A deficiency in arabinogalactan biosynthesis affects Corynebacterium glutamicum mycolate outer membrane stability

Journal of Bacteriology

Volumn 192, Issue 11, 2010, Pages 2691-2700

  Raad, Roland Bou ^a   Méniche, Xavier ^a,b   De Sousa D'Auria, Celia ^c   Chami, Mohamed ^d   Salmeron, Christophe ^a   Tropis, Marielle ^b   Labarre, Cecile ^c   Daffé, Mamadou ^b   Houssin, Christine ^c   Bayan, Nicolas ^a  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b UNIVERSITÉ PAUL SABATIER   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AFTB PROTEIN; ARABINOGALACTAN; MUTANT PROTEIN; MYCOLOYLTRANSFERASE; OUTER MEMBRANE PROTEIN; PHOSPHOLIPID; PORH PROTEIN; PORIN; PORIN A; PROTEIN PS2; TRANSFERASE; TREHALOSE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; GALACTAN;

ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; CARBOHYDRATE SYNTHESIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CORYNEBACTERIUM GLUTAMICUM; CULTURE MEDIUM; HYDROPHOBICITY; MEMBRANE STABILIZATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; BIOSYNTHESIS; CELL MEMBRANE; CHEMISTRY; CRYOELECTRON MICROSCOPY; GENETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYACRYLAMIDE GEL ELECTROPHORESIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

CORYNEBACTERINEAE; CORYNEBACTERIUM GLUTAMICUM; MYCOBACTERIUM TUBERCULOSIS; POSIBACTERIA;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CELL MEMBRANE; CORYNEBACTERIUM GLUTAMICUM; CRYOELECTRON MICROSCOPY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GALACTANS; MAGNETIC RESONANCE SPECTROSCOPY; MICROSCOPY, ELECTRON, TRANSMISSION;

EID: 77952577998     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00009-10     Document Type: Article

References (67)

