KL Jr, Cox CD (1988) Synthesis and biological activity of pyochelin, a siderophore of Pseudomonas aeruginosa. J Bacteriol 170:5344–5351 Anthoni U, Christophersen C, Nielsen PH, Gram L, Petersen BO (1995) Pseudomonine: an isoxazolidone with siderophore activity from Pseudomonas fluorescens AH2 isolated from Lake Victorian Nile perch. J Nat Prod 58:1786–1789 Audenaert K, Pattery T, Cornelis P, Hofte M (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant Microbe Interact 15:1147–1156 Baldwin A, Mahenthiralingam E, Thickett KM, et al (2005) Multilocus sequence typing scheme that provides both species and strain differentiation for the Burkholderia cepacia complex. J Clin Microbiol 43:4665–4673 Barelmann I, Meyer J-M, Taraz K, Budzikiewicz H (1996) Cepaciachelin, a new catecholate siderophore from Burkholderia (Pseudomonas) cepacia. Z Naturforsch 51c:627–630 Barker WR, Callaghan C, Hill L, et al (1979) G1549, a new cyclic hydroxamic acid antibiotic, isolated from culture broth of Pseudomonas alcaligenes. J Antibiot 32:1096–1103 Baysse C, De Vos D, Naudet Y, et al (2000) Vanadium interferes with siderophore-mediated iron uptake in Pseudomonas aeruginosa. Microbiology 146:2425–2434 Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ Microbiol 7:1673–1685 Braun V, Mahren S (2005) Transmembrane transcriptional control (surface signalling) of the Escherichia coli Fec type. FEMS Microbiol Rev 29:673–684 Bukovits GJ, Mohr N, Budzkiewicz H, Korth H, Pulverer G (1982) 2-Phenyl thiazole derivatives from Pseudomonas cepacia. Z Naturforsch 37b:877–880 Carmi R, Carmeli S, Levy E, Gough FJ (1994) (+)-(S)-Dihydroaeruginoic acid, an inhibitor of Septoria tritici and other phytopathogenic fungi and bacteria, produced by Pseudomonas fluorescens. J Nat Prod 57:1200–1205 Castignetti D (1997) Probing of Pseudomonas aeruginosa, Pseudomonas aureofaciens, Burkholderia (Pseudomonas) cepacia, Pseudomonas fluorescens, and Pseudomonas putida with the ferripyochelin receptor A gene and the synthesis of pyochelin in Pseudomonas aureofaciens, Pseudomonas fluorescens, and Pseudomonas putida. Curr Microbiol 34:250–257 Chipperfield JR, Ratledge C (2000) Salicylic acid is not a bacterial siderophore: a theoretical study. BioMetals 13:165–168 Cobessi D, Celia H, Pattus F (2005) Crystal structure at high resolution of ferric–pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa. J Mol Biol 352:893–904 Coenye T, Vandamme P (2003) Diversity and significance of Burkholderia species occupying diverse ecological niches. Environ Microbiol 5:719–729 Cornish AS, Page WJ (1995) Production of the tricatecholate siderophore protochelin by Azotobacter vinelandii. BioMetals 8:332–338 Cox CD (1980) Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol 142:581–587 Cox CD, Graham R (1979) Isolation of an iron-binding compound from Pseudomonas aeruginosa. J Bacteriol 137:357–364 Cox CD, Rinehart KL, Moore ML, Cook JC (1981) Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc Natl Acad Sci USA 78:4256–4260 Cuppels DA, Stipanovic RD, Stoessl A, Stothers JB (1987) The constitution and properties of a pyochelin–zinc complex. Can J Chem 65:2126–2130 Darling P, Chan M, Cox AD, Sokol PA (1998) Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect Immun 66:874–877 De Voss JJ, Rutter K, Schroeder BG, Su H, Zhu Y-Q, Barry CE (2000) The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc Natl Acad Sci USA 97:1252–1257 Farmer KL, Thomas MS (2004) Isolation and characterization of Burkholderia cenocepacia mutants deficient in pyochelin production: pyochelin biosynthesis is sensitive to sulphur availability. J Bacteriol 186:270–277 Gaille C, Kast P, Haas D (2002) Salicylate biosynthesis in Pseudomonas aeruginosa. J Biol Chem 277:21768–21775 Gaille C, Reimmann C, Haas D (2003) Isochorismate synthase (PchA), the first and rate-limiting enzyme in salicylate biosynthesis of Pseudomonas aeruginosa. J Biol Chem 278:16893–16898 Gehring AM, DeMoll E, Fetherston D, et al (1998) Iron acquisition in plaque: modular logic in enzymatic biogenesis of yersiniabactin by Yersinia pestis. Chem Biol 5:573–586 Genco CA, Dixon DW (2001) Emerging strategies in microbial haem capture. Mol Microbiol 39:1–11 Gensberg K, Hughes K, Smith AW (1992) Siderophore-specific induction of iron uptake in Pseudomonas aeruginosa. J Gen Microbiol 138:2381–2387 Govan JRW, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60:539–574 Hausinger RP (2004) Fe(II)/α-ketoglutarate-dependent hydroxylases and related enzymes. Crit Rev Biochem Mol Biol 39:21–68 Heinrichs DE, Poole K (1993) Cloning and sequence analysis of a gene (pchR) encoding an AraC family activator of pyochelin and ferripyochelin receptor synthesis in Pseudomonas aeruginosa. J Bacteriol 175:5882–5889 Heinrichs DE, Poole K (1996) PchR, a regulator of ferripyochelin receptor gene (fptA) expression in Pseudomonas aeruginosa, functions both as an activator and a repressor. J Bacteriol 178:2586–2592 Heinrichs DE, Young L, Poole K (1991) Pyochelin-mediated transport in Pseudomonas aeruginosa: involvement of a high-molecular-mass outer membrane protein. Infect Immun 59:3680–3684 Hoegy F, Celia H, Mislin GL, Vincent M, Gallay J, Schalk IJ (2005) Binding of iron-free siderophore, a common feature of siderophore outer membrane transporters of Escherichia coli and Pseudomonas aeruginosa. J Biol Chem 280:20222–20230 Holden MT, Titball RW, Peacock SJ, et al (2004) Genome plasticity of the causative agent of melioidosis, Burkholderia pseudomallei. Proc Natl Acad Sci USA 101:14240–14245 Huber B, Feldmann F, Kothe M, et al (2004) Identification of a novel virulence factor in Burkholderia cenocepacia H111 required for efficient slow killing of Caenorhabditis elegans. Infect Immun 72:7220–7230 Ino A, Murabayashi A (2001) Synthetic studies of thiazoline and thiazolidine-containing natural products. Part 3: total synthesis and absolute configuration of the siderophore yersiniabactin. Tetrahedron 57:1897–1902 Isles A, Maclusky I, Corey M, et al (1984) Pseudomonas cepacia infections in cystic fibrosis: an emerging problem. J Pediatr 104:206–210 Itoh J, Miyadoh S, Takahasi S, Amano S, Ezaki N, Yamada Y (1979) Studies on antibiotics BN-227 and BN-227-F, new antibiotics. I. Taxonomy, isolation and characterization. J Antibiot 33:1089–1095 Itoh J, Amano S, Ogawa Y, Kodama Y, Ezaki N, Yamada Y (1980) Studies on antibiotics BN-227 and BN-227-F, new antibiotics. II. Chemical structure of antibiotics BN-227 and BN-227-F. J Antibiot 33:377–382 Keller-Schierlein W, Hagmann L, Zahner H, Huhn W (1988) Maduraferrin, a novel siderophore from Actinomadura madurae. Helv Chim Acta 71:1528–1534 Kerbarh O, Ciulli A, Howard NI, Abell C (2005) Salicylate biosynthesis: purification, and characterization of Irp9, a bifunctional salicylate synthase from Yersinia enterocolitica. J Bacteriol 187:5061–5066 Klumpp C, Burger A, Mislin GL, Abdallah MA (2005) From a total synthesis of cepabactin and its 3:1 ferric complex to the isolation of a 1:1:1 mixed complex between iron (III), cepabactin and pyochelin. Bioorg Med Chem Lett 15:1721–1724 Koebnik R (2005) TonB-dependent trans-envelope signalling: the exception or the rule. Trends Microbiol 13:343–347 Koedam N, Wittouck E, Gaballa A, Gillis A, Hofte M, Cornelis P (1994) Detection and differentiation of microbial siderophores by isoelectric