Borrelia burgdorferi locus BB0795 encodes a BamA orthologue required for growth and efficient localization of outer membrane proteins

Molecular Microbiology

Volumn 75, Issue 3, 2010, Pages 692-709

  Lenhart, Tiffany R ^a   Akins, Darrin R ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOPROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN BAM A; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BORRELIA BURGDORFERI; CELLULAR DISTRIBUTION; GENE EXPRESSION; GENE LOCUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI; GENETIC LOCI; LIPOPROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; NEGIBACTERIA; SPIROCHAETALES;

EID: 75149192610     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.07015.x     Document Type: Article

References (93)

1. Arnold, K., Bordoli, L., Kopp, J. Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 : 195 201.
2. Bagos, P., Liakopoulos, T., Spyropoulos, I. Hamodrakas, S. (2004a) A Hidden Markov Model method, capable of predicting and discriminating beta-barrel outer membrane proteins. BMC Bioinformatics 5 : 29.
3. Bagos, P.G., Liakopoulos, T.D., Spyropoulos, I.C. Hamodrakas, S.J. (2004b) PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res 32 : W400 W404.
4. Barbour, A.G. (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57 : 521 525.
5. Belisle, J.T., Brandt, M.E., Radolf, J.D. Norgard, M.V. (1994) Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J Bacteriol 176 : 2151 2157.
6. Benach, J.L., Bosler, E.M., Hanrahan, J.P., Coleman, J.L., Habicht, G.S., Bast, T.F., et al. (1983) Spirochetes isolated from the blood of two patients with Lyme disease. N Engl J Med 308 : 740 742.
7. Bendtsen, J.D., Nielsen, H., von Heijne, G. Brunak, S. (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 : 783 795.
8. Ben-Menachem, G., Kubler-Kielb, J., Coxon, B., Yergey, A. Schneerson, R. (2003) A newly discovered cholesteryl galactoside from Borrelia burgdorferi. Proc Natl Acad Sci USA 100 : 7913 7918.
9. Bono, J.L., Tilly, K., Stevenson, B., Hogan, D. Rosa, P.A. (1998) Oligopeptide permease in Borrelia burgdorferi: putative peptide-binding components encoded by both chromosomal and plasmid loci. Microbiology 144 : 1033 1044.
10. Bordier, C. (1981) Phase separation of integral membrane proteins in Triton X-114 solution. J Biol Chem 256 : 1604 1607.
11. Bos, M.P., Tefsen, B., Geurtsen, J. Tommassen, J. (2004) Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci USA 101 : 9417 9422.
12. Bos, M.P., Robert, V. Tommassen, J. (2007) Biogenesis of the gram-negative bacterial outer membrane. Ann Rev Microbiol 61 : 191 214.
13. Brandt, M.E., Riley, B.S., Radolf, J.D. Norgard, M.V. (1990) Immunogenic integral membrane proteins of Borrelia burgdorferi are lipoproteins. Infect Immun 58 : 983 991.
14. Brooks, C.S., Vuppala, S.R., Jett, A.M., Alitalo, A., Meri, S. Akins, D.R. (2005) Complement regulator-acquiring surface protein 1 imparts resistance to human serum in Borrelia burgdorferi. J Immunol 175 : 3299 3308.
15. Brooks, C.S., Vuppala, S.R., Jett, A.M. Akins, D.R. (2006) Identification of Borrelia burgdorferi outer surface proteins. Infect Immun 74 : 296 304.
16. Brusca, J.S. Radolf, J.D. (1994) Isolation of integral membrane proteins by phase partitioning with Triton X-114. Methods Enzymol 228 : 182 193.
17. Bunikis, I., Denker, K., Ostberg, Y., Andersen, C., Benz, R. Bergstrom, S. (2008) An RND-type efflux system in Borrelia burgdorferi is involved in virulence and resistance to antimicrobial compounds. PLoS Pathog 4 : e1000009.
18. Bunikis, J., Noppa, L. Bergstrom, S. (1995) Molecular analysis of a 66-kDa protein associated with the outer membrane of Lyme disease Borrelia. FEMS Microbiol Lett 131 : 139 145.
19. Cameron, C.E., Lukehart, S.A., Castro, C., Molini, B., Godornes, C. Van Voorhis, W.C. (2000) Opsonic potential, protective capacity, and sequence conservation of the Treponema pallidum subspecies pallidum Tp92. J Infect Dis 181 : 1401 1413.
20. Casjens, S., Palmer, N., van Vugt, R., Huang, W.M., Stevenson, B., Rosa, P., et al. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35 : 490 516.
21. Chivian, D. Baker, D. (2006) Homology modeling using parametric alignment ensemble generation with consensus and energy-based model selection. Nucleic Acids Res 34 : e112.
