Peptidoglycan plasticity in bacteria: Stress-induced peptidoglycan editing by noncanonical D-amino acids

Microbial Drug Resistance

Volumn 18, Issue 3, 2012, Pages 306-313

  Horcajo, Pilar ^a   De Pedro, Miguel A ^a   Cava, Felipe ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DEXTRO AMINO ACID; GAMMA GLUTAMYLTRANSFERASE; LIGASE; METHIONINE; PEPTIDOGLYCAN;

BACTERIAL CELL WALL; CARBOHYDRATE ANALYSIS; CELL CYCLE REGULATION; CELL METABOLISM; CELL STRESS; ENVIRONMENTAL STRESS; HUMAN; LACTOBACILLUS PLANTARUM; NONHUMAN; PHYLUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROCESSING; REVIEW; VIBRIO CHOLERAE;

AMINO ACIDS; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; CELL WALL; PEPTIDOGLYCAN; PEPTIDYL TRANSFERASES; STEREOISOMERISM; STRESS, PHYSIOLOGICAL;

BACTERIA (MICROORGANISMS);

EID: 84862015701     PISSN: 10766294     EISSN: 19318448     Source Type: Journal    
DOI: 10.1089/mdr.2012.0009     Document Type: Review

References (62)

1. Aaron, M., G. Charbon, H. Lam, H. Schwarz, W. Vollmer, and C. Jacobs-Wagner. 2007. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol. Microbiol. 64:938-952.
2. Barreteau, H., A. Kovac, A. Boniface, M. Sova, S. Gobec, and D. Blanot. 2008. Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32:168-207.
3. Bellais, S., M. Arthur, L. Dubost, J.E. Hugonnet, L. Gutmann, J. van Heijenoort, R. Legrand, J.P. Brouard, L. Rice, and J.L. Mainardi. 2006. Aslfm, the D-aspartate ligase responsible for the addition of D-aspartic acid onto the peptidoglycan precursor of Enterococcus faecium. J. Biol. Chem. 281:11586-11594.
4. Bopp, M. 1965. [Inhibition of Agrobacterium tumefaciens by D-amino acids]. Z Naturforsch B 20:899-905.
5. Brown, P.J.B., M.A. de Pedro, D.T. Kysela, C. Van der Henst, J. Kim, X. De Bolle, C. Fuqua, and Y.V. Brun. 2012. Polar growth in the Alphaproteobacterial Order Rhizobiales. Proc. Natl. Acad. Sci. U. S. A. 109:1697-1701.
6. Caparros, M., V. Aran, and M.A. de Pedro. 1992. Incorporation of S-[3H]methyl-D-cysteine into the peptidoglycan of ether-treated cells of Escherichia coli. FEMS Microbiol. Lett. 72:139-146.
7. Caparros, M., A.G. Pisabarro, and M.A. de Pedro. 1992. Effect of D-amino acids on structure and synthesis of peptidoglycan in Escherichia coli. J. Bacteriol. 174:5549-5559.
8. Caparros, M., J.C. Quintela, and M.A. de Pedro. 1994. Variability of peptidoglycan surface density in Escherichia coli. FEMS Microbiol. Lett. 121:71-76.
9. Caparros, M., J.L. Torrecuadrada, and M.A. de Pedro. 1991. Effect of D-amino acids on Escherichia coli strains with impaired penicillin-binding proteins. Res. Microbiol. 142:345-350.
10. Cava, F., M.A. de Pedro, H. Lam, B.M. Davis, and M.K. Waldor. 2011. Distinct pathways for modification of the bacterial cell wall by non-canonical D-amino acids. EMBO J. 30:3442-3453.
11. Chaput, C., A. Labigne, and I.G. Boneca. 2007. Characterization of Helicobacter pylori lytic transglycosylases Slt and MltD. J. Bacteriol. 189:422-429.
12. Costa, K., G. Bacher, G. Allmaier, M.G. Dominguez- Bello, L. Engstrand, P. Falk, M.A. de Pedro, and F. Garciadel Portillo. 1999. The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J. Bacteriol. 181:3710-3715.
13. Davis, K.M., and J.N. Weiser. 2011. Modifications to the peptidoglycan backbone help bacteria to establish infection. Infect. Immun. 79:562-570.
14. De Jonge, B.L., D. Gage, and N. Xu. 2002. The carboxyl terminus of peptidoglycan stem peptides is a determinant for methicillin resistance in Staphylococcus aureus. Antimicrob. Agents Chemother. 46:3151-3155.
15. de Lencastre, H., D. Oliveira, and A. Tomasz. 2007. Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power. Curr. Opin. Microbiol. 10:428-435.
16. de Pedro, M.A., W.D. Donachie, J.V. Holtje, and H. Schwarz. 2001. Constitutive septal murein synthesis in Escherichia coli with impaired activity of the morphogenetic proteins RodA and penicillin-binding protein 2. J. Bacteriol. 183:4115-4126.
