Investigation of the multifaceted iron acquisition strategies of Burkholderia cenocepacia

BioMetals

Volumn 28, Issue 2, 2015, Pages 367-380

  Tyrrell, J ^a   Whelan, N ^a   Wright, C ^a   Sa Correia I ^b   McClean, S ^a   Thomas, M ^c   Callaghan, Máire ^a  

^a DUBLIN INSTITUTE OF TECHNOLOGY   (Ireland)

^b INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Bacterial adaptation; Burkholderia cenocepacia; Cystic fibrosis; Iron acquisition; Ornibactin; Siderophore

Indexed keywords

HEME; IRON; SIDEROPHORE;

ADAPTATION; BACTERIAL GENE; BACTERIAL PNEUMONIA; BIOSYNTHESIS; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA INFECTION; CYSTIC FIBROSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; TRANSCRIPTION INITIATION;

ADAPTATION, PHYSIOLOGICAL; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA INFECTIONS; CYSTIC FIBROSIS; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HEME; HUMANS; IRON; PNEUMONIA, BACTERIAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIDEROPHORES; TRANSCRIPTIONAL ACTIVATION;

EID: 84939987990     PISSN: 09660844     EISSN: 15728773     Source Type: Journal    
DOI: 10.1007/s10534-015-9840-1     Document Type: Article

References (68)