22. Chivian, D., Kim, D.E., Malmstrom, L., Bradley, P., Robertson, T., Murphey, P., et al. (2003) Automated prediction of CASP-5 structures using the Robetta server. Proteins 53 : 524 533.
23. Chivian, D., Kim, D.E., Malmstrom, L., Schonbrun, J., Rohl, C.A. Baker, D. (2005) Prediction of CASP6 structures using automated Robetta protocols. Proteins 61 : 157 166.
24. Clantin, B., Delattre, A.S., Rucktooa, P., Saint, N., Meli, A.C., Locht, C., et al. (2007) Structure of the Membrane Protein FhaC: A Member of the Omp85-TpsB Transporter Superfamily. Science 317 : 957 961.
25. Cordes, F.S., Roversi, P., Kraiczy, P., Simon, M.M., Brade, V., Jahraus, O., et al. (2005) A novel fold for the factor H-binding protein BbCRASP-1 of Borrelia burgdorferi. Nat Struct Mol Biol 12 : 276 277.
26. Doerrler, W.T. Raetz, C.R.H. (2005) Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant. J Biol Chem 280 : 27679 27687.
27. Eggers, C.H., Caimano, M.J., Clawson, M.L., Miller, W.G., Samuels, D.S. Radolf, J.D. (2002) Identification of loci critical for replication and compatibility of a Borrelia burgdorferi cp32 plasmid and use of a cp32-based shuttle vector for the expression of fluorescent reporters in the Lyme disease spirochaete. Mol Microbiol 43 : 281 295.
28. Eiffert, H., Jarecki-Khan, K. Thomssen, R. (1991) Identification of an immunoreactive nonproteinaceous component in Borrelia burgdorferi. Med Microbiol Immunol 180 : 229 237.
29. Elias, A.F., Stewart, P.E., Grimm, D., Caimano, M.J., Eggers, C.H., Tilly, K., et al. (2002) Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect Immun 70 : 2139 2150.
30. Frank, K.L., Bundle, S.F., Kresge, M.E., Eggers, C.H. Samuels, D.S. (2003) aadA confers streptomycin resistance in Borrelia burgdorferi. J Bacteriol 185 : 6723 6727.
31. Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390 : 580 586.
32. Fraser, C.M., Norris, S.J., Weinstock, G.M., White, O., Sutton, G.C., Dodson, R., et al. (1998) Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281 : 375 388.
33. Fuchs, R., Jauris, S., Lottspeich, F., Preac-Mursic, V., Wilske, B. Soutschek, E. (1992) Molecular analysis and expression of a Borrelia burgdorferi gene encoding a 22kDa protein (pC) in Escherichia coli. Mol Microbiol 6 : 503 509.
34. Gatzeva-Topalova, P.Z., Walton, T.A. Sousa, M.C. (2008) Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure 16 : 1873 1881.
35. Genevrois, S., Steeghs, L., Roholl, P., Letesson, J.J. van der Ley, P. (2003) The Omp85 protein of Neisseria meningitidis is required for lipid export to the outer membrane. EMBO J 22 : 1780 1789.
36. Gentle, I., Gabriel, K., Beech, P., Waller, R. Lithgow, T. (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164 : 19 24.
37. Gentle, I., Burri, L. Lithgow, T. (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58 : 1216 1225.
38. Gilbert, M.A., Morton, E.A., Bundle, S.F. Samuels, D.S. (2007) Artificial regulation of ospC expression in Borrelia burgdorferi. Mol Microbiol 63 : 1259 1273.
39. Guo, B., Norris, S.J., Rosenberg, L.C. Hook, M. (1995) Adherence of Borrelia burgdorferi to the proteoglycan decorin. Infect Immun 63 : 3467 3472.
40. Hossain, H., Wellensiek, H.J., Geyer, R. Lochnit, G. (2001) Structural analysis of glycolipids from Borrelia burgdorferi. Biochimie 83 : 683 692.
41. Howe, T.R., Mayer, L.W. Barbour, A.G. (1985) A single recombinant plasmid expressing two major outer surface proteins of the Lyme disease spirochete. Science 227 : 645 646.
42. Humphrey, W., Dalke, A. Schulten, K. (1996) VMD: visual molecular dynamics. J Mol Graph 14 : 33 38.
43. Jun, H.K., Kang, Y.M., Lee, H.R., Lee, S.H. Choi, B.K. (2008) Highly conserved surface proteins of oral spirochetes as adhesins and potent inducers of proinflammatory and osteoclastogenic factors. Infect Immun 76 : 2428 2438.