17. de Pedro, M.A., J.C. Quintela, J.V. Holtje, and H. Schwarz. 1997. Murein segregation in Escherichia coli. J. Bacteriol. 179:2823-2834.
18. de Pedro, M.A., K.D. Young, J.V. Holtje, and H. Schwarz. 2003. Branching of Escherichia coli cells arises from multiple sites of inert peptidoglycan. J. Bacteriol. 185:1147-1152.
19. Fang, F.C., S.J. Libby, N.A. Buchmeier, P.C. Loewen, J. Switala, J. Harwood, and D.G. Guiney. 1992. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. U. S. A. 89:11978-11982.
20. Fox, S.W., M. Fling, and N. Bollenback. 1944. Inhibition of bacterial growth by d-leucine. J. Biol. Chem. 155:465-468.
21. Ghuysen, J.M. 1961. [Data on the structure of disaccharide-peptide complexes liberated from the wall of Micrococcus lysodeikticus by the action of beta(1-4)N-acetylhexosaminidases]. Biochim Biophys Acta 47:561-568.
22. Grohs, P., L. Gutmann, R. Legrand, B. Schoot, and J.L. Mainardi. 2000. Vancomycin resistance is associated with serine-containing peptidoglycan in Enterococcus gallinarum. J. Bacteriol. 182:6228-6232.
23. Grula, E.A. 1960. Cell division in a species of Erwinia. I. Inhibition of division by D-amino acids. J. Bacteriol. 80:375-385.
24. Hammes, W.P. 1978. The LD-carboxypeptidase activity in Gaffkya homari. The target of the action of D-amino acids or glycine on the formation of wall-bound peptidoglycan. Eur. J. Biochem. 91:501-507.
25. Hancock, R. 1960. The amino acid composition of the protein and cell wall of Staphylococcus aureus. Biochim. Biophys. Acta. 37:42-46.
26. Hengge-Aronis, R. 2002. Recent insights into the general stress response regulatory network in Escherichia coli. J. Mol. Microbiol. Biotechnol. 4:341-346.
27. Holtje, J.V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
28. Izaki, K., M. Matsuhashi, and J.L. Strominger. 1968. Biosynthesis of the peptidoglycan of bacterial cell walls. 8. Peptidoglycan transpeptidase and D-alanine carboxypeptidase: penicillin-sensitive enzymatic reaction in strains of Escherichia coli. J. Biol. Chem. 243:3180-3192.
29. Janssen, P.H., L.E. Parker, and H.W. Morgan. 1991. Filament formation in Thermus species in the presence of some D-amino acids or glycine. Antonie Van Leeuwenhoek 59:147-154.
30. Kobayashi, Y., M. Fling, and S.W. Fox. 1948. Antipodal specificity in the inhibition of growth of Escherichia coli by amino acids. J. Biol. Chem. 174:391-398.
31. Kolodkin-Gal, I., D. Romero, S. Cao, J. Clardy, R. Kolter, and R. Losick. 2010. D-amino acids trigger biofilm disassembly. Science 328:627-629.
32. Lam, H., D.C. Oh, F. Cava, C.N. Takacs, J. Clardy, M.A. de Pedro, and M.K. Waldor. 2009. D-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552-1555.
33. Lark, C., D. Bradley, and K.G. Lark. 1963. Further studies on the incorporation of D-methionine into the bacterial cell wall; its incorporation into the R-layer and the structural consequences. Biochim. Biophys. Acta. 78:278-288.
34. Lark, C., and K.G. Lark. 1959. The effects of D-amino acids on Alcaligenes fecalis. Can. J. Microbiol. 5:369-379.
35. Lark, C., and K.G. Lark. 1961. Studies on the mechanism by which D-amino acids block cell wall synthesis. Biochim. Biophys. Acta. 49:308-322.
36. Lupoli, T.J., H. Tsukamoto, E.H. Doud, T.S. Wang, S. Walker, and D. Kahne. 2011. Transpeptidase-mediated incorporation of D-amino acids into bacterial peptidoglycan. J. Am. Chem. Soc. 133:10748-10751.
37. Ma, L., J. Chen, R. Liu, X.H. Zhang, and Y.A. Jiang. 2009. Mutation of rpoS gene decreased resistance to environmental stresses, synthesis of extracellular products and virulence of Vibrio anguillarum. FEMS Microbiol. Ecol. 70:130-136.
38. Magnet, S., A. Arbeloa, J.L. Mainardi, J.E. Hugonnet, M. Fourgeaud, L. Dubost, A. Marie, V. Delfosse, C. Mayer, L.B. Rice, and M. Arthur. 2007. Specificity of L,D-transpeptidases from gram-positive bacteria producing different peptidoglycan chemotypes. J. Biol. Chem. 282:13151-13159.
