A putative ABC transporter permease is necessary for resistance to acidified nitrite and EDTA in Pseudomonas aeruginosa under aerobic and anaerobic planktonic and biofilm conditions

Frontiers in Microbiology

Volumn 7, Issue APR, 2016, Pages

  McDaniel, Cameron ^a   Su, Shengchang ^a   Panmanee, Warunya ^a   Lau, Gee W ^b   Browne, Tristan ^a   Cox, Kevin ^a   Paul, Andrew T ^a   Ko, Seung Hyun B ^a   Mortensen, Joel E ^c   Lam, Joseph S ^d   Muruve, Daniel A ^e   Hassett, Daniel J ^a,f  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d UNIVERSITY OF GUELPH   (Canada)

^e UNIVERSITY OF CALGARY   (Canada)

^f Veteran's Hospital Medical Center   (United States)

Author keywords

ABC transporter permease; Acidified nitrite; Biofilms; EDTA; Pseudomonas aeruginosa

Indexed keywords

ABC TRANSPORTER; CHLORAMPHENICOL; COLISTIN; DOXYCYCLINE; EDETIC ACID; PERMEASE; RECOMBINANT DNA; TIGECYCLINE;

ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOFILM; CELL VIABILITY; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE MUTATION; MALE; MINIMUM INHIBITORY CONCENTRATION; MOUSE; MUTAGENESIS; NONHUMAN; PLANKTON; PLASMID; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; SPECTROPHOTOMETRY; TRANSMISSION ELECTRON MICROSCOPY; TRANSPOSON;

EID: 84966440583     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00291     Document Type: Article

References (65)

