Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens

Biochimica et Biophysica Acta - Biomembranes

Volumn 1611, Issue 1-2, 2003, Pages 223-233

  Ma, Qinhong ^a   Zhai, Yufeng ^a,c   Schneider, Jane C ^b   Ramseier, Tom M ^b   Saier Jr , Milton H ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b DOW CHEMICAL COMPANY   (United States)

^c BIOGEN   (United States)

Author keywords

Gram negative bacteria; Membrane insertion; Protein; Pseudomonas; Secretion

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENOME; CONTROLLED STUDY; ENERGY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; SYMBIONT;

INSERTION SEQUENCES; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS;

EID: 0037376783     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0005-2736(03)00059-2     Document Type: Article

References (96)

1. Saier M.H. Jr. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64:2000;354-411.
2. Manting E.H., Driessen A.J. Escherichia coli translocase: the unravelling of a molecular machine. Mol. Microbiol. 37:2000;226-238.
3. Müller M., Koch H.G., Beck K., Schäfer U. Protein traffic in bacteria: multiple routes from the ribosome to and across the membrane. Prog. Nucleic Acid Res. Mol. Biol. 66:2001;107-157.
4. Cao T.B., Saier M.H. Jr. The general protein secretory (Sec) pathway: phylogenetic analyses leading to evolutionary conclusions. Biochim. Biophys. Acta. 1609:2003;115-125.
5. de Gier J.-W., Luirink J. Biogenesis of inner membrane proteins in Escherichia coli. Mol. Microbiol. 40:2001;314-322.
6. Luirink J., Samuelsson T., de Gier J.-W. YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly. FEBS Lett. 501:2001;1-5.
7. Yen M.-R., Harley K.T., Tseng Y.-H., Saier M.H. Jr. Phylogenetic and structural analyses of the Oxa1 family of protein translocases. FEMS Microbiol. Lett. 204:2001;223-231.
8. Berks B.C., Sargent F., Palmer T. The Tat protein export pathway. Mol. Microbiol. 35:2000;260-274.
9. Yen M.-R., Tseng Y.-H., Nguyen E.H., Wu L.-F., Saier M.H. Jr. Sequence and phylogenetic analyses of the twin arginine targeting (Tat) protein export system. Arch. Microbiol. 177:2002;441-450.
10. Saier M.H. Jr. Families of transmembrane transporters selective for amino acids and their derivatives. Microbiology. 146:2000;1775-1795.
11. Sandkvist M. Biology of type II secretion. Mol. Microbiol. 40:2001;271-283.
12. Thanassi D.G., Hultgren S.J. Multiple pathways allow protein secretion across the bacterial outer membrane. Curr. Opin. Cell Biol. 12:2000;420-430.
13. Yen M.-R., Peabody C.R., Partovi S.M., Zhai Y., Tseng Y.-H., Saier M.H. Jr. Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim. Biophys. Acta. 1562:2002;6-31.
14. Baron C., Ocallaghan D., Lanka E. Bacterial secrets of secretion: EuroConference on the biology of type IV secretion processes. Mol. Microbiol. 43:2002;1359-1365.
15. Llosa M., Gomis-Ruth F.X., Coll M., de la Cruz F. Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol. 45:2002;1-8.
16. Pantoja M., Chen L., Chen Y., Nester E.W. Agrobacterium type IV secretion is a two-step process in which export substrates associate with the virulence protein VirJ in the periplasm. Mol. Microbiol. 45:2002;1325-1335.
17. Binet R., Létoffé S., Ghigo J.M., Delepelaire P., Wandersman C. Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene. 192:1997;7-11.
18. Cao T.B., Saier M.H. Jr. Conjugal type IV macromolecular transfer systems of Gram-negative bacteria: organismal distribution, structural constraints and evolutionary conclusions. Microbiology. 147:2001;3201-3214.
19. Nguyen L., Paulsen I.T., Tchieu J., Hueck C.J., Saier M.H. Jr. Phylogenetic analyses of the constituents of type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2:2000;125-144.
20. Paulsen I.T., Park J.H., Choi P.S., Saier M.H. Jr. A family of Gram-negative bacterial outer membrane factors that function in the export of proteins, carbohydrates, drugs and heavy metals from Gram-negative bacteria. FEMS Microbiol. Lett. 156:1997;1-8.
21. Mol O., Oudega B. Molecular and structural aspects of fimbriae biosynthesis and assembly in Escherichia coli. FEMS Microbiol. Rev. 19:1996;25-52.