focusing and chrome azurol S overlay. BioMetals 7:287–291 Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 99:7072–7077 Leoni L, Orsi N, de Lorenzo V, Visca P (2000) Functional analysis of PvdS, an iron starvation sigma factor of Pseudomonas aeruginosa. J Bacteriol 182:1481–1491 Lessie TG, Hendrickson W, Manning BD, Devereux R (1996) Genomic complexity and plasticity of Burkholderia cepacia. FEMS Microbiol Lett 144:117–128 Lewenza S, Sokol PA (2001) Regulation of ornibactin biosynthesis and N-acyl-l-homoserine lactone production by CepR in Burkholderia cepacia. J Bacteriol 183:2212–2218 Lewenza S, Conway B, Greenberg EP, Sokol PA (1999) Quorum sensing in Burkholderia cepacia: identification if the LuxRI homologs CepRI. J Bacteriol 181:748–756 LiPuma JJ (1998) Burkholderia cepacia: management issues and new insights. Clin Chest Med 19:473–486 LiPuma JJ, Spilker T, Gill LH, Campbell PW, Liu L, Mahenthiralingam E (2001) Disproportionate distribution of Burkholderia cepacia complex species and transmissibility markers in cystic fibrosis. Am J Respir Crit Care Med 164:92–96 Lowe CA, Asghar AH, Shalom G, Shaw JG, Thomas MS (2001) The Burkholderia cepacia fur gene: co-localisation with omlA and absence of regulation by iron. Microbiology 147:1303–1314 Mahenthiralingam E, Baldwin A, Vandamme P (2002) Burkholderia cepacia complex infection in patients with cystic fibrosis. J Med Microbiol 51:533–538 Mahenthiralingam E, Coenye T, Chung JW, Speert DP, Govan JRW, Taylor P, Vandamme P (2000) Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J Clin Microbiol 38:910–913 Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144–156 Malott RJ, Baldwin A, Mahenthiralingam E, Sokol PA (2005) Characterization of the cciIR quorum-sensing system in Burkholderia cenocepacia. Infect Immun 73:4982–4992 Marshall BJ, Ratledge C (1971) Conversion of chorismic acid and isochorismic acid to salicylic acid by cell-free extracts of Mycobacterium smegmatis. Biochem Biophys Acta 230:643–645 Marshall BJ, Ratledge C (1972) Salicylic acid biosynthesis and its control in Mycobacterium smegmatis. Biochim Biophys Acta 264:106–116 Martell AE, Smith RM (1977) Other organic ligands. In: Martell AE, Smith RM (eds) Critical stability constants, vol 3. Plenum, New York, pp 181–201 Martin RG, Rosner JL (2001) The AraC transcriptional activators. Curr Opin Microbiol 4:132–137 McMorran BJ, Merriman ME, Rombel IT, Lamont IL (1996) Characterisation of the pvdE gene which is required for pyoverdine synthesis in Pseudomonas aeruginosa. Gene 176:55–59 McMorran BJ, Kumara HMCS, Lamont IL (2001) Involvement of a transformylase enzyme in siderophore synthesis in Pseudomonas aeruginosa. Microbiology 147:1517–1524 Mercado-Blanco J, van der Drift KMGM, Olsson PE, Thomas-Oates JE, van Loon LC, Bakker PAHM (2001) Analysis of the pmsCEAB gene cluster involved in the biosynthesis of salicylic acid an the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J Bacteriol 183:1909–1920 Meyer J-M (1992) Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa: possible involvement of porin OprF in iron metabolism. J Gen Microbiol 138:951–958 Meyer J-M (2000) Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent pseudomonas species. Arch Microbiol 174:135–142 Meyer J-M, Hohnadel D, Halle F (1989) Cepabactin from Pseudomonas cepacia, a new type of siderophore. J Gen Microbiol 135:1479–1487 Meyer J-M, Azelvandre P, Georges C (1992) Iron metabolism in Pseudomonas: salicylic acid, a siderophore of Pseudomonas fluorescens CHA0. BioFactors 4:23–27 Meyer J-M, Van VT, Stintzi A, Berge O, Winkelmann G (1995) Ornibactin production and transport properties in strains of Burkholderia