44. Kenedy, M.R., Vuppala, S.R., Siegel, C., Kraiczy, P. Akins, D.R. (2009) CspA-mediated binding of human factor H inhibits complement deposition and confers serum resistance in Borrelia burgdorferi. Infect Immun 77 : 2773 2782.
45. Kim, D.E., Chivian, D. Baker, D. (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32 : W526 W531.
46. Kim, D.E., Chivian, D., Malmstrom, L. Baker, D. (2005) Automated prediction of domain boundaries in CASP6 targets using Ginzu and RosettaDOM. Proteins 61 : 193 200.
47. Kim, S., Malinverni, J.C., Sliz, P., Silhavy, T.J., Harrison, S.C. Kahne, D. (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317 : 961 964.
48. Kinjo, Y., Tupin, E., Wu, D., Fujio, M., Garcia-Navarro, R., Benhnia, M.R., et al. (2006) Natural killer T cells recognize diacylglycerol antigens from pathogenic bacteria. Nat Immunol 7 : 978 986.
49. Knowles, T.J., Jeeves, M., Bobat, S., Dancea, F., McClelland, D., Palmer, T., et al. (2008) Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol Microbiol 68 : 1216 1227.
50. Knowles, T.J., Scott-Tucker, A., Overduin, M. Henderson, I.R. (2009) Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat Rev Microbiol 7 : 206 214.
51. Kraiczy, P., Hellwage, J., Skerka, C., Becker, H., Kirschfink, M., Simon, M.M., et al. (2004) Complement resistance of Borrelia burgdorferi correlates with the expression of BbCRASP-1, a novel linear plasmid-encoded surface protein that interacts with human factor H and FHL-1 and is unrelated to Erp proteins. J Biol Chem 279 : 2421 2429.
52. Kyte, J. Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157 : 105 132.
53. Lam, T.T., Nguyen, T.P.K., Montgomery, R.R., Kantor, F.S., Fikrig, E. Flavell, R.A. (1994) Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease. Infect Immun 62 : 290 298.
54. Li, H., Dunn, J.J., Luft, B.J. Lawson, C.L. (1997) Crystal structure of Lyme disease antigen outer surface protein A complexed with an Fab. Proc Natl Acad Sci USA 94 : 3584 3589.
55. Link, A.J., Robison, K. Church, G.M. (1997) Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18 : 1259 1313.
56. Lugtenberg, B. van Alphen, L. (1983) Molecular architecture and functioning of the outer membrane of Escherichia coli and other Gram-negative bacteria. Biochim Biophys Acta 737 : 51 115.
57. McDowell, J.V., Sung, S.Y., Labandeira-Rey, M., Skare, J.T. Marconi, R.T. (2001) Analysis of mechanisms associated with loss of infectivity of clonal populations of Borrelia burgdorferi B31MI. Infect Immun 69 : 3670 3677.
58. Malinverni, J.C., Werner, J., Kim, S., Sklar, J.G., Kahne, D., Misra, R. Silhavy, T. (2006) YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61 : 151 164. (Pubitemid 43911505)
59. Matsuyama, S., Tajima, T. Tokuda, H. (1995) A novel periplasmic carrier protein involved in the sorting and transport of Escherichia coli lipoproteins destined for the outer membrane. EMBO J 14 : 3365 3372.
60. Mulay, V., Caimano, M., Liveris, D., Desrosiers, D.C., Radolf, J.D. Schwartz, I. (2007) Borrelia burgdorferi BBA74, a periplasmic protein associated with the outer membrane, lacks porin-like properties. J Bacteriol 189 : 2063 2068.
61. Noppa, L., Ostberg, Y., Lavrinovicha, M. Bergstrom, S. (2001) P13, an integral membrane protein of Borrelia burgdorferi, is C-terminally processed and contains surface-exposed domains. Infect Immun 69 : 3323 3334.
62. Norris, S.J., Carter, C.J., Howell, J.K. Barbour, A.G. (1992) Low-passage-associated proteins of Borrelia burgdorferi B31: characterization and molecular cloning of OspD, a surface-exposed, plasmid-encoded lipoprotein. Infect Immun 60 : 4662 4672.
63. Nowalk, A.J., Gilmore, R.D., Jr. Carroll, J.A. (2006) Serologic proteome analysis of Borrelia burgdorferi membrane-associated proteins. Infect Immun 74 : 3864 3873.
64. Papanikou, E., Karamanou, S. Economou, A. (2007) Bacterial protein secretion through the translocase nanomachine. Nat Rev Microbiol 5 : 839 851.
65. Probert, W.S. Johnson, B.J.B. (1998) Identification of a 47 kDa fibronectin-binding protein expressed by Borrelia burgdorferi isolate B31. Mol Microbiol 30 : 1003 1015.
