Molybdate transporter ModABC is important for Pseudomonas aeruginosa chronic lung infection

BMC Research Notes

Volumn 9, Issue 1, 2016, Pages

  Périnet, Simone ^a   Jeukens, Julie ^a   Kukavica Ibrulj, Irena ^a   Ouellet, Myriam M ^a,b   Charette, Steve J ^a,b   Levesque, Roger C ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Anaerobic conditions; Animal model; Biofilm; Chronic lung infection; Cystic fibrosis; ModA; Molybdate; Pseudomonas aeruginosa

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; MOLYBDENUM; MOLYBDIC ACID; RECOMBINANT PROTEIN;

ANIMAL; CHRONIC DISEASE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETICS; ION TRANSPORT; LUNG; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; PATHOGENICITY; PATHOLOGY; PNEUMONIA; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RAT; SPRAGUE DAWLEY RAT; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; CARRIER PROTEINS; CHRONIC DISEASE; CLONING, MOLECULAR; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; ION TRANSPORT; LUNG; MOLYBDENUM; MUTAGENESIS, INSERTIONAL; PNEUMONIA; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; VIRULENCE;

EID: 84954104237     PISSN: None     EISSN: 17560500     Source Type: Journal    
DOI: 10.1186/s13104-016-1840-x     Document Type: Article

References (49)