vietnamiensis and Burkholderia cepacia (formerly Pseudomonas cepacia). BioMetals 8:309–317 Michel L, Gonzalez N, Jagdeep S, Nguyen-Ngoc T, Reimmann C (2005) PchR-box recognition by the AraC-type regulator PchR of Pseudomonas aeruginosa requires the siderophore pyochelin as an effector. Mol Microbiol 58:495–509 Mislin GLA, Hoegy F, Cobessi D, Poole K, Rognan D, Schalk IJ (2006) Binding properties of pyochelin and structurally related molecules to FptA of Pseudomonas aeruginosa. J Mol Biol 357:1437–1448 Muller K, Matzanke BF, Schunemann V, Trautwein AX, Hantke K (1998) FhuF, an iron-regulated protein of Escherichia coli with a new type of [Fe-S] center. Eur J Biochem 258:1001–1008 Ochsner U, Vasil A, Vasil ML (1995) Role of the ferric uptake regulator of Pseudomonas aeruginosa in the regulation of siderophores and exotoxin A expression: purification and activity on iron-regulated promoters. J Bacteriol 177:7194–7201 Ochsner U, Wilderman PJ, Vasil AI, Vasil ML (2002) GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45:1277–1287 O’Cuiv P, Clarke P, Lynch D, O’Connell M (2004) Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, respectively. J Bacteriol 186:2996–3005 Ogawa K, Tobe N (1966) A spectrophotometric study of the complex formation between iron(III) and sulfosalicylic acid. Bull Chem Soc Jpn 39:223–227 Ohta A, Takahashi N, Shirokoma Y, Yuasa K (1990) Heterocycles 30:875–884 Okujo N, Saito M, Yamamoto S, Yoshida T, Miyoshi S, Shimoda S (1994) Structure of vulnibactin, a new polyamine-containing siderophore from Vibrio vulnificus. BioMetals 7:109–116 Parke JL, Gurian-Sherman D (2001) Diversity of the Burkholderia cepacia complex and implications for risk assessment of biological control strains. Annu Rev Phytopathol 39:225–258 Patel HM, Walsh CT (2001) In vitro reconstitution of the Pseudomonas aeruginosa nonribosomal peptide synthesis of pyochelin: characterization of backbone tailoring thiazoline reductase and N-methyltransferase activities. Biochemistry 40:9023–9031 Patel HM, Tao J, Walsh CT (2003) Epimerization of an l-cysteinyl to a d-cysteinyl residue during thiazoline ring formation in siderophore chain elongation by pyochelin synthetase from Pseudomonas aeruginosa. Biochemistry 42:10514–10527 Paulsen IT, Press CM, Ravel J, et al (2005) Complete genome sequence of the plant commensal Pseudomonas fluorescens Pf-5. Nat Biotechnol 23:873–878 Payne GW, Ramette A, Rose HL, et al (2006) Application of a recA gene-based identification approach to the maize rhizosphere reveals novel diversity in Burkholderia species. FEMS Microbiol Lett 259:126–132 Peterson T, Nielands JB (1979) Revised structure of a catecholamide spermidine siderophore. Tetrahedron Lett 20:4805–4808 Quadri LEN (2000) Assembly of aryl-capped siderophores by modular peptide synthetases and polyketide synthetases. Mol Microbiol 37:1–12 Quadri LEN, Sello J, Keating TA, Weinreb PH, Walsh CT (1998) Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin. Chem Biol 5:631–645 Quadri LEN, Keating TA, Patel HM, Walsh CT (1999) Assembly of the Pseudomonas aeruginosa nonribosomal peptide siderophore pyochelin: in vitro reconstitution of aryl-4,2-bisthiazoline synthetase activity from PchD, PchE and PchF. Biochemistry 38:14941–14954 Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941 Ratledge C, Hall MJ (1972) Isolation and properties of auxotrophic mutants of Mycobacterium smegmatis requiring either salicylic acid or mycobactin. J Gen Microbiol 72:143–150 Ratledge C, Winder FG (1962) The accumulation of salicylic acid by mycobacteria during growth on iron-deficient medium. Biochem J 84:501–506 Ratledge C, Macham LP, Brown KA, Marshall