1. Agnoli K, Lowe CA, Farmer KL, Husnain SI, Thomas MS (2006) The ornibactin biosynthesis and transport genes of Burkholderia cenocepacia are regulated by an extracytoplasmic function sigma factor which is a part of the Fur regulon. J Bacteriol 188:3631-3644. doi: 10.1128/JB.188.10.3631-3644.2006
2. Asghar AH, Shastri S, Dave E, Wowk I, Agnoli K, Cook AM, Thomas MS (2011) The pobA gene of Burkholderia cenocepacia encodes a group I Sfp-type phosphopantetheinyltransferase required for biosynthesis of the siderophores ornibactin and pyochelin. Microbiology 157(2):349-361. doi: 10.1099/mic.0.045559-0
3. Baker HM, Baker EN (2004) Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals 17:209-216
4. Bakkal S, Robinson SM, Ordonez CL, Waltz DA, Riley MA (2010) Role of bacteriocins in mediating interactions of bacterial isolates taken from cystic fibrosis patients. Microbiology 156:2058-2067. doi: 10.1099/mic.0.036848-0
5. Brock JH (2012) Lactoferrin-50 years on. Biochem Cell Biol 90:245-251. doi: 10.1139/o2012-018
6. Caraher EM, Gumulapurapu K, Taggart CC, Murphy P, McClean S, Callaghan M (2007) The effect of recombinant human lactoferrin on growth and the antibiotic susceptibility of the cystic fibrosis pathogen Burkholderia cepacia complex when cultured planktonically or as biofilms. J Antimicrob Chemother 60(3):546-554
7. Caza M, Kronstad JW (2013) Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front Cell Infect Microbiol 3:80. doi: 10.3389/fcimb.2013.00080
8. Costello A, Reen FJ, O'Gara F, Callaghan M, McClean S (2014) Inhibition of co-colonizing cystic fibrosis-associated pathogens by Pseudomonas aeruginosa and Burkholderia multivorans. Microbiology 160:1474-1487. doi: 10.1099/mic.0.074203-0
9. Coutinho CP, de Carvalho CC, Madeira A, Pinto-de-Oliveira A, Sa-Correia I (2011a) Burkholderia cenocepacia phenotypic clonal variation during a 3.5-year colonization in the lungs of a cystic fibrosis patient. Infect Immun 79:2950-2960. doi: 10.1128/IAI.01366-10
10. Coutinho CP, Dos Santos SC, Madeira A, Mira NP, Moreira AS, Sa-Correia I (2011b) Long-term colonization of the cystic fibrosis lung by Burkholderia cepacia complex bacteria: epidemiology, clonal variation, and genome-wide expression alterations. Front Cell Infect Microbiol 1:12. doi: 10.3389/fcimb.2011.00012
11. Cunha MV, Leitao JH, Mahenthiralingam E, Vandamme P, Lito L, Barreto C, Salgado MJ, Sa-Correia I (2003) Molecular analysis of Burkholderia cepacia complex isolates from a Portuguese cystic fibrosis center: a 7-year study. J Clin Microbiol 41:4113-4120
12. Darling P, Chan M, Cox AD, Sokol PA (1998) Siderophore production by cystic fibrosis isolates of Burkholderia cepacia. Infect Immun 66:874-877
13. Davis PB, Drumm M, Konstan MW (1996) Cystic fibrosis. Am J Respir Crit Care Med 154:1229-1256. doi: 10.1164/ajrccm.154.5.8912731
14. De Vos D, De Chial M, Cochez C, Jansen S, Tummler B, Meyer JM, Cornelis P (2001) Study of pyoverdine type and production by Pseudomonas aeruginosa isolated from cystic fibrosis patients: prevalence of type II pyoverdine isolates and accumulation of pyoverdine-negative mutations. Arch Microbiol 175:384-388
15. Drevinek P, Mahenthiralingam E (2010) Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin Microbiol Infect 16:821-830. doi: 10.1111/j.1469-0691.2010.03237.x
16. Drevinek P, Holden MT, Ge Z, Jones AM, Ketchell I, Gill RT, Mahenthiralingam E (2008) Gene expression changes linked to antimicrobial resistance, oxidative stress, iron depletion and retained motility are observed when Burkholderia cenocepacia grows in cystic fibrosis sputum. BMC Infect Dis 8:121. doi: 10.1186/1471-2334-8-121
17. Ganz T (2009) Iron in innate immunity: starve the invaders. Curr Opin Immunol 21:63-67. doi: 10.1016/j.coi.2009.01.011
18. Ghio AJ, Roggli VL, Soukup JM, Richards JH, Randell SH, Muhlebach MS (2013) Iron accumulates in the lavage and explanted lungs of cystic fibrosis patients. J Cyst Fibros 12:390-398. doi: 10.1016/j.jcf.2012.10.010
19. Harrison F, Paul J, Massey RC, Buckling A (2008) Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J 2:49-55. doi: 10.1038/ismej.2007.96
20. Henry DA, Campbell ME, LiPuma JJ, Speert DP (1997) Identification of Burkholderia cepacia isolates from patients with cystic fibrosis and use of a simple new selective medium. J Clin Microbiol 35:614-619