1. Adindla, S., K. K. Inampudi, K. Guruprasad, and L. Guruprasad. 2004. Identification and analysis of novel tandem repeats in the cell surface proteins of archaeal and bacterial genomes using computational tools. Comp. Funct. Genomics 5:2-16.
2. Aggerbeck, L. P., and T. Gulik-Krzywicki. 1986. Studies of lipoproteins by freeze-fracture and etching electron microscopy. Methods Enzymol. 128:457-472. (Pubitemid 16100911)
3. Alderwick, L. J., E. Radmacher, M. Seidel, R. Gande, P. G. Hitchen, H. R. Morris, A. Dell, H. Sahm, L. Eggeling, and G. S. Besra. 2005. Deletion of Cg-emb in corynebacterianeae leads to a novel truncated cell wall arabinogalactan, whereas inactivation of Cg-ubiA results in an arabinan-deficient mutant with a cell wall galactan core. J. Biol. Chem. 280:32362-32371.
4. Alderwick, L. J., M. Seidel, H. Sahm, G. S. Besra, and L. Eggeling. 2006. Identification of a novel arabinofuranosyltransferase (AftA) involved in cell wall arabinan biosynthesis in Mycobacterium tuberculosis. J. Biol. Chem. 281:15653-15661.
5. Anderson, D. H., G. Harth, M. A. Horwitz, and D. Eisenberg. 2001. An interfacial mechanism and a class of inhibitors inferred from two crystal structures of the Mycobacterium tuberculosis 30 kDa major secretory protein (antigen 85B), a mycolyl transferase. J. Mol. Biol. 307:671-681.
6. Barth, E., M. A. Barcelo, C. Klackta, and R. Benz. 2010. Reconstitution experiments and gene deletions reveal the existence of two-component major cell wall channels in the genus Corynebacterium. J. Bacteriol. 192:786-800.
7. Belisle, J. T., V. D. Vissa, T. Sievert, K. Takayama, P. J. Brennan, and G. S. Besra. 1997. Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276:1420-1422.
8. Bernadac, A., M. Gavioli, J. C. Lazzaroni, S. Raina, and R. Lloubes. 1998. Escherichia coli tol-pal mutants form outer membrane vesicles. J. Bacteriol. 180:4872-4878. (Pubitemid 28429375)
9. Birch, H. L., L. J. Alderwick, A. Bhatt, D. Rittmann, K. Krumbach, A. Singh, Y. Bai, T. L. Lowary, L. Eggeling, and G. S. Besra. 2008. Biosynthesis of mycobacterial arabinogalactan: identification of a novel alpha(1-33) arabinofuranosyltransferase. Mol. Microbiol. 69:1191-1206.
10. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
11. Bokas, D., D. Uy, F. Grattepanche, G. Duportail, E. Guedon, S. Delaunay, and J. L. Goergen. 2007. Cell envelope fluidity modification for an effective glutamate excretion in Corynebacterium glutamicum 2262. Appl. Microbiol. Biotechnol. 76:773-781.
12. Bonamy, C., A. Guyonvarch, O. Reyes, F. David, and G. Leblon. 1990. Interspecies electro-transformation in Corynebacteria. FEMS Microbiol. Lett. 54:263-269.
13. Brand, S., K. Niehaus, A. Puhler, and J. Kalinowski. 2003. Identification and functional analysis of six mycolyltransferase genes of Corynebacterium glutamicum ATCC 13032: the genes cop1, cmt1, and cmt2 can replace each other in the synthesis of trehalose dicorynomycolate, a component of the mycolic acid layer of the cell envelope. Arch. Microbiol. 180:33-44.
14. Braun, V., and U. Sieglin. 1970. The covalent murein-lipoprotein structure of the Escherichia coli cell wall. The attachment site of the lipoprotein on the murein. Eur. J. Biochem. 13:336-346.
15. Cascales, E., A. Bernadac, M. Gavioli, J. C. Lazzaroni, and R. Lloubes. 2002. Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J. Bacteriol. 184:754-759. (Pubitemid 34150222)
16. Chami, M., N. Bayan, J. Dedieu, G. Leblon, E. Shechter, and T. Gulik- Krzywicki. 1995. Organization of the outer layers of the cell envelope of Corynebacterium glutamicum: a combined freeze-etch electron microscopy and biochemical study. Biol. Cell 83:219-229.
17. Chami, M., N. Bayan, J. L. Peyret, T. Gulik-Krzywicki, G. Leblon, and E. Shechter. 1997. The S-layer protein of Corynebacterium glutamicum is anchored to the cell wall by its C-terminal hydrophobic domain. Mol. Microbiol. 23:483-492.
18. Costa-Riu, N., E. Maier, A. Burkovski, R. Kramer, F. Lottspeich, and R. Benz. 2003. Identification of an anion-specific channel in the cell wall of the Gram-positive bacterium Corynebacterium glutamicum. Mol. Microbiol. 50:1295-1308.
19. Daffe, M., P. J. Brennan, and M. McNeil. 1990. Predominant structural features of the cell wall arabinogalactan of Mycobacterium tuberculosis as revealed through characterization of oligoglycosyl alditol fragments by gas chromatography/mass spectrometry and by 1H and 13C NMR analyses. J. Biol. Chem. 265:6734-6743.
20. Daffe, M., M. McNeil, and P. J. Brennan. 1993. Major structural features of the cell wall arabinogalactans of Mycobacterium, Rhodococcus, and Nocardia spp. Carbohydr. Res. 249:383-398.
21. Daffe, M. M. 1983. Structure of the lipid constituents of Mycobacterium leprae. Comparison with various species of mycobacteria. Acta Leprol. 1:205-209. (In French.)