BJ (1974) Iron transport in Mycobacterium smegmatis: a restricted role for salicylic acid in the extracellular environment. Biochim Biophys Acta 372:39–51 Ravel J, Cornelis P (2003) Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11:195–200 Reik R, Spilker T, LiPuma JJ (2005) Distribution of Burkholderia cepacia complex species among isolates recovered from persons with or without cystic fibrosis. J Clin Microbiol 43:2926–2928 Reimmann C, Serino L, Beyeler M, Haas D (1998) Dihydroaeruginoic acid synthetase and pyochelin synthetase, products of the pchEF genes are induced by extracellular pyochelin in Pseudomonas aeruginosa. Microbiology 144:3135–3148 Reimmann C, Patel HM, Serino L, Barone M, Walsh CT, Haas D (2001) Essential PchG-dependent reduction in pyochelin biosynthesis of Pseudomonas aeruginosa. J Bacteriol 183:813–820 Reimmann C, Patel HM, Walsh CT, Haas D (2004) PchC thioesterase optimizes nonribosomal biosynthesis of the peptide siderophore pyochelin in Pseudomonas aeruginosa. J Bacteriol 186:6367–6373 Rinehart KL, Staley AL, Wilson SR, Ankenbauer RG, Cox CD (1995) Stereochemical assignment of the pyochelins. J Org Chem 60:2786–2791 Rodley PD, Romling U, Tummler B (1995) A physical genome map of the Burkholderia cepacia type strain. Mol Microbiol 17:57–67 Rodriguez GM, Voskuil MI, Gold B, Schoolnik GK, Smith I (2002) ideR, an essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response. Infect Immun 70:3371–3381 Saxena B, Modi M, Modi VV (1986) Isolation and characterization of siderophores from Azospirillum lipoferum D-2. J Gen Microbiol 132:2219–2224 Schalk IJ, Yue WW, Buchanan SK (2004) Recognition of iron-free siderophores by TonB-dependent iron transporters. Mol Microbiol 54:14–22 Schlegel K, Taraz K, Budzikiewicz H (2004) The stereoisomers of pyochelin, a siderophore of Pseudomonas aeruginosa. BioMetals 17:409–414 Schmidli-Sacherer P, Keel C, Defago G (1997) The global regulator GacA of Pseudomonas fluorescens CHA0 is required for suppression of root diseases in dicotyledons but not in Graminae. Plant Pathol 46:80–90 Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56 Serino L, Reimmann C, Baur H, Beyeler M, Visca P, Haas D (1995) Structural genes for salicylate biosynthesis from chorismate in Pseudomonas aeruginosa. Mol Gen Genet 249:217–228 Serino L, Reimmann C, Visca P, Beyeler M, Della Chiesa V, Haas D (1997) Biosynthesis of pyochelin and dihydroaeruginoic acid requires the iron-regulated pchDCBA operon in Pseudomonas aeruginosa. J Bacteriol 179:248–257 Sokol PA (1984) Production of the ferripyochelin outer-membrane receptor by Pseudomonas species. FEMS Microbiol Lett 23:313–317 Sokol PA (1986) Production and utilization of pyochelin by clinical isolates of Pseudomonas cepacia. J Clin Microbiol 23:560–562 Sokol PA (1987) Tn5 insertion mutants of Pseudomonas aeruginosa deficient in surface expression of ferripyochelin-binding protein. J Bacteriol 169:3365–3368 Sokol PA, Woods DE (1983) Demonstration of an iron-siderophore-binding protein in the outer membrane of Pseudomonas aeruginosa. Infect Immun 40:665–669 Sokol PA, Lewis CJ, Dennis JJ (1992) Isolation of a novel siderophore from Pseudomonas cepacia. J Med Microbiol 36:184–189 Sokol PA, Darling P, Woods DE, Mahenthiralingam E, Kooi C (1999) Role of ornibactin biosynthesis in the virulence of Burkholderia cepacia: characterization of pvdA, the gene encoding l-ornithine N 5-oxygenase. Infect Immun 67:4443–4455 Sokol PA, Darling P, Lewenza S, Corbett CR, Kooi CD (2000) Identification of a siderophore receptor required for ferric ornibactin uptake in Burkholderia cepacia. Infect Immun 68:6554–6560 Speert DP (2001) Understanding