22. Sauer F.G., Barnhart M., Choudhury D., Knight S.D., Waksman G., Hultgren S.J. Chaperone-assisted pilus assembly and bacterial attachment. Curr. Opin. Struct. Biol. 10:2000;548-556.
23. Van Rosmalen M., Saier M.H. Jr. Structural and evolutionary relationships between two families of bacterial extracytoplasmic chaperone proteins which function cooperatively in fimbrial assembly. Res. Microbiol. 144:1993;507-527.
24. Henderson I.R., Navarro-Garcia F., Nataro J.P. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 6:1998;370-378.
25. Loveless B.J., Saier M.H. Jr. A novel family of autotransporting, channel-forming, bacterial virulence proteins. Mol. Membr. Biol. 14:1997;113-123.
26. Jacob-Dubuisson F., Locht C., Antoine R. Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol. Microbiol. 40:2001;306-313.
27. Lee V.T., Schneewind O. Protein secretion and the pathogenesis of bacterial infections. Genes Dev. 15:2001;1725-1752.
28. Stover K.C., 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., 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. 406:2000;959-964.
29. Gerritse G., Hommes R.W., Quax W.J. Development of a lipase fermentation process that uses a recombinant Pseudomonas alcaligenes strain. Appl. Environ. Microbiol. 64:1998;1651-2644.
30. Bender C.L., Palmer D.A., Penaloza-Vazquez A., Rangaswamy V., Ullrich M. Biosynthesis and regulation of coronatine, a non-host-specific phytotoxin produced by Pseudomonas syringae. Subcell. Biochem. 29:1998;321-341.
31. Bender C., Rangaswamy V., Loper J. Polyketide production by plant-associated pseudomonads. Annu. Rev. Phytopathol. 37:1999;175-196.
32. O'Tool G., Kaplan H.B., Kolter R. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:2000;49-79.
33. Pereira M.O., Kuehn M., Wuertz S., Neu T., Melo L.F. Effect of flow regime on the architecture of a Pseudomonas fluorescens biofilm. Biotechnol. Bioeng. 78:2002;164-171.
34. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:1997;3389-3402.
35. Sonnhammer E.L., Eddy S.R., Durbin R. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins. 28:1997;405-420.
36. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:2001;567-580.
37. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. A neural network method for identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Int. J. Neural Syst. 8:1997;581-599.
38. Nielsen H., Brunak S., von Heijne G. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 12:1999;3-9.
39. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:1997;4876-4882.
40. Jones D.T. Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292:1999;195-202.
41. Le T., Tseng T.-T., Saier M.H. Jr. Flexible programs for the estimation of average amphipathicity of multiply aligned homologous proteins: application to integral membrane transport proteins. Mol. Membr. Biol. 16:1999;173-179.
42. Zhai Y., Saier M.H. Jr. A web-based program (WHAT) for the simultaneous prediction of hydropathy, amphipathicity, secondary structure and transmembrane topology for a single protein sequence. J. Mol. Microbiol. Biotechnol. 3:2001;501-502.
43. Young R. Bacteriophage lysis: mechanism and regulation. Microbiol. Rev. 56:1992;430-481.
44. Ajouz B., Berrier C., Garrigues A., Besnard M., Ghazi A. Release of thioredoxin via the mechanosensitive channel MscL during osmotic downshock of Escherichia coli cells. J. Biol. Chem. 273:1998;26670-26674.
45. Kloda A., Martinac B. Mechanosensitive channels in archaea. Cell Biochem. Biophys. 34:2001;349-381.
46. Koprowski P., Kubalski A. Bacterial ion channels and their eukaryotic homologues. BioEssays. 23:2001;1148-1158.
47. Wang I.N., Smith D.L., Young R. Holins. The protein clocks of bacteriophage infections. Annu. Rev. Microbiol. 54:2000;799-825.
48. Agarrabeus F.A., Dice J.F. Protein translocation across membranes. Biochim. Biophys. Acta. 1513:2001;1-24.
49. Tseng T.-T., Gratwick K.S., Kollman J., Park D., Nies D.H., Goffeau A., Saier M.H. Jr. The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol. 1:1999;107-125.
50. Samuelson J.C., Jiang F., Yi L., Chen M., de Gier J.W., Kuhn A., Dalbey R.E. Function of YidC for the insertion of M13 procoat protein in Escherichia coli: translocation of mutants that show differences in their membrane potential dependence and Sec requirement. J. Biol. Chem. 276:2001;34847-34852.
