Proteome Profiles of Outer Membrane Vesicles and Extracellular Matrix of Pseudomonas aeruginosa Biofilms

Journal of Proteome Research

Volumn 14, Issue 10, 2015, Pages 4207-4222

  Couto, Narciso ^a   Schooling, Sarah R ^b   Dutcher, John R ^b   Barber, Jill ^a,c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF GUELPH   (Canada)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

biofilms; matrix; outer membrane vesicles; proteome; Pseudomonas aeruginosa

Indexed keywords

PROTEOME; BACTERIAL PROTEIN; GEL; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BIOFILM; CYSTIC FIBROSIS; EXTRACELLULAR MATRIX; LIFESTYLE; MEMBRANE VESICLE; NONHUMAN; OUTER MEMBRANE; OUTER MEMBRANE VESICLE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEOMICS; PSEUDOMONAS AERUGINOSA; CELL MEMBRANE; CHEMISTRY; EXOSOME; GEL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR GENETICS; PROCEDURES; TANDEM MASS SPECTROMETRY;

BACTERIAL PROTEINS; BIOFILMS; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; EXTRACELLULAR MATRIX; EXTRACELLULAR VESICLES; GELS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE ANNOTATION; PROTEOME; PROTEOMICS; PSEUDOMONAS AERUGINOSA; TANDEM MASS SPECTROMETRY; VIRULENCE FACTORS;

EID: 84942937038     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00312     Document Type: Article

References (98)

1. Romeo, A.; Sonnleitner, E.; Sorger-Domenigg, T.; Nakano, M.; Eisenhaber, B.; Bläsi, U. Transcriptional regulation of nitrate assimilation in Pseudomonas aeruginosa occurs via transcriptional antitermination within the nirBD-PA1779-cobA operon Microbiology 2012, 158, 1543-1552 10.1099/mic.0.053850-0
2. Schreiber, K.; Krieger, R.; Benkert, B.; Eschbach, M.; Arai, H.; Schobert, M.; Jahn, D. The anaerobic regulatory network required for Pseudomonas aeruginosa nitrate respiration J. Bacteriol. 2007, 189, 4310-4314 10.1128/JB.00240-07
3. Kerr, K. G.; Snelling, A. M. Pseudomonas aeruginosa: a formidable and ever-present adversary J. Hosp. Infect. 2009, 73, 338-344 10.1016/j.jhin.2009.04.020
4. Ciofu, O.; Tolker-Nielsen, T.; Jensen, P. Ø.; Wang, H.; Høiby, N. Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients Adv. Drug Delivery Rev. 2015, 85, 7-23 10.1016/j.addr.2014.11.017
5. López-Causapé, C.; Rojo-Molinero, E.; Macià, M. D.; Oliver, A. The problems of antibiotic resistance in cystic fibrosis and solutions Expert Rev. Respir. Med. 2015, 9, 73-88 10.1586/17476348.2015.995640
6. Ciofu, O.; Hansen, C. R.; Høiby, N. Respiratory bacterial infections in cystic fibrosis Curr. Opin. Pulm. Med. 2013, 19, 251-258 10.1097/MCP.0b013e32835f1afc
7. Schooling, S. R.; Hubley, A.; Beveridge, T. J. Interactions of DNA with biofilm-derived membrane vesicles J. Bacteriol. 2009, 191, 4097-4102 10.1128/JB.00717-08
8. Schooling, S. R.; Beveridge, T. J. Membrane vesicles: an overlooked component of the matrices of biofilms J. Bacteriol. 2006, 188, 5945-5957 10.1128/JB.00257-06
9. Flemming, H.-C.; Wingender, J. The biofilm matrix Nat. Rev. Microbiol. 2010, 8, 623-633 10.1038/nrmicro2415
10. Gellatly, S. L.; Hancock, R. E. Pseudomonas aeruginosa: new insights into pathogenesis and host defenses Pathog. Dis. 2013, 67, 159-173 10.1111/2049-632X.12033
11. Rumbaugh, K. P.; Armstrong, A. The Role of Quorum Sensing in Biofilm Development. In Antibiofilm Agents; Springer: New York, 2014; pp 97-113.