39. Magnet, S., S. Bellais, L. Dubost, M. Fourgeaud, J.L. Mainardi, S. Petit-Frere, A. Marie, D. Mengin-Lecreulx, M. Arthur, and L. Gutmann. 2007. Identification of the L,D-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J. Bacteriol. 189:3927-3931.
40. Magnet, S., L. Dubost, A. Marie, M. Arthur, and L. Gutmann. 2008. Identification of the L,D-transpeptidases for peptidoglycan cross-linking in Escherichia coli. J. Bacteriol. 190:4782-4785.
41. Mengin-Lecreulx, D., and B. Lemaitre. 2005. Structure and metabolism of peptidoglycan and molecular requirements allowing its detection by the Drosophila innate immune system. J. Endotoxin Res. 11:105-111.
42. Nanninga, N. 1998. Morphogenesis of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:110-129.
43. Nystrom, T. 2004. Stationary-phase physiology. Annu. Rev. Microbiol. 58:161-181.
44. Ottolenghi, A.C., M. Caparros, and M.A. de Pedro. 1993. Peptidoglycan tripeptide content and cross-linking are altered in Enterobacter cloacae induced to produce AmpC beta-lactamase by glycine and D-amino acids. J. Bacteriol. 175:1537-1542.
45. Ouyang, Z., R.K. Deka, and M.V. Norgard. 2011. BosR (BB0647) controls the RpoN-RpoS regulatory pathway and virulence expression in Borrelia burgdorferi by a novel DNA-binding mechanism. PLoS Pathog. 7:e1001272.
46. Park, J.T., and J.L. Strominger. 1957. Mode of action of penicillin. Science 125:99-101.
47. Park, J.T., and T. Uehara. 2008. How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol. Mol. Biol. Rev. 72:211-227, table of contents.
48. Reynolds, P.E., and P. Courvalin. 2005. Vancomycin resistance in enterococci due to synthesis of precursors terminating in D-alanyl-D-serine. Antimicrob. Agents Chemother. 49:21-25.
49. Setlow, P. 2003. Spore germination. Curr. Opin. Microbiol. 6:550-556.
50. Sieradzki, K., and A. Tomasz. 1996. A highly vancomycin-resistant laboratory mutant of Staphylococcus aureus. FEMS Microbiol. Lett. 142:161-166.
51. Strijdom, B.W., and O.N. Allen. 1966. Medium supplementation with L- and D-amino acids relative to growth and efficiency of Rhizobium meliloti. Can. J. Microbiol. 12:275-283.
52. Teeri, A.E. 1954. Effect of D-amino acids on growth of Lactobacilli. J. Bacteriol. 67:686-688.
53. Tsuruoka, T., A. Tamura, A. Miyata, T. Takei, S. Inouye, and M. Matsuhashi. 1985. Second lytic target of beta-lactam compounds that have a terminal D-amino acid residue. Eur. J. Biochem. 151:209-216.
54. Tsuruoka, T., A. Tamura, A. Miyata, T. Takei, K. Iwamatsu, S. Inouye, and M. Matsuhashi. 1984. Penicillin-insensitive incorporation of D-amino acids into cell wall peptidoglycan influences the amount of bound lipoprotein in Escherichia coli. J. Bacteriol. 160:889-894.
55. Tuomanen, E., and A. Tomasz. 1984. Protection by D-amino acids against growth inhibition and lysis caused by betalactam antibiotics. Antimicrob. Agents Chemother. 26: 414-416.
56. Tuttle, A.L., and H. Gest. 1960. Induction of morphological aberrations in Rhodospirillum rubrum by D-amino acids. J. Bacteriol. 79:213-216.
57. Veiga, P., S. Piquet, A. Maisons, S. Furlan, P. Courtin, M.P. Chapot-Chartier, and S. Kulakauskas. 2006. Identification of an essential gene responsible for D-Asp incorporation in the Lactococcus lactis peptidoglycan crossbridge. Mol. Microbiol. 62:1713-1724.
58. Vollmer, W., D. Blanot, and M.A. de Pedro. 2008. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32:149-167.
59. Vollmer, W., B. Joris, P. Charlier, and S. Foster. 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259-286.
60. Wecke, J., T. Kersten, and P. Giesbrecht. 1992. The modulation of the bacteriolytic effect of beta-lactam antibiotics by non-antibiotics. APMIS Suppl 30:32-39.
61. Yaw, K.E., and J.C. Kakavas. 1952. Studies on the effects of D-amino acids on Brucella abortus. J. Bacteriol. 63:263-268.
62. Young, K.D. 2006. The selective value of bacterial shape. Microbiol. Mol. Biol. Rev. 70:660-703.