22. Deatherage, B. L., J. C. Lara, T. Bergsbaken, S. L. Rassoulian Barrett, S. Lara, and B. T. Cookson. 2009. Biogenesis of bacterial membrane vesicles. Mol. Microbiol. 72:1395-1407.
23. Dubochet, J., M. Adrian, J. J. Chang, J. C. Homo, J. Lepault, A. W. McDowall, and P. Schultz. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129-228.
24. Dusch, N., A. Puhler, and J. Kalinowski. 1999. Expression of the Corynebacterium glutamicum panD gene encoding L-aspartate-alpha-decarboxylase leads to pantothenate overproduction in Escherichia coli. Appl. Environ. Microbiol. 65:1530-1539.
25. Faller, M., M. Niederweis, and G. E. Schulz. 2004. The structure of a mycobacterial outer-membrane channel. Science 303:1189-1192.
26. Ferrandez, Y., and G. Condemine. 2008. Novel mechanism of outer membrane targeting of proteins in Gram-negative bacteria. Mol. Microbiol. 69:1349-1357.
27. Hansmeier, N., A. Albersmeier, A. Tauch, T. Damberg, R. Ros, D. Anselmetti, A. Puhler, and J. Kalinowski. 2006. The surface (S)-layer gene cspB of Corynebacterium glutamicum is transcriptionally activated by a LuxR-type regulator and located on a 6 kb genomic island absent from the type strain ATCC 13032. Microbiology 152:923-935.
28. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. (Pubitemid 19125653)
29. Hoffmann, C., A. Leis, M. Niederweis, J. M. Plitzko, and H. Engelhardt. 2008. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc. Natl. Acad. Sci. U. S. A. 105:3963-3967.
30. Hunten, P., B. Schiffler, F. Lottspeich, and R. Benz. 2005. PorH, a new channel-forming protein present in the cell wall of Corynebacterium efficiens and Corynebacterium callunae. Microbiology 151:2429-2438. (Pubitemid 40984316)
31. Inouye, M., J. Shaw, and C. Shen. 1972. The assembly of a structural lipoprotein in the envelope of Escherichia coli. J. Biol. Chem. 247:8154-8159.
32. Joliff, G., L. Mathieu, V. Hahn, N. Bayan, F. Duchiron, M. Renaud, E. Schechter, and G. Leblon. 1992. Cloning and nucleotide sequence of the csp1 gene encoding PS1, one of the two major secreted proteins of Corynebacterium glutamicum: the deduced N-terminal region of PS1 is similar to the Mycobacterium antigen 85 complex. Mol. Microbiol. 6:2349-2362.
33. Kacem, R., C. De Sousa-D'Auria, M. Tropis, M. Chami, P. Gounon, G. Leblon, C. Houssin, and M. Daffe. 2004. Importance of mycoloyltransferases on the physiology of Corynebacterium glutamicum. Microbiology 150:73-84. (Pubitemid 38111472)
34. Kuehn, M. J., and N. C. Kesty. 2005. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 19:2645-2655. (Pubitemid 41627932)
35. Lee, E. Y., J. Y. Bang, G. W. Park, D. S. Choi, J. S. Kang, H. J. Kim, K. S. Park, J. O. Lee, Y. K. Kim, K. H. Kwon, K. P. Kim, and Y. S. Gho. 2007. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7:3143-3153.
36. Lichtinger, T., F. G. Riess, A. Burkovski, F. Engelbrecht, D. Hesse, H. D. Kratzin, R. Kramer, and R. Benz. 2001. The low-molecular-mass subunit of the cell wall channel of the Gram-positive Corynebacterium glutamicum. Immunological localization, cloning and sequencing of its gene porA. Eur. J. Biochem. 268:462-469.
37. Mashburn-Warren, L. M., and M. Whiteley. 2006. Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 61:839-846.
38. McNeil, M., M. Daffe, and P. J. Brennan. 1990. Evidence for the nature of the link between the arabinogalactan and peptidoglycan of mycobacterial cell walls. J. Biol. Chem. 265:18200-18206.
39. McNeil, M., M. Daffe, and P. J. Brennan. 1991. Location of the mycolyl ester substituents in the cell walls of mycobacteria. J. Biol. Chem. 266:13217-13223.
40. Minnikin, D. E. 1982. Lipids: complex lipids, their chemistry, biosynthesis and roles, p. 95-184. In C. R. J. L. Stanford (ed.), The biology of Mycobacteria, vol. 1. Academic press, London, United Kingdom.
41. Niederweis, M. 2003. Mycobacterial porins - new channel proteins in unique outer membranes. Mol. Microbiol. 49:1167-1177.
42. Niederweis, M., E. Maier, T. Lichtinger, R. Benz, and R. Kramer. 1995. Identification of channel-forming activity in the cell wall of Corynebacterium glutamicum. J. Bacteriol. 177:5716-5718. (Pubitemid 26028887)
43. Pajon, R., D. Yero, A. Lage, A. Llanes, and C. J. Borroto. 2006. Computational identification of beta-barrel outer-membrane proteins in Mycobacterium tuberculosis predicted proteomes as putative vaccine candidates. Tuberculosis (Edinb.) 86:290-302.
44. Peyret, J. L., N. Bayan, G. Joliff, T. Gulik-Krzywicki, L. Mathieu, E. Schechter, and G. Leblon. 1993. Characterization of the cspB gene encoding PS2, an ordered surface-layer protein in Corynebacterium glutamicum. Mol. Microbiol. 9:97-109.