21. Hoiby N, Ciofu O, Bjarnsholt T (2010) Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 5:1663-1674. doi: 10.2217/fmb.10.125
22. Holden MT, Seth-Smith HM, Crossman LC, Sebaihia M, Bentley SD, Cerdeño-Tárraga AM, Thomson NR, Bason N, Quail MA, Sharp S, Cherevach I, Churcher C, Goodhead I, Hauser H, Holroyd N, Mungall K, Scott P, Walker D, White B, Rose H, Iversen P, Mil-Homens D, Rocha EP, Fialho AM, Baldwin A, Dowson C, Barrell BG, Govan JR, Vandamme P, Hart CA, Mahenthiralingam E, Parkhill J (2009) The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J Bacteriol 191(1):261-277. doi: 10.1128/JB.01230-08. Erratum in: J Bacteriol 191(8):2907
23. Hunter RC, Asfour F, Dingemans J, Osuna BL, Samad T, Malfroot A, Cornelis P, Newman DK (2013) Ferrous iron is a significant component of bioavailable iron in cystic fibrosis airways. MBio 4(4):pii:e00557-13. doi: 10.1128/mBio.00557-13
24. Hutchison ML, Poxton IR, Govan JR (1998) Burkholderia cepacia produces a hemolysin that is capable of inducing apoptosis and degranulation of mammalian phagocytes. Infect Immun 66:2033-2039
25. Imperi F, Tiburzi F, Visca P (2009) Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 106:20440-20445. doi: 10.1073/pnas.0908760106
26. Isles A, Maclusky I, Corey M, Gold R, Prober C, Fleming P, Levison H (1984) Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J Pediatr 104:206-210
27. Jacquot J, Tabary O, Le Rouzic P, Clement A (2008) Airway epithelial cell inflammatory signalling in cystic fibrosis. Int J Biochem Cell Biol 40:1703-1715. doi: 10.1016/j.biocel.2008.02.002
28. Konings AF, Martin LW, Sharples KJ, Roddam LF, Latham R, Reid DW, Lamont IL (2013) Pseudomonas aeruginosa uses multiple pathways to acquire iron during chronic infection in cystic fibrosis lungs. Infect Immun 81:2697-2704
29. Kooi C, Corbett CR, Sokol PA (2005) Functional analysis of the Burkholderia cenocepacia ZmpA metalloprotease. J Bacteriol 187:4421-4429. doi: 10.1128/JB.187.13.4421-4429.2005
30. Kvitko BH, Goodyear A, Propst KL, Dow SW, Schweizer HP (2012) Burkholderia pseudomallei known siderophores and hemin uptake are dispensable for lethal murine melioidosis. PLoS Negl Trop Dis 6:e1715. doi: 10.1371/journal.pntd.0001715
31. Lubamba B, Dhooghe B, Noel S, Leal T (2012) Cystic fibrosis: insight into CFTR pathophysiology and pharmacotherapy. Clin Biochem 45:1132-1144. doi: 10.1016/j.clinbiochem.2012.05.034
32. Lyczak JB, Cannon CL, Pier GB (2002) Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15:194-222
33. Madeira A, Santos PM, Coutinho CP, Pinto-de-Oliveira A, Sa-Correia I (2011) Quantitative proteomics (2-D DIGE) reveals molecular strategies employed by Burkholderia cenocepacia to adapt to the airways of cystic fibrosis patients under antimicrobial therapy. Proteomics 11:1313-1328. doi: 10.1002/pmic.201000457
34. Madeira A et al (2013) Proteomic profiling of Burkholderia cenocepacia clonal isolates with different virulence potential retrieved from a cystic fibrosis patient during chronic lung infection. PLoS One 8:e83065. doi: 10.1371/journal.pone.0083065
35. Mahenthiralingam E, Vandamme P (2005) Taxonomy and pathogenesis of the Burkholderia cepacia complex. Chronic Respir Dis 2:209-217
36. Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3:144-156. doi: 10.1038/nrmicro1085
37. Mahenthiralingam E, Baldwin A, Dowson CG (2008) Burkholderia cepacia complex bacteria: opportunistic pathogens with important natural biology. J Appl Microbiol 104:1539-1551. doi: 10.1111/j.1365-2672.2007.03706.x
38. Martin LW, Reid DW, Sharples KJ, Lamont IL (2011) Pseudomonas siderophores in the sputum of patients with cystic fibrosis. Biometals 24:1059-1067
39. Marvig RL, Damkiaer S, Khademi SM, Markussen TM, Molin S, Jelsbak L (2014) Within-host evolution of Pseudomonas aeruginosa reveals adaptation toward iron acquisition from hemoglobin. MBio 5:e00966-00914. doi: 10.1128/mBio.00966-14
40. Masson PL, Heremans JF (1968) Metal-combining properties of human lactoferrin (red milk protein). 1. The involvement of bicarbonate in the reaction. Eur J Biochem FEBS 6:579-584
41. Mathew A, Eberl L, Carlier AL (2014) A novel siderophore-independent strategy of iron uptake in the genus Burkholderia. Mol Microbiol 91:805-820. doi: 10.1111/mmi.12499
42. McKenney D, Brown KE, Allison DG (1995) Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication. J Bacteriol 177:6989-6992
