Characterization of a novel two-partner secretion system implicated in the virulence of Pseudomonas aeruginosa

Microbiology (United Kingdom)

Volumn 160, Issue PART 9, 2014, Pages 1940-1952

  Faure, Laura M ^a   Garvis, Steve ^a   de Bentzmann, Sophie ^a   Bigot, Sarah ^a  

^a CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; MUTANT PROTEIN; PDTA EXOPROTEIN; PDTB EXOPROTEIN; PHOSPHATE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL SECRETION SYSTEM; BACTERIAL TRANSLOCATION; BACTERIAL VIRULENCE; CAENORHABDITIS ELEGANS; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; TWO PARTNER SECRETION SYSTEM; WILD TYPE; ANIMAL; DISEASE MODEL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PSEUDOMONAS INFECTION; VIRULENCE;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL SECRETION SYSTEMS; CAENORHABDITIS ELEGANS; DISEASE MODELS, ANIMAL; PHOSPHATES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; VIRULENCE; VIRULENCE FACTORS;

EID: 84906861170     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.079616-0     Document Type: Article

References (53)

1. Aoki, S. K., Pamma, R., Hernday, A. D., Bickham, J. E., Braaten, B. A. & Low, D. A. (2005). Contact-dependent inhibition of growth in Escherichia coli. Science 309, 1245-1248.
2. Bleves, S., Viarre, V., Salacha, R., Michel, G. P., Filloux, A. & Voulhoux, R. (2010). Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. Int J Med Microbiol 300, 534-543.
3. Borlee, B. R., Goldman, A. D., Murakami, K., Samudrala, R., Wozniak, D. J. & Parsek, M. R. (2010). Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75, 827-842.
4. Braun, V., Hobbie, S. & Ondraczek, R. (1992). Serratia marcescens forms a new type of cytolysin. FEMS Microbiol Lett 100, 299-305.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Buscher, A. Z., Grass, S., Heuser, J., Roth, R. & St Geme, J. W., III (2006). Surface anchoring of a bacterial adhesin secreted by the twopartner secretion pathway. Mol Microbiol 61, 470-483.
7. Choi, K. H. & Schweizer, H. P. (2006). mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc 1, 153-161.
8. Clantin, B., Delattre, A. S., Rucktooa, P., Saint, N., Méli, A. C., Locht, C., Jacob-Dubuisson, F. & Villeret, V. (2007). Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317, 957-961.
9. Coutte, L., Antoine, R., Drobecq, H., Locht, C. & Jacob-Dubuisson, F. (2001). Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J 20, 5040-5048.
10. Delattre, A. S., Saint, N., Clantin, B., Willery, E., Lippens, G., Locht, C., Villeret, V. & Jacob-Dubuisson, F. (2011). Substrate recognition by the POTRA domains of TpsB transporter FhaC. Mol Microbiol 81, 99-112.
11. vreI ECF factor and its target genes. Microbiology 159, 1315-1327.
12. Figurski, D. H. & Helinski, D. R. (1979). Replication of an origincontaining derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648-1652.
13. Flemming, H. C. & Wingender, J. (2010). The biofilm matrix. Nat Rev Microbiol 8, 623-633.
14. Garvis, S., Munder, A., Ball, G., de Bentzmann, S., Wiehlmann, L., Ewbank, J. J., Tümmler, B. & Filloux, A. (2009). Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. Plos Pathog 5, e1000540.
15. Grass, S. & St Geme, J. W., III (2000). Maturation and secretion of the non-typable Haemophilus influenzae HMW1 adhesin: roles of the N-terminal and C-terminal domains. Mol Microbiol 36, 55-67.
16. Guédin, S., Willery, E., Locht, C. & Jacob-Dubuisson, F. (1998). Evidence that a globular conformation is not compatible with FhaCmediated secretion of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 29, 763-774.
17. Herrero, M., de Lorenzo, V. & Timmis, K. N. (1990). Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gramnegative bacteria. J Bacteriol 172, 6557-6567.
18. Hertle, R. (2005). The family of Serratia type pore forming toxins. Curr Protein Pept Sci 6, 313-325.
19. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J. & Schweizer, H. P. (1998). A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212, 77-86.
20. Hoang, T. T., Kutchma, A. J., Becher, A. & 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.
21. Ize, B., Viarre, V. & Voulhoux, R. (2014). Cell fractionation. Methods Mol Biol 1149, 185-191.
22. Jacob-Dubuisson, F., Buisine, C., Willery, E., Renauld-Mongénie, G. & Locht, C. (1997). Lack of functional complementation between Bordetella pertussis filamentous hemagglutinin and Proteus mirabilis HpmA hemolysin secretion machineries. J Bacteriol 179, 775-783.
23. Jacob-Dubuisson, F., El-Hamel, C., Saint, N., Guédin, S., Willery, E., Molle, G. & Locht, C. (1999). Channel formation by FhaC, the outer membrane protein involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J Biol Chem 274, 37731-37735.
24. Jacob-Dubuisson, F., Locht, C. & Antoine, R. (2001). Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol 40, 306-313.
25. Kajava, A. V., Cheng, N., Cleaver, R., Kessel, M., Simon, M. N., Willery, E., Jacob-Dubuisson, F., Locht, C. & Steven, A. C. (2001). Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42, 279-292.
26. Kaniga, K., Delor, I. & Cornelis, G. R. (1991). A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109, 137-141.
