BB0250 of Borrelia burgdorferi is a conserved and essential inner membrane protein required for cell division

Journal of Bacteriology

Volumn 192, Issue 23, 2010, Pages 6105-6115

  Liang, Fang Ting ^a   Xu, Qilong ^a   Sikdar, Rakesh ^a   Xiao, Ying ^a   Cox, James S ^a   Doerrler, William T ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROPYL THIOGALACTOSIDE; MEMBRANE PROTEIN; PHOSPHOLIPID; PROTEIN BB 0250; PROTEIN DEDA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BORRELIA BURGDORFERI; CELL DEATH; CELL DIVISION; CELL GROWTH; CELL MEMBRANE; CELL SIZE; ESCHERICHIA COLI; GENE DELETION; GRAM NEGATIVE BACTERIUM; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE SENSITIVITY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CELL DEATH; CELL DIVISION; CELL MEMBRANE; CONSERVED SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENES, ESSENTIAL; GENETIC COMPLEMENTATION TEST; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR SEQUENCE DATA; PHOSPHOLIPIDS; PROMOTER REGIONS, GENETIC; TRANSCRIPTIONAL ACTIVATION;

BACTERIA (MICROORGANISMS); BORRELIA; BORRELIA BURGDORFERI; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 78649345956     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00571-10     Document Type: Article

References (43)

1. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
2. Belisle, J. T., M. E. Brandt, J. D. Radolf, and M. V. Norgard. 1994. Fatty acids of Treponema pallidum and Borrelia burgdorferi lipoproteins. J. Bacteriol. 176:2151-2157.
3. Benach, J. L., E. M. Bosler, J. P. Hanrahan, J. L. Coleman, G. S. Habicht, T. F. Bast, D. J. Cameron, J. L. Ziegler, A. G. Barbour, W. Burgdorfer, R. Edelman, and R. A. Kaslow. 1983. Spirochetes isolated from the blood of two patients with Lyme disease. N. Engl. J. Med. 308:740-742.
4. Berks, B. C., T. Palmer, and F. Sargent. 2005. Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr. Opin. Microbiol. 8:174-181.
5. Berks, B. C., F. Sargent, and T. Palmer. 2000. The Tat protein export pathway. Mol. Microbiol. 35:260-274.
6. Bernhardt, T. G., and P. A. de Boer. 2003. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48:1171-1182.
7. Blevins, J. S., A. T. Revel, A. H. Smith, G. N. Bachlani, and M. V. Norgard. 2007. Adaptation of a luciferase gene reporter and lac expression system to Borrelia burgdorferi. Appl. Environ. Microbiol. 73:1501-1513.
8. Braga, P. C., M. Dal Sasso, and S. Maci. 1997. Cefodizime: effects of sub-inhibitory concentrations on adhesiveness and bacterial morphology of Staphylococcus aureus and Escherichia coli: comparison with cefotaxime and ceftriaxone. J. Antimicrob. Chemother. 39:79-84.
9. Burgdorfer, W., A. G. Barbour, S. F. Hayes, J. L. Benach, E. Grunwaldt, and J. P. Davis. 1982. Lyme disease - a tick-borne spirochetosis? Science 216:1317-1319.
10. Dalhoff, A., T. Nasu, and K. Okamoto. 2003. Target affinities of faropenem to and its impact on the morphology of Gram-positive and gram-negative bacteria. Chemotherapy 49:172-183. (Pubitemid 36928692)
11. De Buck, E., E. Lammertyn, and J. Anne. 2008. The importance of the twin-arginine translocation pathway for bacterial virulence. Trends Microbiol. 16:442-453.
12. Dilks, K., R. W. Rose, E. Hartmann, and M. Pohlschroder. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185:1478-1483.
13. Doerrler, W. T., and C. R. H. Raetz. 2005. Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant. J. Biol. Chem. 280:27679-27687.
14. Downie, A. B., L. M. Dirk, Q. Xu, J. Drake, D. Zhang, M. Dutt, A. Butterfield, R. R. Geneve, J. W. Corum III, K. G. Lindstrom, and J. C. Snyder. 2004. A physical, enzymatic, and genetic characterization of perturbations in the seeds of the brownseed tomato mutants. J. Exp. Bot. 55:961-973.
15. Dubytska, L., H. P. Godfrey, and F. C. Cabello. 2006. Borrelia burgdorferi ftsZ plays a role in cell division. J. Bacteriol. 188:1969-1978.
16. Elias, A. F., J. L. Bono, J. J. Kupko III, P. E. Stewart, J. G. Krum, and P. A. Rosa. 2003. New antibiotic resistance cassettes suitable for genetic studies in Borrelia burgdorferi. J. Mol. Microbiol. Biotechnol. 6:29-40.
17. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, J. Gocayne, J. Weidman, T. Utterback, L. Watthey, L. McDonald, P. Artiach, C. Bowman, S. Garland, C. Fuji, M. D. Cotton, K. Horst, K. Roberts, B. Hatch, H. O. Smith, and J. C. Venter. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
18. Heidrich, C., M. F. Templin, A. Ursinus, M. Merdanovic, J. Berger, H. Schwarz, M. A. de Pedro, and J. V. Holtje. 2001. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167-178.
19. Heidrich, C., A. Ursinus, J. Berger, H. Schwarz, and J. V. Holtje. 2002. Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J. Bacteriol. 184:6093-6099.
20. Hovius, J. W., A. P. van Dam, and E. Fikrig. 2007. Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol. 23:434-438.
21. Inadome, H., Y. Noda, Y. Kamimura, H. Adachi, and K. Yoda. 2007. Tvp38, Tvp23, Tvp18 and Tvp15: novel membrane proteins in the Tlg2-containing Golgi/endosome compartments of Saccharomyces cerevisiae. Exp. Cell Res. 313:688-697.
22. Ize, B., N. R. Stanley, G. Buchanan, and T. Palmer. 2003. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48:1183-1193.
23. Kudryashev, M., M. Cyrklaff, W. Baumeister, M. M. Simon, R. Wallich, and F. Frischknecht. 2009. Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol. Microbiol. 71:1415-1434.
24. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson, and D. G. Higgins. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
25. Lee, A. G. 2004. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 1666:62-87.
26. Lee, P. A., D. Tullman-Ercek, and G. Georgiou. 2006. The bacterial twin-arginine translocation pathway. Annu. Rev. Microbiol. 60:373-395.
27. Motaleb, M. A., L. Corum, J. L. Bono, A. F. Elias, P. Rosa, D. S. Samuels, and N. W. Charon. 2000. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl. Acad. Sci. U. S. A. 97:10899-10904.
28. Osborn, M. J., J. E. Gander, E. Parisi, and J. Carson. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J. Biol. Chem. 247:3962-3972.
29. Rosa, P. A., K. Tilly, and P. E. Stewart. 2005. The burgeoning molecular genetics of the Lyme disease spirochaete. Nat. Rev. Microbiol. 3:129-143.
30. Shi, Y., Q. Xu, S. V. Seemanapalli, K. McShan, and F. T. Liang. 2006. The dbpBA locus of Borrelia burgdorferi is not essential for infection of mice. Infect. Immun. 74:6509-6512.
31. Sikdar, R., and W. T. Doerrler. 2010. Inefficient Tat-dependent export of periplasmic amidases in an Escherichia coli strain with mutations in two DedA family genes. J. Bacteriol. 192:807-818.
32. Sohlenkamp, C., I. M. Lopez-Lara, and O. Geiger. 2003. Biosynthesis of phosphatidylcholine in bacteria. Prog. Lipid Res. 42:115-162.
33. Stanley, N. R., K. Findlay, B. C. Berks, and T. Palmer. 2001. Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J. Bacteriol. 183:139-144.
34. Steere, A. C., R. L. Grodzicki, A. N. Kornblatt, J. E. Craft, A. G. Barbour, W. Burgdorfer, G. P. Schmid, E. Johnson, and S. E. Malawista. 1983. The spirochetal etiology of Lyme disease. N. Engl. J. Med. 308:733-740.
35. Thompkins, K., B. Chattopadhyay, Y. Xiao, M. C. Henk, and W. T. Doerrler. 2008. Temperature sensitivity and cell division defects in an Escherichia coli strain with mutations in yghB and yqjA, encoding related and conserved inner membrane proteins. J. Bacteriol. 190:4489-4500.
36. Wang, X. G., J. P. Scagliotti, and L. T. Hu. 2004. Phospholipid synthesis in Borrelia burgdorferi: BB0249 and BB0721 encode functional phosphatidylcholine synthase and phosphatidylglycerolphosphate synthase proteins. Microbiology 150:391-397.
37. Xu, Q., K. McShan, and F. T. Liang. 2008. Essential protective role attributed to the surface lipoproteins of Borrelia burgdorferi against innate defences. Mol. Microbiol. 69:15-29.
38. Xu, Q., K. McShan, and F. T. Liang. 2007. Identification of an ospC operator critical for immune evasion of Borrelia burgdorferi. Mol. Microbiol. 64:220-231.
39. Xu, Q., S. V. Seemanapalli, L. Lomax, K. McShan, X. Li, E. Fikrig, and F. T. Liang. 2005. Association of linear plasmid 28-1 with an arthritic phenotype of Borrelia burgdorferi. Infect. Immun. 73:7208-7215.
40. Yang, Y., and C. Li. 2009. Transcription and genetic analyses of a putative N-acetylmuramyl-L-alanine amidase in Borrelia burgdorferi. FEMS Microbiol. Lett. 290:164-173.
41. Yook, K., and J. Hodgkin. 2007. MosI mutagenesis reveals a diversity of mechanisms affecting response of Caenorhabditis elegans to the bacterial pathogen Microbacterium nematophilum. Genetics 175:681-697. (Pubitemid 46798268)
42. Zhang, Y. M., and C. O. Rock. 2008. Membrane lipid homeostasis in bacteria. Nat. Rev. Microbiol. 6:222-233.
43. Zhou, Z., K. A. White, A. Polissi, C. Georgopoulos, and C. R. H. Raetz. 1998. Function of Escherichia coli MsbA, an essential ABC family transporter, in lipid A and phospholipid biosynthesis. J. Biol. Chem. 273:12466-12475.