51. Seluanov A., Bibi E. FtsY, the prokaryotic signal recognition particle receptor homologue, is essential for biogenesis of membrane proteins. J. Biol. Chem. 272:1997;2053-2055.
52. Chen M., Samuelson J.C., Jiang F., Muller M., Kuhn A., Dalbey R.E. Direct interaction of YidC with the Sec-independent Pf3 coat protein during its membrane protein insertion. J. Biol. Chem. 277:2002;7670-7675.
53. Samuelson J.C., Chen M., Jiang F., Moller I., Wiedmann M., Kuhn A., Phillips G.J., Dalbey R.E. YidC mediates membrane protein insertion in bacteria. Nature. 406:2000;637-641.
54. Paetzel M., Strynadka N.C., Tschantz W.R., Casareno R., Bullinger P.R., Dalbey R.E. Use of site-directed chemical modification to study an essential lysine in Escherichia coli leader peptidase. J. Biol. Chem. 272:1997;9994-10003.
55. Tschantz W.R., Sung M., Delgado-Partin V.M., Dalbey R.E. A serine and a lysine residue implicated in the catalytic mechanism of the Escherichia coli leader peptidase. J. Biol. Chem. 268:1993;27349-27354.
56. Bogsch E.G., Sargent F., Stanley N.R., Berks B.C., Robinson C., Palmer T. An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J. Biol. Chem. 273:1998;18003-18006.
57. Sargent F., Stanley N.R., Berks B.C., Palmer T. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 274:1999;36073-36082.
58. Heikkilä M.P., Honisch U., Wunsch P., Zumft W.G. Role of the Tat transport system in nitrous oxide reductase translocation and cytochrome cd1 biosynthesis in Pseudomonas stutzeri. J. Bacteriol. 183:2001;1663-1671.
59. Ochsner U.A., Snyder A., Vasil A.I., Vasil M.L. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 99:2002;8312-8317.
60. Voulhoux R., Ball G., Ize B., Vasil M.L., Lazdunski A., Wu L.-F., Filloux A. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J. 20:2001;6735-6741.
61. Wang I.N., Dykhuizen D.E., Slobodkin L.B. The evolution of phage lysis timing. Evol. Ecol. 10:1996;545-558.
62. Nakayama K., Takashima K., Ishihara H., Shinomiya T., Kageyama M., Kanaya S., Ohnishi M., Murata T., Mori H., Hayashi T. The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol. Microbiol. 38:2000;213-231.
63. Chang G., Spencer R.H., Lee A.T., Barclay M.T., Rees D.C. Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. Science. 282:1998;2220-2226.
64. Rees D.C., Chang G., Spencer R.H. Crystallographic analyses of ion channels: lessons and challenges. J. Biol. Chem. 275:2000;713-716.
65. Pivetti C.D., Yen M.-R., Miller S., Busch W., Tseng Y.-H., Booth I.R., Saier M.H. Jr. Two families of prokaryotic mechanosensitive channel proteins. Microbiol. Mol. Biol. Rev. 2003;. (in press).
66. Ahn J.H., Pan J.G., Rhee J.S. Identification of the tliDEF ABC transporter specific for lipase in Pseudomonas fluorescens SIK W1. J. Bacteriol. 181:1999;1847-1852.
67. Ahn J.H., Pan J.G., Rhee J.S. Homologous expression of the lipase and ABC transporter gene cluster, tliDEF, enhances lipase secretion in Pseudomonas spp. Appl. Environ. Microbiol. 67:2001;5506-5511.
68. Chabeaud P., de Groot A., Bitter W., Tommassen J., Heulin T., Achouak W. Phase-variable expression of an operon encoding extracellular alkaline protease, a serine protease homolog, and lipase in Pseudomonas brassicacearum. J. Bacteriol. 183:2001;2117-2120.
69. Duong F., Lazdunski A., Cami B., Murgier M. Sequence of a cluster of genes controlling synthesis and secretion of alkaline protease in Pseudomonas aeruginosa: relationships to other secretory pathways. Gene. 121:1992;47-54.
70. Kawai E., Idei A., Kumura H., Shimazaki K., Akatsuka H., Omori K. The ABC-exporter genes involved in the lipase secretion are clustered with the genes for lipase, alkaline protease, and serine protease homologues in Pseudomonas fluorescens no. 33. Biochim. Biophys. Acta. 1446:1999;377-382.
71. Liao C.H., McCallus D.E. Biochemical and genetic characterization of an extracellular protease from Pseudomonas fluorescens CY091. Appl. Environ. Microbiol. 64:1998;914-921.
72. Woods R.G., Burger M., Beven C.A., Beacham I.R. The aprX-lipA operon of in Pseudomonas fluorescens B52: a molecular analysis of metalloprotease and lipase production. Microbiology. 147:2001;345-354.