1. Rosenfeld M, Gibson RL, McNamara S, Emerson J, Burns JL, Castile R, et al. Early pulmonary infection, inflammation, and clinical outcomes in infants with cystic fibrosis. Pediatr Pulmonol. 2001;32(5):356-66. doi: 10.1002/ppul.1144.
2. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature. 2000;406(6799):959-64. doi: 10.1038/35023079.
3. Silby MW, Winstanley C, Godfrey SA, Levy SB, Jackson RW. Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev. 2011;35(4):652-80. doi: 10.1111/j.1574-6976.2011.00269.x.
4. Balasubramanian D, Schneper L, Kumari H, Mathee K. A dynamic and intricate regulatory network determines Pseudomonas aeruginosa virulence. Nucleic Acids Res. 2013;41(1):1-20. doi: 10.1093/nar/gks1039.
5. Worlitzsch D, Tarran R, Ulrich M, Schwab U, Cekici A, Meyer KC, et al. Effects of reduced mucus oxygen concentration in airway Pseudomonas infections of cystic fibrosis patients. J Clin Invest. 2002;109(3):317-25. doi: 10.1172/JCI13870.
6. Tunney MM, Field TR, Moriarty TF, Patrick S, Doering G, Muhlebach MS, et al. Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am J Respir Crit Care Med. 2008;177(9):995-1001. doi: 10.1164/rccm.200708-1151OC.
7. Alvarez-Ortega C, Harwood CS. Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol Microbiol. 2007;65(1):153-65. doi: 10.1111/j.1365-2958.2007.05772.x.
8. Schobert M, Jahn D. Anaerobic physiology of Pseudomonas aeruginosa in the cystic fibrosis lung. Int J Med Microbiol. 2010;300(8):549-56. doi: 10.1016/j.ijmm.2010.08.007.
9. Yoon SS, Hennigan RF, Hilliard GM, Ochsner UA, Parvatiyar K, Kamani MC, et al. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev Cell. 2002;3(4):593-603.
10. Carlson CA, Ingraham JL. Comparison of denitrification by Pseudomonas stutzeri, Pseudomonas aeruginosa, and Paracoccus denitrificans. Appl Environ Microbiol. 1983;45(4):1247-53.
11. Arai H. Regulation and Function of Versatile Aerobic and Anaerobic Respiratory Metabolism in Pseudomonas aeruginosa. Front Microbiol. 2011;2:103. doi: 10.3389/fmicb.2011.00103.
12. Grunden AM, Shanmugam KT. Molybdate transport and regulation in bacteria. Arch Microbiol. 1997;168(5):345-54.
13. Frausto da Silva JJR, Williams RJP. The biological chemistry of the elements: the inorganic chemistry of life. Oxford: University press;1993.
14. Schwartz G, Hagedoorn P-L, Fischer K. Molybdate and tungstate: uptake, homeostatis, cofactors, and enzymes. In: Nies DH, Silver S, editors. Molecular Microbiology of Heavy Metals. Berlin: Springer-Verlag; 2007.
15. Potvin E, Lehoux DE, Kukavica-Ibrulj I, Richard KL, Sanschagrin F, Lau GW, et al. In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. Environ Microbiol. 2003;5(12):1294-308. doi: 10.1046/j.1462-2920.2003.00542.x.
16. Rech S, Deppenmeier U, Gunsalus RP. Regulation of the molybdate transport operon, modABCD, of Escherichia coli in response to molybdate availability. J Bacteriol. 1995;177(4):1023-9.
17. Self WT, Grunden AM, Hasona A, Shanmugam KT. Molybdate transport. Res Microbiol. 2001;152(3-4):311-21.
18. Pederick VG, Eijkelkamp BA, Ween MP, Begg SL, Paton JC, McDevitt CA. Acquisition and role of molybdate in Pseudomonas aeruginosa. Appl Environ Microbiol. 2014;80(21):6843-52. doi: 10.1128/aem.02465-14.
19. Lehoux DE, Sanschagrin F, Levesque RC. Identification of in vivo essential genes from Pseudomonas aeruginosa by PCR-based signature-tagged mutagenesis. FEMS Microbiol Lett. 2002;210(1):73-80.
20. Sanschagrin F, Kukavica-Ibrulj I, Levesque RC. Essential genes in the infection model of Pseudomonas aeruginosa PCR-based signature-tagged mutagenesis. Methods Mol Biol. 2008;416:61-82. doi: 10.1007/978-1-59745-321-9-5.
21. Kukavica-Ibrulj I, Bragonzi A, Paroni M, Winstanley C, Sanschagrin F, O'Toole GA, et al. In Vivo Growth of Pseudomonas aeruginosa Strains PAO1 and PA14 and the hypervirulent strain LESB58 in a rat model of chronic lung infection. J Bacteriol. 2008;190(8):2804-13. doi: 10.1128/jb.01572-07.
22. Winsor GL, Van Rossum T, Lo R, Khaira B, Whiteside MD, Hancock RE, et al. Pseudomonas Genome Database: facilitating user-friendly, comprehensive comparisons of microbial genomes. Nucleic Acids Res. 2009;37:483-8. doi: 10.1093/nar/gkn861.
23. Miranda KM, Espey MG, Wink DA. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide. 2001;5(1):62-71. doi: 10.1006/niox.2000.0319.
24. Jeukens J, Boyle B, Kukavica-Ibrulj I, Ouellet MM, Aaron SD, Charette SJ, et al. Comparative genomics of isolates of a Pseudomonas aeruginosa epidemic strain associated with chronic lung infections of cystic fibrosis patients. PLoS One. 2014;9(2):e87611. doi: 10.1371/journal.pone.0087611.