Burkholderia cepacia: epidemiology, genomovars and virulence. Infect Med 18:49–56 Speert DP (2002) Advances in Burkholderia cepacia complex. Pediatr Respir Rev 3:230–235 Speert DP, Henry D, Vandamme P, Corey M, Mahenthiralingam E (2002) Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg Infect Dis 8:181–187 Sriyosachati S, Cox CD (1986) Siderophore-mediated iron acquisition from transferrin by Pseudomonas aeruginosa. Infect Immun 52:885–891 Stanier RY, Palleroni NJ, Doudoroff M (1966) Aerobic pseudomonads—a taxonomic study. J Gen Microbiol 43:159–271 Stephan H, Freund S, Beck W, Jung G, Meyer J-M, Winkelmann G (1993) Ornibactins—a new family of siderophores from Pseudomonas cepacia. BioMetals 6:93–100 Stojiljkovic I, Perkins-Balding D (2002) Processing of heme and heme-containing proteins by bacteria. DNA Cell Biol 21:281–295 Tabacchioni S, Bevivino A, Dalmastri C, Chiarini L (2002) Burkhoderia cepacia complex in the rhizosphere: a minireview. Ann Microbiol 52:103–117 Taraz K, Ehlert G, Geisen K, Budzikiewicz H, Korth H, Pulverer G (1990) Protochelin, ein catecholat-siderophor aus einem bakterium (DMS Nr. 5746). Z Naturforsch 45b:1327–1332 Tseng C-F, Burger A, Mislin GLA, et al (2006) Bacterial siderophores: the solution stoichiometry and coordination of the Fe(III) complexes of pyochelin and related compounds. J Biol Inorg Chem 11:419–432 Tuanyok A, Kim HS, Nierman WC, et al (2005) Genome-wide expression analysis of iron regulation in Burkholderia pseudomallei and Burkholderia mallei using DNA microarrays. FEMS Microbiol Lett 252:327–335 Visca P, Colotti G, Serino L, Verzili D, Orsi N, Chiancone E (1992) Metal regulation of siderophore synthesis in Pseudomonas aeruginosa and functional effects of siderophore-metal complexes. Appl Environ Microbiol 58:2886–2893 Visca P, Ciervo A, Sanfilippo V, Orsi N (1993) Iron-regulated salicylate synthesis by Pseudomonas spp. J Gen Microbiol 139:1995–2001 Visca P, Ciervo A, Orsi N (1994) Cloning and nucleotide sequence of the pvdA gene encoding the pyoverdin biosynthetic enzyme l-ornithine N 5-oxygenase in Pseudomonas aeruginosa. J Bacteriol 176:1128–1140 Visca P, Leoni L, Wilson MJ, Lamont IL (2002) Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45:1177–1190 Visser MB, Majumdar S, Hani E, Sokol PA (2004) Importance of the ornibactin and pyochelin siderophore transport systems in Burkholderia cenocepacia lung infections. Infect Immun 72:2850–2857 Wandersman C, Stojiljkovic I (2000) Bacterial heme sources: the role of heme, hemoprotein receptors and hemophores. Curr Opin Microbiol 3:215–220 Wang J, Lory S, Ramphal R, Jin S (1996) Isolation and characterisation of Pseudomonas aeruginosa genes inducible by respiratory mucus derived from cystic fibrosis patients. Mol Microbiol 22:1005–1012 Weingart C, White CE, Liu S, et al (2005) Direct binding of the quorum sensing regulator CepR of Burkholderia cenocepacia to two target promoters in vitro. Mol Microbiol 57:452–467 Whitby PW, VanWagoner T, Springer JM, Morton DJ, Seale TW, Stull TL (2006) Burkholderia cenocepacia utilizes ferritin as an iron source. J Med Microbiol 55:661–668 Wilson MJ, McMorran BJ, Lamont IL (2001) Analysis of promoters recognized by PvdS, an extracytoplasmic-function sigma factor protein from Pseudomonas aeruginosa. J Bacteriol 183:2151–2155 Wyckoff EE, Lopreato GF, Tipton KA, Payne SM (2005) Shigella dysenteriae ShuS promotes utilization of heme as an iron source and protects against heme toxicity. J Bacteriol 187:5658–5664 Zamri A, Abdallah MA (2000) An improved stereocontrolled synthesis of pyochelin, siderophore of Pseudomonas aeruginosa and Burkholderia cepacia. Tetrahedron 56:249–256