12. Winson, M. K.; Camara, M.; Latifi, A.; Foglino, M.; Chhabra, S. R.; Daykin, M.; Bally, M.; Chapon, V.; Salmond, G.; Bycroft, B. W. Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U. S. A. 1995, 92, 9427-9431 10.1073/pnas.92.20.9427
13. Bonnington, K.; Kuehn, M. Protein selection and export via outer membrane vesicles Biochim. Biophys. Acta, Mol. Cell Res. 2014, 1843, 1612-1619 10.1016/j.bbamcr.2013.12.011
14. Li, Z.; Clarke, A. J.; Beveridge, T. J. Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria J. Bacteriol. 1998, 180, 5478-5483
15. Oglesby, A. G.; Farrow, J. M.; Lee, J.-H.; Tomaras, A. P.; Greenberg, E.; Pesci, E. C.; Vasil, M. L. The Influence of Iron on Pseudomonas aeruginosa Physiology J. Biol. Chem. 2008, 283, 15558-15567 10.1074/jbc.M707840200
16. Bullen, J.; Ward, C.; Wallis, S. Virulence and the role of iron in Pseudomonas aeruginosa infection Infect. Immun. 1974, 10, 443-450
17. Wiens, J. R.; Vasil, A. I.; Schurr, M. J.; Vasil, M. L. Iron-regulated expression of alginate production, mucoid phenotype, and biofilm formation by Pseudomonas aeruginosa mBio 2014, 5, e01010-13 10.1128/mBio.01010-13
18. Mislin, G. L.; Schalk, I. J. Siderophore-dependent iron uptake systems as gates for antibiotic Trojan horse strategies against Pseudomonas aeruginosa Metallomics 2014, 6, 408-420 10.1039/c3mt00359k
19. Bergeron, R. J., Jr Siderophore conjugate immunogenic compositions and vaccines. Google Patents, 2014.
20. de Carvalho, C. C.; Fernandes, P. Siderophores as "Trojan Horses": tackling multidrug resistance? Front. Microbiol. 2014, 5, 10.3389/fmicb.2014.00290
21. Bjune, G.; Hoiby, E.; Gronnesby, J.; Arnesen, O.; Fredriksen, J. H.; Lindbak, A.; Nokleby, H.; Rosenqvist, E.; Solberg, L.; Closs, O. Effect of outer membrane vesicle vaccine against group B meningococcal disease in Norway Lancet 1991, 338, 1093-1096 10.1016/0140-6736(91)91961-S
22. Holst, J.; Martin, D.; Arnold, R.; Huergo, C. C.; Oster, P.; O'Hallahan, J.; Rosenqvist, E. Properties and clinical performance of vaccines containing outer membrane vesicles from Neisseria meningitidis Vaccine 2009, 27, B3-B12 10.1016/j.vaccine.2009.04.071
23. Stover, C. K.; Pham, X. Q.; Erwin, A. L.; Mizoguchi, S. D.; Warrener, P.; Hickey, M. J.; Brinkman, F. S. L.; Hufnagle, W. O.; Kowalik, D. J.; Lagrou, M.; Garber, R. L.; Goltry, L.; Tolentino, E.; Westbrock-Wadman, S.; Yuan, Y.; Brody, L. L.; Coulter, S. N.; Folger, K. R.; Kas, A.; Larbig, K.; Lim, R.; Smith, K.; Spencer, D.; Wong, G. K. S.; Wu, Z.; Paulsen, I. T.; Reizer, J.; Saier, M. H.; Hancock, R. E. W.; Lory, S.; Olson, M. V. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen Nature 2000, 406, 959-964 10.1038/35023079
24. Choi, D. S.; Kim, D. K.; Choi, S. J.; Lee, J.; Choi, J. P.; Rho, S.; Park, S. H.; Kim, Y. K.; Hwang, D.; Gho, Y. S. Proteomic analysis of outer membrane vesicles derived from Pseudomonas aeruginosa Proteomics 2011, 11, 3424-3429 10.1002/pmic.201000212
25. Maredia, R.; Devineni, N.; Lentz, P.; Dallo, S. F.; Yu, J.; Guentzel, N.; Chambers, J.; Arulanandam, B.; Haskins, W. E.; Weitao, T. Vesiculation from Pseudomonas aeruginosa under SOS Sci. World J. 2012, 2012, 1 10.1100/2012/402919