43. Meyer JM, Stintzi A, De Vos D, Cornelis P, Tappe R, Taraz K, Budzikiewicz H (1997) Use of siderophores to type pseudomonads: the three Pseudomonas aeruginosa pyoverdine systems. Microbiology 143(Pt 1):35-43
44. Mietzner TA, Morse SA (1994) The role of iron-binding proteins in the survival of pathogenic bacteria. Annu Rev Nutr 14:471-493. doi: 10.1146/annurev.nu.14.070194.002351
45. Moon CD, Zhang XX, Matthijs S, Schafer M, Budzikiewicz H, Rainey PB (2008) Genomic, genetic and structural analysis of pyoverdine-mediated iron acquisition in the plant growth-promoting bacterium Pseudomonas fluorescens SBW25. BMC Microbiol 8:7. doi: 10.1186/1471-2180-8-7
46. Mossialos D, Amoutzias GD (2009) Role of siderophores in cystic fibrosis pathogenesis: foes or friends? Int J Med Microbiol 299:87-98. doi: 10.1016/j.ijmm.2008.06.008
47. Nguyen AT, O'Neill MJ, Watts AM, Robson CL, Lamont IL, Wilks A, Oglesby-Sherrouse AG (2014) Adaptation of iron homeostasis pathways by a Pseudomonas aeruginosa pyoverdine mutant in the cystic fibrosis lung. J Bacteriol 196:2265-2276. doi: 10.1128/JB.01491-14
48. Payne SM (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol 235:329-344
49. Peeters C, Zlosnik JE, Spilker T, Hird TJ, LiPuma JJ, Vandamme P (2013) Burkholderia pseudomultivorans sp. nov., a novel Burkholderia cepacia complex species from human respiratory samples and the rhizosphere. Syst Appl Microbiol 36:483-489. doi: 10.1016/j.syapm.2013.06.003
50. Ravel J, Cornelis P (2003) Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11:195-200
51. Riedel K et al (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:3249-3262
52. Schade AL, Reinhart RW, Levy H (1949) Carbon dioxide and oxygen in complex formation with iron and siderophilin, the iron-binding component of human plasma. Arch Biochem 20:170-172
53. 3+ by transferrin. Implications for the interlocking sites hypothesis. J Biol Chem 250:2182-2188
54. Shalom G, Shaw JG, Thomas MS (2007) In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153:2689-2699. doi: 10.1099/mic.0.2007/006585-0
55. 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
56. 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
57. Stites SW, Plautz MW, Bailey K, O'Brien-Ladner AR, Wesselius LJ (1999) Increased concentrations of iron and isoferritins in the lower respiratory tract of patients with stable cystic fibrosis. Am J Respir Crit Care Med 160:796-801. doi: 10.1164/ajrccm.160.3.9811018
58. Tashiro Y, Ichikawa S, Nakajima-Kambe T, Uchiyama H, Nomura N (2010) Pseudomonas quinolone signal affects membrane vesicle production in not only gram-negative but also gram-positive bacteria. Microbes Environ 25:120-125
59. Thomas MS (2007) Iron acquisition mechanisms of the Burkholderia cepacia complex. Biometals 20:431-452. doi: 10.1007/s10534-006-9065-4
60. Tomlin KL, Coll OP, Ceri H (2001) Interspecies biofilms of Pseudomonas aeruginosa and Burkholderia cepacia. Can J Microbiol 47:949-954
61. Turi JL, Yang F, Garrick MD, Piantadosi CA, Ghio AJ (2004) The iron cycle and oxidative stress in the lung. Free Radic Biol Med 36:850-857. doi: 10.1016/j.freeradbiomed.2003.12.008
62. Vanlaere E et al (2008) Burkholderia latens sp. nov., Burkholderia diffusa sp. nov., Burkholderia arboris sp. nov., Burkholderia seminalis sp. nov. and Burkholderia metallica sp. nov., novel species within the Burkholderia cepacia complex. Int J Syst Evol Microbiol 58:1580-1590. doi: 10.1099/ijs.0.65634-0
63. Vanlaere E et al (2009) Taxon K, a complex within the Burkholderia cepacia complex, comprises at least two novel species, Burkholderia contaminans sp. nov. and Burkholderia lata sp. nov. Int J Syst Evol Microbiol 59:102-111. doi: 10.1099/ijs.0.001123-0
64. 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
65. Weaver VB, Kolter R (2004) Burkholderia spp. alter Pseudomonas aeruginosa through iron sequestration. J Bacteriol 186:2376-2384
66. Whitby PW, Vanwagoner TM, Springer JM, Morton DJ, Seale TW, Stull TL (2006) Burkholderia cenocepacia utilizes ferritin as an iron source. J Med Microbiol 55:661-668. doi: 10.1099/jmm.0.46199-0
67. Wolz C et al (1994) Iron release from transferrin by pyoverdin and elastase from Pseudomonas aeruginosa. Infect Immun 62:4021-4027
68. Wright C, Herbert G, Pilkington R, Callaghan M, McClean S (2010) Real-time PCR method for the quantification of Burkholderia cepacia complex attached to lung epithelial cells and inhibition of that attachment. Lett Appl Microbiol 50:500-506