1. Alakomi, H. L., Paananen, A., Suihko, M. L., Helander, I. M., and Saarela, M. (2006). Weakening effect of cell permeabilizers on gram-negative bacteria causing biodeterioration. Appl. Environ. Microbiol. 72, 4695-4703. doi: 10.1128/AEM.00142-06
2. Al-Hamad, A., Upton, M., and Burnie, J. (2009). Molecular cloning and characterization of SmrA, a novel ABC multidrug efflux pump from Stenotrophomonas maltophilia. J. Antimicrob. Chemother. 64, 731-734. doi: 10.1093/jac/dkp271
3. Alvarez-Ortega, C., and Harwood, C. S. (2007). Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol. Microbiol. 65, 153-165. doi: 10.1111/j.1365-2958.2007.05772.x
4. Arai, H., Igarashi, Y., and Kodama, T. (1995). Expression of the nir and nor genes for denitrification of Pseudomonas aeruginosa requires a novel CRP/FNR-related transcriptional regulator, DNR, in addition to ANR. FEBS Lett. 371, 73-76. doi: 10.1016/0014-5793(95)00885-D
5. Barraud, N., Hassett, D. J., Hwang, S. H., Rice, S. A., Kjelleberg, S., and Webb, J. S. (2006). Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol. 188, 7344-7353. doi: 10.1128/JB.00779-06
6. Boucher, R. C. (2002). An overview of the pathogenesis of cystic fibrosis lung disease. Adv. Drug Deliv. Rev. 54, 1359-1371. doi: 10.1016/S0169-409X(02)00144-8
7. Brown, J., Mellis, C. M., and Wood, R. E. (1985). Edetate sodium aerosol in Pseudomonas lung infection in cystic fibrosis. Am. J. Dis. Child 139, 836-839. doi: 10.1001/archpedi.1985.02140100098043
8. Caetano-Anolles, G. (1993). Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl. 3, 85-94. doi: 10.1101/gr.3.2.85
9. Champlin, F. R., Ellison, M. L., Bullard, J. W., and Conrad, R. S. (2005). Effect of outer membrane permeabilisation on intrinsic resistance to low triclosan levels in Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 26, 159-164. doi: 10.1016/j.ijantimicag.2005.04.020
10. Choi, D. S., Kim, D. K., Choi, S. J., Lee, J., Choi, J. P., Rho, S., et al. (2011). Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa. Proteomics 11, 3424-3429. doi: 10.1002/pmic.201000212
11. Coakley, R. D., Grubb, B. R., Paradiso, A. M., Gatzy, J. T., Johnson, L. G., Kreda, S. M., et al. (2003). Abnormal surface liquid pH regulation by cultured cystic fibrosis bronchial epithelium. Proc. Natl. Acad. Sci. U.S.A. 100, 16083-16088. doi: 10.1073/pnas.2634339100
12. Creuzenet, C., and Lam, J. S. (2001). Topological and functional characterization of WbpM, an inner membrane UDP-GlcNAc C6 dehydratase essential for lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 41, 1295-1310. doi: 10.1046/j.1365-2958.2001.02589.x
13. Dong, C., Major, L. L., Srikannathasan, V., Errey, J. C., Giraud, M. F., Lam, J. S., et al. (2007). RmlC, a C3' and C5' carbohydrate epimerase, appears to operate via an intermediate with an unusual twist boat conformation. J. Mol. Biol. 365, 146-159. doi: 10.1016/j.jmb.2006.09.063
14. Farinha, M. A., and Helinski, A. M. (1990). Construction of broad-host-range plasmid vectors for easy visible selection and analysis of promoters. J. Bacteriol. 172, 3496-3499
15. Govan, J. R. W., and Deretic, V. (1996). Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60, 539-574
16. Hao, Y., Hwang, S., Zhang, S., Kim, E., Akinbi, H. T., Schurr, M. J., et al. (2011). The Pseudomonas aeruginosa flagellum confers resistance to pulmonary surfactant protein-A by impacting the production of exoproteases through quorum-sensing. Mol. Microbiol. 79, 1220-1235. doi: 10.1111/j.1365-2958.2010.07516.x
17. Hassett, D. J. (1996). Anaerobic production of alginate by Pseudomonas aeruginosa: alginate restricts diffusion of oxygen. J. Bacteriol. 178, 7322-7325