26. Ouidir, T.; Jarnier, F.; Cosette, P.; Jouenne, T.; Hardouin, J. Extracellular Ser/Thr/Tyr phosphorylated proteins of Pseudomonas aeruginosa PA14 strain Proteomics 2014, 14, 2017-2030 10.1002/pmic.201400190
27. Toyofuku, M.; Roschitzki, B.; Riedel, K.; Eberl, L. Identification of proteins associated with the Pseudomonas aeruginosa biofilm extracellular matrix J. Proteome Res. 2012, 11, 4906-4915 10.1021/pr300395j
28. Bauman, S. J.; Kuehn, M. J. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response Microbes Infect. 2006, 8, 2400-2408 10.1016/j.micinf.2006.05.001
29. Hanna, S. L.; Sherman, N. E.; Kinter, M. T.; Goldberg, J. B. Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry Microbiology 2000, 146, 2495-2508 10.1099/00221287-146-10-2495
30. Molloy, M. P.; Gillings, M.; Willcox, M. D.; Walsh, B. J.; Wales, N. S. Complementing genomics with proteomics: the membrane subproteome of Pseudomonas aeruginosa PAO1 Electrophoresis 2000, 21, 3797-3809 10.1002/1522-2683(200011)21:17<3797::AID-ELPS3797>3.0.CO;2-P
31. Couto, N.; Barber, J.; Gaskell, S. J. Matrix-assisted laser desorption/ionisation mass spectrometric response factors of peptides generated using different proteolytic enzymes J. Mass Spectrom. 2011, 46, 1233-1240 10.1002/jms.2009
32. Couto, N.; Malys, N.; Gaskell, S. J.; Barber, J. Partition and turnover of glutathione reductase from Saccharomyces cerevisiae: a proteomic approach J. Proteome Res. 2013, 12, 2885-2894 10.1021/pr4001948
33. Ishihama, Y.; Oda, Y.; Tabata, T.; Sato, T.; Nagasu, T.; Rappsilber, J.; Mann, M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein Mol. Cell. Proteomics 2005, 4, 1265-1272 10.1074/mcp.M500061-MCP200
34. Kyte, J.; Doolittle, R. F. A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 1982, 157, 105-132 10.1016/0022-2836(82)90515-0
35. Jiang, X.-S.; Zhou, H.; Zhang, L.; Sheng, Q.-H.; Li, S.-J.; Li, L.; Hao, P.; Li, Y.-X.; Xia, Q.-C.; Wu, J.-R. A high-throughput approach for subcellular proteome identification of rat liver proteins using subcellular fractionation coupled with two-dimensional liquid chromatography tandem mass spectrometry and bioinformatic analysis Mol. Cell. Proteomics 2004, 3, 441-455 10.1074/mcp.M300117-MCP200
36. Santoni, V.; Molloy, M.; Rabilloud, T. Membrane proteins and proteomics: un amour impossible? Electrophoresis 2000, 21, 1054-1070 10.1002/(SICI)1522-2683(20000401)21:6<1054::AID-ELPS1054>3.3.CO;2-#
37. Ernst, R. K.; Adams, K. N.; Moskowitz, S. M.; Kraig, G. M.; Kawasaki, K.; Stead, C. M.; Trent, M. S.; Miller, S. I. The Pseudomonas aeruginosa lipid A deacylase: selection for expression and loss within the cystic fibrosis airway J. Bacteriol. 2006, 188, 191-201 10.1128/JB.188.1.191-201.2006
38. Rutten, L.; Geurtsen, J.; Lambert, W.; Smolenaers, J. J.; Bonvin, A. M.; de Haan, A.; van der Ley, P.; Egmond, M. R.; Gros, P.; Tommassen, J. Crystal structure and catalytic mechanism of the LPS 3-O-deacylase PagL from Pseudomonas aeruginosa Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 7071-7076 10.1073/pnas.0509392103