25. O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp. 2011;47:2437. doi: 10.3791/2437.
26. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 1998;28(3):449-61.
27. Cash HA, Woods DE, McCullough B, Johanson WG Jr, Bass JA. A rat model of chronic respiratory infection with Pseudomonas aeruginosa. Am Rev Respir Dis. 1979;119(3):453-9.
28. Filion G, Charette SJ. Assessing Pseudomonas aeruginosa virulence using a nonmammalian host: Dictyostelium discoideum. Method Mol Biol. 2014;1149:671-80.
29. Froquet R, Lelong E, Marchetti A, Cosson P. Dictyostelium discoideum: a model host to measure bacterial virulence. Nat Protoc. 2009;4(1):25-30. doi: 10.1038/nprot.2008.212.
30. Vizvaryova M, Valkova D. Transposons - the useful genetic tools. Biologia, Bratislava. 2004;59(3):309-18.
31. Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, et al. Pseudomonas genome database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res. 2011;39:596-600. doi: 10.1093/nar/gkq869.
32. Hollenstein K, Dawson RJ, Locher KP. Structure and mechanism of ABC transporter proteins. Curr Opin Struct Biol. 2007;17(4):412-8. doi: 10.1016/j.sbi.2007.07.003.
33. Glaser JH, DeMoss JA. Phenotypic restoration by molybdate of nitrate reductase activity in chlD mutants of Escherichia coli. J Bacteriol. 1971;108(2):854-60.
34. Lee JH, Wendt JC, Shanmugam KT. Identification of a new gene, molR, essential for utilization of molybdate by Escherichia coli. J Bacteriol. 1990;172(4):2079-87.
35. Gisin J, Muller A, Pfander Y, Leimkuhler S, Narberhaus F, Masepohl B. A Rhodobacter capsulatus member of a universal permease family imports molybdate and other oxyanions. J Bacteriol. 2010;192(22):5943-52. doi: 10.1128/JB.00742-10.
36. O'May CY, Reid DW, Kirov SM. Anaerobic culture conditions favor biofilm-like phenotypes in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. FEMS Immunol Med Microbiol. 2006;48(3):373-80.
37. Kukavica-Ibrulj I, Sanschagrin F, Peterson A, Whiteley M, Boyle B, MacKay J, et al. Functional genomics of PycR, a LysR family transcriptional regulator essential for maintenance of Pseudomonas aeruginosa in the rat lung. Microbiology. 2008;154(7):2106-18. doi: 10.1099/mic.0.2007/011239-0.
38. Lau GW, Britigan BE, Hassett DJ. Pseudomonas aeruginosa oxyr is required for full virulence in rodent and insect models of infection and for resistance to human neutrophils. Infect Immun. 2005;73(4):2550-3. doi: 10.1128/iai.73.4.2550-2553.2005.
39. Dallaire-Dufresne S, Paquet VE, Charette SJ. Dictyostelium discoideum: a model for the study of bacterial virulence. Can J Microbiol. 2011;57(9):699-707. doi: 10.1139/w11-072.
40. Alibaud L, Kohler T, Coudray A, Prigent-Combaret C, Bergeret E, Perrin J, et al. Pseudomonas aeruginosa virulence genes identified in a Dictyostelium host model. Cell Microbiol. 2008;10(3):729-40. doi: 10.1111/j.1462-5822.2007.01080.x.
41. Hassett DJ, Sutton MD, Schurr MJ, Herr AB, Caldwell CC, Matu JO. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol. 2009;17(3):130-8. doi: 10.1016/j.tim.2008.12.003.
42. Palmer KL, Brown SA, Whiteley M. Membrane-bound nitrate reductase is required for anaerobic growth in cystic fibrosis sputum. J Bacteriol. 2007;189(12):4449-55. doi: 10.1128/JB.00162-07.
43. Hoiby N, Ciofu O, Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol. 2010;5(11):1663-74. doi: 10.2217/fmb.10.125.
44. Iwashkiw JA, Seper A, Weber BS, Scott NE, Vinogradov E, Stratilo C, et al. Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog. 2012;8(6):e1002758. doi: 10.1371/journal.ppat.1002758.
45. Filiatrault MJ, Tombline G, Wagner VE, Van Alst N, Rumbaugh K, Sokol P, et al. Pseudomonas aeruginosa PA1006, which plays a role in molybdenum homeostasis, is required for nitrate utilization, biofilm formation, and virulence. PLoS ONE. 2013;8(2):e55594. doi: 10.1371/journal.pone.0055594.
46. Williams M, Mizrahi V, Kana BD. Molybdenum cofactor: a key component of Mycobacterium tuberculosis pathogenesis? Crit Rev Microbiol. 2013;40:18-29. doi: 10.3109/1040841X.2012.749211.
47. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol. 1999;34(2):257-67. doi: 10.1046/j.1365-2958.1999.01593.x.
48. Holloway BW. Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol. 1955;13(3):572-81.
49. Schweizer HP. Escherichia-Pseudomonas shuttle vector derived from pUC18/19. Gene. 1991;97(03838):109-12.