18. Hassett, D. J., Borchers, M. T., and Panos, R. J. (2014). Chronic obstructive pulmonary disease (COPD): evaluation from clinical, immunological and bacterial pathogenesis perspectives. J. Microbiol. 52, 211-226. doi: 10.1007/s12275-014-4068-2
19. Hentzer, M., Teitzel, G. M., Balzer, G. J., Heydorn, A., Molin, S., Givskov, M., et al. (2001). Alginate overproduction affects Pseudomonas aeruginosa biofilm structure and function. J. Bacteriol. 183, 5395-5401. doi: 10.1128/JB.183.18.5395-5401.2001
20. Higgins, C. F. (1992). ABC transporters: from microorganisms to man. Ann. Rev. Cell Biol. 8, 67-113. doi: 10.1146/annurev.cb.08.110192.000435
21. Hoang, T. T., Kutchma, A. J., Becher, A., and Schweizer, H. P. (2000). Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43, 59-72. doi: 10.1006/plas.1999.1441
22. Holloway, B. W., Krishnapillai, V., and Morgan, A. F. (1979). Chromosomal genetics of Pseudomonas. Microbiol. Rev. 43, 73-102
23. Kim, Y. M., Farrah, S., and Baney, R. H. (2007). Structure-antimicrobial activity relationship for silanols, a new class of disinfectants, compared with alcohols and phenols. Int. J. Antimicrob. Agents 29, 217-222. doi: 10.1016/j.ijantimicag.2006.08.036
24. Kolpen, M., Kuhl, M., Bjarnsholt, T., Moser, C., Hansen, C. R., Liengaard, L., et al. (2014). Nitrous oxide production in sputum from cystic fibrosis patients with chronic Pseudomonas aeruginosa lung infection. PLoS ONE 9:e84353. doi: 10.1371/journal.pone.0084353
25. Kulasekara, H. D., Ventre, I., Kulasekara, B. R., Lazdunski, A., Filloux, A., and Lory, S. (2005). A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol. Microbiol. 55, 368-380. doi: 10.1111/j.1365-2958.2004.04402.x
26. Lam, J. S., Taylor, V. L., Islam, S. T., Hao, Y., and Kocincova, D. (2011). Genetic and functional diversity of pseudomonas aeruginosa lipopolysaccharide. Front. Microbiol. 2:118. doi: 10.3389/fmicb.2011.00118
27. Lau, G. W., Britigan, B. E., and Hassett, D. J. (2005). Pseudomonas aeruginosa OxyR is required for full virulence in rodent and insect models of infection and for resistance to human neutrophils. Infect. Immun. 73, 2550-2553. doi: 10.1128/IAI.73.4.2550-2553.2005
28. Lenz, A. P., Williamson, K. S., Pitts, B., Stewart, P. S., and Franklin, M. J. (2008). Localized gene expression in Pseudomonas aeruginosa biofilms. Appl. Environ. Microbiol. 74, 4463-4471. doi: 10.1128/AEM.00710-08
29. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
30. Macdonald, I. A., and Kuehn, M. J. (2013). Stress-induced outer membrane vesicle production by Pseudomonas aeruginosa. J. Bacteriol. 195, 2971-2981. doi: 10.1128/JB.02267-12
31. MacKenzie, T., Gifford, A. H., Sabadosa, K. A., Quinton, H. B., Knapp, E. A., Goss, C. H., et al. (2014). Longevity of patients with cystic fibrosis in 2000 to 2010 and beyond: survival analysis of the cystic fibrosis foundation patient registry. Ann. Intern. Med. 161, 233-241. doi: 10.7326/M13-0636
32. Major, T. A., Panmanee, W., Mortensen, J. E., Gray, L. D., Hoglen, N., and Hassett, D. J. (2010). Sodium nitrite-mediated killing of the major cystic fibrosis pathogens Pseudomonas aeruginosa, Staphylococcus aureus, and Burkholderia cepacia under anaerobic planktonic and biofilm conditions. Antimicrob. Agents Chemother. 54, 4671-4677. doi: 10.1128/AAC.00379-10
33. Malinverni, J. C., and Silhavy, T. J. (2009). An ABC transport system that maintains lipid asymmetry in the gram-negative outer membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 8009-8014. doi: 10.1073/pnas.0903229106
34. Maniatis, T., Fritsch, E. F., and Sambrook, J. (1982). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory
35. Martin, D. W., Schurr, M. J., Mudd, M. H., Govan, J. R., Holloway, B. W., and Deretic, V. (1993). Mechanism of conversion to mucoidy in Pseudomonas aeruginosa infecting cystic fibrosis patients. Proc. Natl. Acad. Sci. U.S.A. 90, 8377-8381. doi: 10.1073/pnas.90.18.8377