45. Portevin, D., C. De Sousa-D'Auria, C. Houssin, C. Grimaldi, M. Chami, M. Daffe, and C. Guilhot. 2004. A polyketide synthase catalyzes the last condensation step of mycolic acid biosynthesis in mycobacteria and related organisms. Proc. Natl. Acad. Sci. U. S. A. 101:314-319.
46. Puech, V., N. Bayan, K. Salim, G. Leblon, and M. Daffe. 2000. Characterization of the in vivo acceptors of the mycoloyl residues transferred by the corynebacterial PS1 and the related mycobacterial antigens 85. Mol. Microbiol. 35:1026-1041.
47. Puech, V., M. Chami, A. Lemassu, M. A. Laneelle, B. Schiffler, P. Gounon, N. Bayan, R. Benz, and M. Daffe. 2001. Structure of the cell envelope of corynebacteria: importance of the non-covalently bound lipids in the formation of the cell wall permeability barrier and fracture plane. Microbiology 147:1365-1382. (Pubitemid 32454654)
48. Puech, V., C. Guilhot, E. Perez, M. Tropis, L. Y. Armitige, B. Gicquel, and M. Daffe. 2002. Evidence for a partial redundancy of the fibronectin-binding proteins for the transfer of mycoloyl residues onto the cell wall arabinogalactan termini of Mycobacterium tuberculosis. Mol. Microbiol. 44:1109-1122.
49. Richter, W., F. Hanel, and M. Hilliger. 1985. Freeze-fracture observations of Corynebacterium glutamicum: the occurrence of an outer membrane-like structure and the influence of temperature on the cytoplasmic membrane. J. Basic Microbiol. 25:527-536.
50. Ronning, D. R., T. Klabunde, G. S. Besra, V. D. Vissa, J. T. Belisle, and J. C. Sacchettini. 2000. Crystal structure of the secreted form of antigen 85C reveals potential targets for mycobacterial drugs and vaccines. Nat. Struct. Biol. 7:141-146.
51. Salim, K., V. Haedens, J. Content, G. Leblon, and K. Huygen. 1997. Heterologous expression of the Mycobacterium tuberculosis gene encoding antigen 85A in Corynebacterium glutamicum. Appl. Environ. Microbiol. 63:4392-4400.
52. Schafer, A., A. Tauch, W. Jager, J. Kalinowski, G. Thierbach, and A. Puhler. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73.
53. Seeman, P., and S. Roth. 1972. General anesthetics expand cell membranes at surgical concentrations. Biochim. Biophys. Acta 255:171-177.
54. Seidel, M., L. J. Alderwick, H. L. Birch, H. Sahm, L. Eggeling, and G. S. Besra. 2007. Identification of a novel arabinofuranosyltransferase AftB involved in a terminal step of cell wall arabinan biosynthesis in Corynebacterianeae, such as Corynebacterium glutamicum and Mycobacterium tuberculosis. J. Biol. Chem. 282:14729-14740.
55. Siroy, A., C. Mailaender, D. Harder, S. Koerber, F. Wolschendorf, O. Danilchanka, Y. Wang, C. Heinz, and M. Niederweis. 2008. Rv1698 of Mycobacterium tuberculosis represents a new class of channel-forming outer membrane proteins. J. Biol. Chem. 283:17827-17837.
56. Skovierova, H., G. Larrouy-Maumus, J. Zhang, D. Kaur, N. Barilone, J. Kordulakova, M. Gilleron, S. Guadagnini, M. Belanova, M. C. Prevost, B. Gicquel, G. Puzo, D. Chatterjee, P. J. Brennan, J. Nigou, and M. Jackson. 2009. AftD, a novel essential arabinofuranosyltransferase from mycobacteria. Glycobiology 19:1235-1247.
57. Song, H., R. Sandie, Y. Wang, M. A. Andrade-Navarro, and M. Niederweis. 2008. Identification of outer membrane proteins of Mycobacterium tuberculosis. Tuberculosis (Edinb.) 88:526-544.
58. Stephan, J., J. Bender, F. Wolschendorf, C. Hoffmann, E. Roth, C. Mailander, H. Engelhardt, and M. Niederweis. 2005. The growth rate of Mycobacterium smegmatis depends on sufficient porin-mediated influx of nutrients. Mol. Microbiol. 58:714-730.
59. Sweeley, C. C. 1963. Purification and partial characterization of sphingomyelin from human plasma. J. Lipid Res. 4:402-406.
60. Ton-That, H., L. A. Marraffini, and O. Schneewind. 2004. Protein sorting to the cell wall envelope of Gram-positive bacteria. Biochim. Biophys. Acta 1694:269-278.
61. Ton-That, H., and O. Schneewind. 2004. Assembly of pili in Gram-positive bacteria. Trends Microbiol. 12:228-234.
62. Trias, J., V. Jarlier, and R. Benz. 1992. Porins in the cell wall of mycobacteria. Science 258:1479-1481.
63. Webster, R. E. 1991. The tol gene products and the import of macromolecules into Escherichia coli. Mol. Microbiol. 5:1005-1011.
64. Wolschendorf, F., M. Mahfoud, and M. Niederweis. 2007. Porins are required for uptake of phosphates by Mycobacterium smegmatis. J. Bacteriol. 189:2435-2442.
65. Yoo, J., and Q. Cui. 2009. Curvature generation and pressure profile modulation in membrane by lysolipids: insights from coarse-grained simulations. Biophys. J. 97:2267-2276.
66. Ziegler, K., R. Benz, and G. E. Schulz. 2008. A putative alpha-helical porin from Corynebacterium glutamicum. J. Mol. Biol. 379:482-491.
67. Zuber, B., M. Chami, C. Houssin, J. Dubochet, G. Griffiths, and M. Daffe. 2008. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J. Bacteriol. 190:5672-5680.