39. Geurtsen, J.; Steeghs, L.; ten Hove, J.; van der Ley, P.; Tommassen, J. Dissemination of lipid A deacylases (PagL) among Gram-negative bacteria identification of active-site histidine and serine residues J. Biol. Chem. 2005, 280, 8248-8259 10.1074/jbc.M414235200
40. Wilhelm, S.; Gdynia, A.; Tielen, P.; Rosenau, F.; Jaeger, K.-E. The autotransporter esterase EstA of Pseudomonas aeruginosa is required for rhamnolipid production, cell motility, and biofilm formation J. Bacteriol. 2007, 189, 6695-6703 10.1128/JB.00023-07
41. van den Berg, B. Crystal structure of a full-length autotransporter J. Mol. Biol. 2010, 396, 627-633 10.1016/j.jmb.2009.12.061
42. Hancock, R.; Siehnel, R.; Martin, N. Outer membrane proteins of Pseudomonas Mol. Microbiol. 1990, 4, 1069-1075 10.1111/j.1365-2958.1990.tb00680.x
43. Siryaporn, A.; Kuchma, S. L.; O'Toole, G. A.; Gitai, Z. Surface attachment induces Pseudomonas aeruginosa virulence Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 16860-16865 10.1073/pnas.1415712111
44. Georgiadou, M.; Pelicic, V.; Barocchi, M.; Telford, J. Type IV Pili: Functions and Biogenesis. Bacterial Pili: Structure, Synthesis and Role in Disease; CAB International: Oxfordshire, U.K., 2014; pp 71-84.
45. Taguchi, F.; Ichinose, Y. Role of type IV pili in virulence of Pseudomonas syringae pv. tabaci 6605: correlation of motility, multidrug resistance, and HR-inducing activity on a nonhost plant Mol. Plant-Microbe Interact. 2011, 24, 1001-1011 10.1094/MPMI-02-11-0026
46. Punsalang, A. P.; Sawyer, W. D. Role of pili in the virulence of Neisseria gonorrhoeae Infect. Immun. 1973, 8, 255-263
47. O'Toole, G. A.; Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development Mol. Microbiol. 1998, 30, 295-304 10.1046/j.1365-2958.1998.01062.x
48. Cornelis, P.; Matthijs, S.; Van Oeffelen, L. Iron uptake regulation in Pseudomonas aeruginosa BioMetals 2009, 22, 15-22 10.1007/s10534-008-9193-0
49. Cornelis, P.; Dingemans, J. Pseudomonas aeruginosa adapts its iron uptake strategies in function of the type of infections Front. Cell. Infect. Microbiol. 2013, 3, 1-7 10.3389/fcimb.2013.00075
50. Nguyen, A. T.; O'Neill, M. J.; Watts, A. M.; Robson, C. L.; Lamont, I. L.; Wilks, A.; Oglesby-Sherrouse, A. G. Adaptation of iron homeostasis pathways by a Pseudomonas aeruginosa pyoverdine mutant in the cystic fibrosis lung J. Bacteriol. 2014, 196, 2265-2276 10.1128/JB.01491-14
51. Hannauer, M.; Barda, Y.; Mislin, G. L.; Shanzer, A.; Schalk, I. J. The ferrichrome uptake pathway in Pseudomonas aeruginosa involves an iron release mechanism with acylation of the siderophore and recycling of the modified desferrichrome J. Bacteriol. 2010, 192, 1212-1220 10.1128/JB.01539-09
52. Poole, K.; Young, L.; Neshat, S. Enterobactin-mediated iron transport in Pseudomonas aeruginosa J. Bacteriol. 1990, 172, 6991-6996
53. Llamas, M. A.; Sparrius, M.; Kloet, R.; Jiménez, C. R.; Vandenbroucke-Grauls, C.; Bitter, W. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa J. Bacteriol. 2006, 188, 1882-1891 10.1128/JB.188.5.1882-1891.2006