36. Matsushita, K., Adachi, O., Shinagawa, E., and Ameyama, M. (1978). Isolation and characterization of outer and inner membranes from Pseudomonas aeruginosa and effect of EDTA on the membranes. J. Biochem. 83, 171-181
37. Meshulam, T., Obedeanu, N., Merzbach, D., and Sobel, J. D. (1984). Phagocytosis of mucoid and nonmucoid strains of Pseudomonas aeruginosa. Clin. Immunol. Immunopathol. 32, 151-165. doi: 10.1016/0090-1229(84)90117-X
38. Miller, J. H. (1992). A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Plainview, NY: Cold Spring Harbor Laboratory Press
39. Murphy, K., Park, A. J., Hao, Y., Brewer, D., Lam, J. S., and Khursigara, C. M. (2014). Influence of O polysaccharides on biofilm development and outer membrane vesicle biogenesis in Pseudomonas aeruginosa PAO1. J. Bacteriol. 196, 1306-1317. doi: 10.1128/JB.01463-13
40. Murphy, T. F., Brauer, A. L., Eschberger, K., Lobbins, P., Grove, L., Cai, X., et al. (2008). Pseudomonas aeruginosa in chronic obstructive pulmonary disease. Am. J. Respir. Crit. Care Med. 177, 853-860. doi: 10.1164/rccm.200709-1413OC
41. O'May, C. Y., Sanderson, K., Roddam, L. F., Kirov, S. M., and Reid, D. W. (2009). Iron-binding compounds impair Pseudomonas aeruginosa biofilm formation, especially under anaerobic conditions. J. Med. Microbiol. 58, 765-773. doi: 10.1099/jmm.0.004416-0
42. Pletzer, D., Braun, Y., Dubiley, S., Lafon, C., Kohler, T., Page, M. G., et al. (2015). The Pseudomonas aeruginosa PA14 ABC transporter NppA1A2BCD is required for uptake of peptidyl nucleoside antibiotics. J. Bacteriol. 197, 2217-2228. doi: 10.1128/JB.00234-15
43. Rahim, R., Burrows, L. L., Monteiro, M. A., Perry, M. B., and Lam, J. S. (2000). Involvement of the rml locus in core oligosaccharide and O polysaccharide assembly in Pseudomonas aeruginosa. Microbiology 146 (Pt 11), 2803-2814. doi: 10.1099/00221287-146-11-2803
44. Reilman, E., Mars, R. A., van Dijl, J. M., and Denham, E. L. (2014). The multidrug ABC transporter BmrC/BmrD of Bacillus subtilis is regulated via a ribosome-mediated transcriptional attenuation mechanism. Nucleic Acids Res. 42, 11393-11407. doi: 10.1093/nar/gku832
45. Rocchetta, H. L., Burrows, L. L., Pacan, J. C., and Lam, J. S. (1998a). Three rhamnosyltransferases responsible for assembly of the A-band D-rhamnan polysaccharide in Pseudomonas aeruginosa: a fourth transferase, WbpL, is required for the initiation of both A-band and B-band lipopolysaccharide synthesis. Mol. Microbiol. 28, 1103-1119
46. Rocchetta, H. L., Pacan, J. C., and Lam, J. S. (1998b). Synthesis of the A-band polysaccharide sugar D-rhamnose requires Rmd and WbpW: identification of multiple AlgA homologues, WbpW and ORF488, in Pseudomonas aeruginosa. Mol. Microbiol. 29, 1419-1434
47. Sabra, W., Lunsdorf, H., and Zeng, A. P. (2003). Alterations in the formation of lipopolysaccharide and membrane vesicles on the surface of Pseudomonas aeruginosa PAO1 under oxygen stress conditions. Microbiology 149, 2789-2795. doi: 10.1099/mic.0.26443-0
48. Schweizer, H. P. (1991). Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97, 109-121. doi: 10.1016/0378-1119(91)90016-5
49. Schweizer, H. P. (1992). Allelic exchange in Pseudomonas aeruginosa using novel ColE1-type vectors and a family of cassettes containing a portable oriT and the counter-selectable Bacillus subtilis sacB marker. Mol. Microbiol. 6, 1195-1204. doi: 10.1111/j.1365-2958.1992.tb01558.x
50. Schweizer, H. P. (1993). Small broad-host-range gentamicin resistance gene cassettes for site-specific insertion and deletion mutagenesis. Biotechniques 15, 831-833
51. Schweizer, H. P., and Hoang, T. T. (1995). An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158, 15-22. doi: 10.1016/0378-1119(95)00055-B