66. Probert, W.S., Allsup, K.M. LeFebvre, R.B. (1995) Identification and characterization of a surface-exposed 66-kilodalton protein from Borrelia burgdorferi. Infect Immun 63 : 1933 1939.
67. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57 : 50 108.
68. Purser, J.E. Norris, S.J. (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci USA 97 : 13865 13870.
69. Purser, J.E., Lawrenz, M.B., Caimano, M.J., Howell, J.K., Radolf, J.D. Norris, S.J. (2003) A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48 : 753 764.
70. Radolf, J.D., Bourell, K.W., Akins, D.R., Brusca, J.S. Norgard, M.V. (1994) Analysis of Borrelia burgdorferi membrane architecture by freeze-fracture electron microscopy. J Bacteriol 176 : 21 31.
71. Reumann, S., Davila-Aponte, J. Keegstra, K. (1999) The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: Identification of a cyanobacterial homolog. Proc Natl Acad Sci USA 96 : 784 789.
72. Robert, V., Volokhina, E.B., Senf, F., Bos, M.P., Gelder, P.V. Tommassen, J. (2006) Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4 : e377.
73. Rohl, C.A., Strauss, C.E., Chivian, D. Baker, D. (2004) Modeling structurally variable regions in homologous proteins with Rosetta. Proteins 55 : 656 677.
74. Samuels, D.S. (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47 : 253 259.
75. Sanchez-Pulido, L., Devos, D., Genevrois, S., Vicente, M. Valencia, A. (2003) POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. Trends Biochem Sci 28 : 523 526.
76. Schulze, R.J. Zuckert, W.R. (2006) Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol Microbiol 59 : 1473 1484.
77. Skare, J.T., Shang, E.S., Foley, D.M., Blanco, D.R., Champion, C.I., Mirzabekov, T., et al. (1995) Virulent strain associated outer membrane proteins of Borrelia burgdorferi. J Clin Invest 96 : 2380 2392.
78. Sklar, J.G., Wu, T., Gronenberg, L.S., Malinverni, J.C., Kahne, D. Silhavy, T.J. (2007) Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci USA 104 : 6400 6405.
79. Steere, A.C., Grodzicki, R.L., Kornblatt, A.N., Craft, J.E., Barbour, A.G., Burgdorfer, W., et al. (1983) The spirochetal etiology of Lyme disease. N Engl J Med 308 : 733 740.
80. Stegmeier, J.F. Andersen, C. (2006) Characterization of pores formed by YaeT (Omp85) from Escherichia coli. J Biochem 140 : 275 283.
81. Stewart, P., Thalken, R., Bono, J. Rosa, P. (2001) Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol Microbiol 39 : 714 721.
82. Sun, G., Pal, S., Sarcon, A.K., Kim, S., Sugawara, E., Nikaido, H., et al. (2007) Structural and functional analyses of the major outer membrane protein of Chlamydia trachomatis. J Bacteriol 189 : 6222 6235.
83. Thomas, K.L., Leduc, I., Olsen, B., Thomas, C.E., Cameron, D.W. Elkins, C. (2001) Cloning, overexpression, purification, and immunobiology of an 85-kilodalton outer membrane protein from Haemophilus ducreyi. Infect Immun 69 : 4438 4446.
84. Tokuda, H. (2009) Biogenesis of outer membranes in Gram-negative bacteria. Biosci Biotechnol Biochem 73 : 465 473.
85. Voulhoux, R. Tommassen, J. (2004) Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res Microbiol 155 : 129 135.
86. 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.
87. Vuong, P., Bennion, D., Mantei, J., Frost, D. Misra, R. (2008) Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry. J Bacteriol 190 : 1507 1517.
88. Wallich, R., Pattathu, J., Kitiratschky, V., Brenner, C., Zipfel, P.F., Brade, V., et al. (2005) Identification and functional characterization of complement regulator-acquiring surface protein 1 of the Lyme disease spirochetes Borrelia afzelii and Borrelia garinii. Infect Immun 73 : 2351 2359.
89. Waterhouse, A.M., Procter, J.B., Martin, D.M.A., Clamp, M. Barton, G.J. (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 : 1189 1191.
90. Werner, J. Misra, R. (2005) YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol Microbiol 57 : 1450 1459.
91. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T.J. Kahne, D. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121 : 235 245.
92. Yokota, N., Kuroda, T., Matsuyama, S. Tokuda, H. (1999) Characterization of the LolA-LolB system as the general lipoprotein localization mechanism of Escherichia coli. J Biol Chem 274 : 30995 30999.
93. Zhang, J.R., Hardham, J.M., Barbour, A.G. Norris, S.J. (1997) Antigenic variation in Lyme disease Borreliae by promiscuous recombination of Vmp-like sequence cassettes. Cell 89 : 275 285.