54. Braun, V.; Killmann, H. Bacterial solutions to the iron-supply problem Trends Biochem. Sci. 1999, 24, 104-109 10.1016/S0968-0004(99)01359-6
55. Marshall, B.; Stintzi, A.; Gilmour, C.; Meyer, J.-M.; Poole, K. Citrate-mediated iron uptake in Pseudomonas aeruginosa: involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter Microbiology 2009, 155, 305-315 10.1099/mic.0.023531-0
56. Andrews, S. C. Iron storage in bacteria Adv. Microb. Physiol. 1998, 40, 281-351 10.1016/S0065-2911(08)60134-4
57. Ebrahimi, K. H.; Bill, E.; Hagedoorn, P.-L.; Hagen, W. R. The catalytic center of ferritin regulates iron storage via Fe (II)-Fe (III) displacement Nat. Chem. Biol. 2012, 8, 941-948 10.1038/nchembio.1071
58. Smith, J. L. The physiological role of ferritin-like compounds in bacteria Crit. Rev. Microbiol. 2004, 30, 173-185 10.1080/10408410490435151
59. Pelzer, A.; Polen, T.; Funken, H.; Rosenau, F.; Wilhelm, S.; Bott, M.; Jaeger, K. E. Subtilase SprP exerts pleiotropic effects in Pseudomonas aeruginosa MicrobiologyOpen 2014, 3, 89-103 10.1002/mbo3.150
60. Luckett, J. C.; Darch, O.; Watters, C.; AbuOun, M.; Wright, V.; Paredes-Osses, E.; Ward, J.; Goto, H.; Heeb, S.; Pommier, S. A novel virulence strategy for Pseudomonas aeruginosa mediated by an autotransporter with arginine-specific aminopeptidase activity PLoS Pathog. 2012, 8, e1002854 10.1371/journal.ppat.1002854
61. Kessler, E.; Safrin, M.; Gustin, J. K.; Ohman, D. E. Elastase and the LasA protease of Pseudomonas aeruginosa are secreted with their propeptides J. Biol. Chem. 1998, 273, 30225-30231 10.1074/jbc.273.46.30225
62. Gonzales, T.; Robert-Baudouy, J. Bacterial aminopeptidases: properties and functions FEMS Microbiol. Rev. 1996, 18, 319-344 10.1111/j.1574-6976.1996.tb00247.x
63. Yalak, G.; Vogel, V. Extracellular phosphorylation and phosphorylated proteins: not just curiosities but physiologically important Sci. Signaling 2012, 5, re7-re7 10.1126/scisignal.2003273
64. Callewaert, L.; Van Herreweghe, J. M.; Vanderkelen, L.; Leysen, S.; Voet, A.; Michiels, C. W. Guards of the great wall: bacterial lysozyme inhibitors Trends Microbiol. 2012, 20, 501-510 10.1016/j.tim.2012.06.005
65. Akama, H.; Kanemaki, M.; Yoshimura, M.; Tsukihara, T.; Kashiwagi, T.; Yoneyama, H.; Narita, S.-i.; Nakagawa, A.; Nakae, T. Crystal Structure of the Drug Discharge Outer Membrane Protein, OprM, of Pseudomonas aeruginosa J. Biol. Chem. 2004, 279, 52816-52819 10.1074/jbc.C400445200
66. Masuda, N.; Sakagawa, E.; Ohya, S. Outer membrane proteins responsible for multiple drug resistance in Pseudomonas aeruginosa Antimicrob. Agents Chemother. 1995, 39, 645-649 10.1128/AAC.39.3.645
67. Nordmann, P.; Ronco, E.; Naas, T.; Duport, C.; Michel-Briand, Y.; Labia, R. Characterization of a novel extended-spectrum beta-lactamase from Pseudomonas aeruginosa Antimicrob. Agents Chemother. 1993, 37, 962-969 10.1128/AAC.37.5.962
68. Sahl, H.-G. Gene-encoded antibiotics made in bacteria Antimicrob. Pept. 1994, 186, 27 10.1002/9780470514658.ch3