27. Kida, Y., Higashimoto, Y., Inoue, H., Shimizu, T. & Kuwano, K. (2008). A novel secreted protease from Pseudomonas aeruginosa activates NF-κB through protease-activated receptors. Cell Microbiol 10, 1491-1504.
28. Kida, Y., Shimizu, T. & Kuwano, K. (2011). Cooperation between LepA and PlcH contributes to the in vivo virulence and growth of Pseudomonas aeruginosa in mice. Infect Immun 79, 211-219.
29. Llamas, M. A., van der Sar, A., Chu, B. C., Sparrius, M., Vogel, H. J. & Bitter, W. (2009). A novel extracytoplasmic function (ECF) sigma factor regulates virulence in Pseudomonas aeruginosa. PLoS Pathog 5, e1000572.
30. Makhov, A. M., Hannah, J. H., Brennan, M. J., Trus, B. L., Kocsis, E., Conway, J. F., Wingfield, P. T., Simon, M. N. & Steven, A. C. (1994). Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in beta strands and turns. J Mol Biol 241, 110-124.
31. Mazar, J. & Cotter, P. A. (2006). Topology and maturation of filamentous haemagglutinin suggest a new model for two-partner secretion. Mol Microbiol 62, 641-654.
32. Mazar, J. & Cotter, P. A. (2007). New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15, 508-515.
33. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
34. Newman, J. R. & Fuqua, C. (1999). Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227, 197-203.
35. Noë l, C. R., Mazar, J., Melvin, J. A., Sexton, J. A. & Cotter, P. A. (2012). The prodomain of the Bordetella two-partner secretion pathway protein FhaB remains intracellular yet affects the conformation of the mature C-terminal domain. Mol Microbiol 86, 988-1006.
36. Ostroff, R. M., Wretlind, B. & Vasil, M. L. (1989). Mutations in the hemolytic-phospholipase C operon result in decreased virulence of Pseudomonas aeruginosa PAO1 grown under phosphate-limiting conditions. Infect Immun 57, 1369-1373.
37. Petrova, O. E., Schurr, J. R., Schurr, M. J. & Sauer, K. (2011). The novel Pseudomonas aeruginosa two-component regulator BfmR controls bacteriophage-mediated lysis and DNA release during biofilm development through PhdA. Mol Microbiol 81, 767-783.
38. Relman, D. A., Domenighini, M., Tuomanen, E., Rappuoli, R. & Falkow, S. (1989). Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A 86, 2637-2641.
39. Renauld-Mongénie, G., Cornette, J., Mielcarek, N., Menozzi, F. D. & Locht, C. (1996). Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J Bacteriol 178, 1053-1060.
40. Sana, T. G., Hachani, A., Bucior, I., Soscia, C., Garvis, S., Termine, E., Engel, J., Filloux, A. & Bleves, S. (2012). The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J Biol Chem 287, 27095-27105.
41. Schleiff, E. & Soll, J. (2005). Membrane protein insertion: mixing eukaryotic and prokaryotic concepts. EMBO Rep 6, 1023-1027.
42. Spagnolo, J., Bigot, S., Denis, Y., Bordi, C. & de Bentzmann, S. (2012). Development of a genetic tool for activating chromosomal expression of cryptic or tightly regulated loci in Pseudomonas aeruginosa. Plasmid 67, 245-251.
43. St Geme, J. W., III & Yeo, H. J. (2009). A prototype two-partner secretion pathway: the Haemophilus influenzae HMW1 and HMW2 adhesin systems. Trends Microbiol 17, 355-360.
44. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6. 0. Mol Biol Evol 30, 2725-2729.
45. Tan, M. W., Rahme, L. G., Sternberg, J. A., Tompkins, R. G. & Ausubel, F. M. (1999). Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96, 2408-2413.
46. Thanassi, D. G., Stathopoulos, C., Karkal, A. & Li, H. (2005). Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/usher pathways of Gram-negative bacteria (review). Mol Membr Biol 22, 63-72.
47. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M. & Tommassen, J. (2003). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262-265.
48. Webb, J. S., Nikolakakis, K. C., Willett, J. L., Aoki, S. K., Hayes, C. S. & Low, D. A. (2013). Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition. PLoS ONE 8, e57609.
49. Willems, R. J., van der Heide, H. G. & Mooi, F. R. (1992). Characterization of a Bordetella pertussis fimbrial gene cluster which is located directly downstream of the filamentous haemagglutinin gene. Mol Microbiol 6, 2661-2671.
50. Willems, R. J., Geuijen, C., van der Heide, H. G., Renauld, G., Bertin, P., van den Akker, W. M., Locht, C. & Mooi, F. R. (1994). Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol Microbiol 11, 337-347.
51. Winsor, G. L., Lam, D. K., Fleming, L., Lo, R., Whiteside, M. D., Yu, N. Y., Hancock, R. E. & Brinkman, F. S. (2011). Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res 39 (Database issue), D596-D600.
52. Zaborin, A., Romanowski, K., Gerdes, S., Holbrook, C., Lepine, F., Long, J., Poroyko, V., Diggle, S. P., Wilke, A. & other authors (2009). Red death in Caenorhabditis elegans caused by Pseudomonas aeruginosa PAO1. Proc Natl Acad Sci U S A 106, 6327-6332.
53. Zaborina, O., Holbrook, C., Chen, Y., Long, J., Zaborin, A., Morozova, I., Fernandez, H., Wang, Y., Turner, J. R. & Alverdy, J. C. (2008). Structure-function aspects of PstS in multi-drug-resistant Pseudomonas aeruginosa. PLoS Pathog 4, e43.