52. Sherman, D. J., Okuda, S., Denny, W. A., and Kahne, D. (2013). Validation of inhibitors of an ABC transporter required to transport lipopolysaccharide to the cell surface in Escherichia coli. Bioorg. Med. Chem. 21, 4846-4851. doi: 10.1016/j.bmc.2013.04.020
53. Simon, R., Priefer, U., and Puehler, A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat. Bio Technol. 1, 784-791. doi: 10.1038/nbt1183-784
54. Su, S., Panmanee, W., Wilson, J. J., Mahtani, H. K., Li, Q., Vanderwielen, B. D., et al. (2014). Catalase (KatA) plays a role in protection against anaerobic nitric oxide in Pseudomonas aeruginosa. PLoS ONE 9:e91813. doi: 10.1371/journal.pone.0091813
55. Tunney, M. M., Field, T. R., Moriarty, T. F., Patrick, S., Doering, G., Muhlebach, M. S., et al. (2008). Detection of anaerobic bacteria in high numbers in sputum from patients with cystic fibrosis. Am. J. Respir. Crit. Care Med. 177, 995-1001. doi: 10.1164/rccm.200708-1151OC
56. Valderrey, A. D., Pozuelo, M. J., Jimenez, P. A., Macia, M. D., Oliver, A., and Rotger, R. (2010). Chronic colonization by Pseudomonas aeruginosa of patients with obstructive lung diseases: cystic fibrosis, bronchiectasis, and chronic obstructive pulmonary disease. Diagn. Microbiol. Infect. Dis. 68, 20-27. doi: 10.1016/j.diagmicrobio.2010.04.008
57. Woldringh, C. L., and van Iterson, W. (1972). Effects of treatment with sodium dodecyl sulfate on the ultrastructure of Escherichia coli. J. Bacteriol. 111, 801-813
58. Wood, R. E., Klinger, J. D., Thomassen, M. J., and Cash, H. A. (1980). "The effect of EDTA and antibiotics on Pseudomonas aeruginosa isolated from cystic fibrosis patients: a new chemotherapeutic approach, " in Perspectives in Cystic Fibrosis, ed J. M. Sturgess (Toronto, ON: Canadian Cystic Fibrosis Foundation), 365-369
59. Worlitzsch, D., Tarran, R., Ulrich, M., Schwab, U., Cekici, A., Meyer, K. C., et al. (2002). Reduced oxygen concentrations in airway mucus contribute to the early and late pathogenesis of Pseudomonas aeruginosa cystic fibrosis airway infection. J. Clin. Invest. 109, 317-325. doi: 10.1172/JCI0213870
60. Yoon, S. S., Coakley, R., Lau, G. W., Lymar, S. V., Gaston, B., Karabulut, A. C., et al. (2006). Anaerobic killing of mucoid Pseudomonas aeruginosa by acidified nitrite derivatives under cystic fibrosis airway conditions. J. Clin. Invest. 116, 436-446. doi: 10.1172/JCI24684
61. Yoon, S. S., Hennigan, R. F., Hilliard, G. M., Ochsner, U. A., Parvatiyar, K., Kamani, M. C., et al. (2002). Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3, 593-603. doi: 10.1016/S1534-5807(02)00295-2
62. Yoon, S. S., Karabulut, A. C., Lipscomb, J. D., Hennigan, R. F., Lymar, S. V., Groce, S. L., et al. (2007). Two-pronged survival strategy for the major cystic fibrosis pathogen, Pseudomonas aeruginosa, lacking the capacity to degrade nitric oxide during anaerobic respiration. EMBO J. 26, 3662-3672. doi: 10.1038/sj.emboj.7601787
63. Zemke, A. C., Gladwin, M. T., and Bomberger, J. M. (2015). Sodium nitrite blocks the activity of aminoglycosides against Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother. 59, 3329-3334. doi: 10.1128/AAC.00546-15
64. Zemke, A. C., Shiva, S., Burns, J. L., Moskowitz, S. M., Pilewski, J. M., Gladwin, M. T., et al. (2014). Nitrite modulates bacterial antibiotic susceptibility and biofilm formation in association with airway epithelial cells. Free Radic. Biol. Med. 77, 307-316. doi: 10.1016/j.freeradbiomed.2014.08.011
65. Zhang, S., Chen, Y., Potvin, E., Sanschagrin, F., Levesque, R. C., McCormack, F. X., et al. (2005). Comparative signature-tagged mutagenesis identifies pseudomonas factors conferring resistance to the pulmonary collectin SP-A. PLoS Pathog. 1:e31. doi: 10.1371/journal.ppat.0010031