69. Pommier, S.; Gavioli, M.; Cascales, E.; Lloubès, R. Tol-dependent macromolecule import through the Escherichia coli cell envelope requires the presence of an exposed TolA binding motif J. Bacteriol. 2005, 187, 7526-7534 10.1128/JB.187.21.7526-7534.2005
70. Bender, R. A. Regulation of the histidine utilization (hut) system in bacteria Microbiol. Mol. Biol. Rev. 2012, 76, 565-584 10.1128/MMBR.00014-12
71. Tielen, P.; Rosenau, F.; Wilhelm, S.; Jaeger, K.-E.; Flemming, H.-C.; Wingender, J. Extracellular enzymes affect biofilm formation of mucoid Pseudomonas aeruginosa Microbiology 2010, 156, 2239-2252 10.1099/mic.0.037036-0
72. Lee, A. I.; Delgado, A.; Gunsalus, R. P. Signal-Dependent Phosphorylation of the Membrane-Bound NarX Two-Component Sensor-Transmitter Protein of Escherichia coli: Nitrate Elicits a Superior Anion Ligand Response Compared to Nitrite J. Bacteriol. 1999, 181, 5309-5316
73. Henderson, B.; Martin, A. Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease Infect. Immun. 2011, 79, 3476-3491 10.1128/IAI.00179-11
74. Al-Majdoub, Z. M.; Carroll, K. M.; Gaskell, S. J.; Barber, J. Quantification of the proteins of the bacterial ribosome using QconCAT technology J. Proteome Res. 2014, 13, 1211-1222 10.1021/pr400667h
75. Jennings, M. P.; Beacham, I. R. Analysis of the Escherichia coli gene encoding L-asparaginase II, ansB, and its regulation by cyclic AMP receptor and FNR proteins J. Bacteriol. 1990, 172, 1491-1498
76. Jennings, M. P.; Scott, S. P.; Beacham, I. R. Regulation of the ansB gene of Salmonella enterica Mol. Microbiol. 1993, 9, 165-172 10.1111/j.1365-2958.1993.tb01678.x
77. George, D. T.; Mathesius, U.; Behm, C. A.; Verma, N. K. The Periplasmic Enzyme, AnsB, of Shigella flexneri Modulates Bacterial Adherence to Host Epithelial Cells PLoS One 2014, 9, e94954 10.1371/journal.pone.0094954
78. Lindsey, T. L.; Hagins, J. M.; Sokol, P. A.; Silo-Suh, L. A. Virulence determinants from a cystic fibrosis isolate of Pseudomonas aeruginosa include isocitrate lyase Microbiology 2008, 154, 1616-1627 10.1099/mic.0.2007/014506-0
79. Zimmermann, A.; Reimmann, C.; Galimand, M.; Haas, D. Anaerobic growth and cyanide synthesis of Pseudomonas aeruginosa depend on anr, a regulatory gene homologous with fnr of Escherichia coli Mol. Microbiol. 1991, 5, 1483-1490 10.1111/j.1365-2958.1991.tb00794.x
80. Arai, H. Regulation and function of versatile aerobic and anaerobic respiratory metabolism in Pseudomonas aeruginosa. Front. Microbiol. 2011, 2, 10.3389/fmicb.2011.00103
81. Kuroki, M.; Igarashi, Y.; Ishii, M.; Arai, H. Fine-tuned regulation of the dissimilatory nitrite reductase gene by oxygen and nitric oxide in Pseudomonas aeruginosa Environ. Microbiol. Rep. 2014, 6, 792-801 10.1111/1758-2229.12212
82. Gerlach, D.; Reichardt, W.; Vettermann, S. Extracellular superoxide dismutase from Streptococcus pyogenes type 12 strain is manganese-dependent FEMS Microbiol. Lett. 1998, 160, 217-224 10.1111/j.1574-6968.1998.tb12914.x
83. Pezzoni, M.; Pizarro, R. A.; Costa, C. S. Protective role of extracellular catalase (KatA) against UV radiation in Pseudomonas aeruginosa biofilms J. Photochem. Photobiol., B 2014, 131, 53-64 10.1016/j.jphotobiol.2014.01.005