73. Guzzo J., Pages J.M., Duong F., Lazdunski A., Murgier M. Pseudomonas aeruginosa alkaline protease: evidence for secretion genes and study of secretion mechanism. J. Bacteriol. 173:1991;5290-5297.
74. Beven C.A., Dieckelmann M., Beacham I.R. A strain of Pseudomonas fluorescens with two lipase-encoding genes, one of which possibly encodes cytoplasmic lipolytic activity. J. Appl. Microbiol. 90:2001;979-987.
75. Felmlee T., Welch R.A. Alterations of amino acid repeats in the Escherichia coli hemolysin affect cytolytic activity and secretion. Proc. Natl. Acad. Sci. U. S. A. 85:1988;5269-5273.
76. Ghigo J.M., Wandersman C. A carboxyl-terminal four-amino acid motif is required for secretion of the metalloprotease PrtG through the Erwinia chrysanthemi protease secretion pathway. J. Biol. Chem. 269:1994;8979-8985.
77. Duong F., Bonnet E., Geli V., Lazdunski A., Murgier M., Filloux A. The AprX protein of Pseudomonas aeruginosa: a new substrate for the Apr type I secretion system. Gene. 262:2001;147-153.
78. Idei A., Kawai E., Akatsuka H., Omori K. Cloning and characterization of the Pseudomonas fluorescens ATP-binding cassette exporter, HasDEF, for the heme acquisition protein HasA. J. Bacteriol. 181:1999;7451-7545.
79. Buell C.R., Anderson A.J. Genetic analysis of the aggA locus involved in agglutination and adherence of Pseudomonas putida, a beneficial fluorescent pseudomonad. Mol. Plant-Microb. Interact. 5:1992;154-162.
80. Hueck C.J. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:1998;379-433.
81. Aizawa S.-I. Bacterial flagella and type III secretion systems. FEMS Microbiol. Lett. 202:2001;157-164.
82. Yahr T.L., Goranson J., Frank D.W. Exoenzymes of Pseudomonas aeruginosa is secreted by type III pathway. Mol. Microbiol. 22:1996;991-1003.
83. Yahr T.L., Mende-Mueller L.M., Friese M.B., Frank D.W. Identification of type III secreted products of the Pseudomonas aeruginosa exoenzyme S regulon. J. Bacteriol. 179:1997;7165-7168.
84. Yahr T.L., Vallis A.J., Hancock M.K., Barbieri J.T., Frank D.W. ExoY, an adenylate cyclase secreted by the Pseudomonas aeruginosa type III system. Proc. Natl. Acad. Sci. U. S. A. 95:1998;13899-13904.
85. Preston G.M., Bertrand N., Rainey P.B. Type III secretion in plant growth-promoting Pseudomonas fluorescens SBW25. Mol. Microbiol. 41:2001;999-1014.
86. Filloux A., Michel G., Bally M. GSP-dependent protein secretion in Gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. FEMS Microbiol. Rev. 22:1998;177-198.
87. Chapon-Herve V., Akrim M., Latifi A., Williams P., Lazdunski A., Bally M. Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol. Microbiol. 24:1997;1169-1178.
88. Ball G., Durand E., Lazdunski A., Filloux A. A novel type II secretion system in Pseudomonas aeruginosa. Mol. Microbiol. 43:2002;475-485.
89. Martinez A., Ostrovsky P., Nunn D.N. Identification of an additional member of the secretin superfamily of proteins in Pseudomonas aeruginosa that is able to function in type II protein secretion. Mol. Microbiol. 28:1998;1235-1246.
90. Vallet I., Olson J.W., Lory S., Lazdunski A., Filloux A. The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc. Natl. Acad. Sci. U. S. A. 98:2001;6911-6916.
91. Koebnik R., Locher K.P., Van Gelder P. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:2000;239-253.
92. Tamm L.K., Arora A., Kleinschmidt J.H. Structure and assembly of beta-barrel membrane proteins. J. Biol. Chem. 276:2001;32399-323402.
93. Veiga E., Sugawara E., Nikaido H., de Lorenzo V., Fernandez L.A. Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J. 21:2002;2122-2131.
94. Wilhelm S., Tommassen J., Jaeger K.E. A novel lipolytic enzyme located in the outer membrane of Pseudomonas aeruginosa. J. Bacteriol. 181:1999;6977-6986.
95. Loosmore S.M., Yang Y.P., Coleman D.C., Shortreed J.M., England D.M., Klein M.H. Outer membrane protein D15 is conserved among Haemophilus influenzae species and may represent a universal protective antigen against invasive disease. Infect. Immun. 65:1997;3701-3707.
96. Létoffé S., Redeker V., Wandersman C. Isolation and characterization of an extracellular haembinding protein from Pseudomonas aeruginosa that shares function and sequence similarities with the Serratia marcescens HasA haemophore. Mol. Microbiol. 28:1998;1223-1234.