84. Oliveira, P.; Martins, N. M.; Santos, M.; Couto, N. A.; Wright, P. C.; Tamagnini, P. The Anabaena sp. PCC 7120 Exoproteome: Taking a Peek outside the Box Life 2015, 5, 130-163 10.3390/life5010130
85. Rompf, A.; Hungerer, C.; Hoffmann, T.; Lindenmeyer, M.; Römling, U.; Groß, U.; Doss, M. O.; Arai, H.; Igarashi, Y.; Jahn, D. Regulation of Pseudomonas aeruginosa hemF and hemN by the dual action of the redox response regulators Anr and Dnr Mol. Microbiol. 1998, 29, 985-997 10.1046/j.1365-2958.1998.00980.x
86. Cartron, M. L.; Maddocks, S.; Gillingham, P.; Craven, C. J.; Andrews, S. C. Feo-transport of ferrous iron into bacteria BioMetals 2006, 19, 143-157 10.1007/s10534-006-0003-2
87. Matsubara, T.; Frunzke, K.; Zumft, W. Modulation by copper of the products of nitrite respiration in Pseudomonas perfectomarinus J. Bacteriol. 1982, 149, 816-823
88. Pederick, V. G.; Eijkelkamp, B. A.; Ween, M. P.; Begg, S. L.; Paton, J. C.; McDevitt, C. A. Acquisition and Role of Molybdate in Pseudomonas aeruginosa Appl. Environ. Microbiol. 2014, 80, 6843-6852 10.1128/AEM.02465-14
89. Absalon, C.; Ymele-Leki, P.; Watnick, P. I. The bacterial biofilm matrix as a platform for protein delivery mBio 2012, 3, e00127-12 10.1128/mBio.00127-12
90. Kay, E.; Humair, B.; Dénervaud, V.; Riedel, K.; Spahr, S.; Eberl, L.; Valverde, C.; Haas, D. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa J. Bacteriol. 2006, 188, 6026-6033 10.1128/JB.00409-06
91. Folders, J.; Algra, J.; Roelofs, M. S.; van Loon, L. C.; Tommassen, J.; Bitter, W. Characterization of Pseudomonas aeruginosa Chitinase, a gradually secreted protein J. Bacteriol. 2001, 183, 7044-7052 10.1128/JB.183.24.7044-7052.2001
92. Yu, H.; He, X.; Xie, W.; Xiong, J.; Sheng, H.; Guo, S.; Huang, C.; Zhang, D.; Zhang, K. Elastase LasB of Pseudomonas aeruginosa promotes biofilm formation partly through rhamnolipid-mediated regulation Can. J. Microbiol. 2014, 60, 227-235 10.1139/cjm-2013-0667
93. Vinayak, M.; Pathak, C. Queuosine modification of tRNA: its divergent role in cellular machinery Biosci. Rep. 2010, 30, 135-148 10.1042/BSR20090057
94. Iyer, L. M.; Zhang, D.; Rogozin, I. B.; Aravind, L. Evolution of the deaminase fold and multiple origins of eukaryotic editing and mutagenic nucleic acid deaminases from bacterial toxin systems Nucleic Acids Res. 2011, 39, 9473-9497 10.1093/nar/gkr691
95. Robert-Genthon, M.; Casabona, M. G.; Neves, D.; Couté, Y.; Cicéron, F.; Elsen, S.; Dessen, A.; Attrée, I. Unique features of a Pseudomonas aeruginosa α2-macroglobulin homolog mBio 2013, 4, e00309-13 10.1128/mBio.00309-13
96. Borth, W. Alpha 2-macroglobulin, a multifunctional binding protein with targeting characteristics FASEB J. 1992, 6, 3345-3353
97. Sampedro, I.; Parales, R. E.; Krell, T.; Hill, J. E. Pseudomonas chemotaxis FEMS Microbiol. Rev. 2015, 39, 17-46 10.1111/1574-6976.12081
98. Bordoli, M. R.; Yum, J.; Breitkopf, S. B.; Thon, J. N.; Italiano, J. E.; Xiao, J.; Worby, C.; Wong, S.-K.; Lin, G.; Edenius, M. A secreted tyrosine kinase acts in the extracellular environment Cell 2014, 158, 1033-1044 10.1016/j.cell.2014.06.048