User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

Characterization of O-acetylation of N-acetylglucosamine : a novel structural variation of bacterial peptidoglycan.

Primary tabs

download
  • Open access
  • PDF
  • 65.72 K
Bernard, Elvis [UCL] Rolain, Thomas [UCL] Courtin, Pascal Guillot, Alain Langella, Philippe Hols, Pascal [UCL] Chapot-Chartier, Marie-Pierre

Peptidoglycan (PG) N-acetyl muramic acid (MurNAc) O-acetylation is widely spread in gram-positive bacteria and is generally associated with resistance against lysozyme and endogenous autolysins. We report here the presence of O-acetylation on N-acetylglucosamine (GlcNAc) in Lactobacillus plantarum PG. This modification of glycan strands was never described in bacteria. Fine structural characterization of acetylated muropeptides released from L. plantarum PG demonstrated that both MurNAc and GlcNAc are O-acetylated in this species. These two PG post-modifications rely on two dedicated O-acetyltransferase encoding genes, named oatA and oatB, respectively. By analyzing the resistance to cell wall hydrolysis of mutant strains, we showed that GlcNAc O-acetylation inhibits N-acetylglucosaminidase Acm2, the major L. plantarum autolysin. In this bacterial species, inactivation of oatA, encoding MurNAc O-acetyltransferase, resulted in marked sensitivity to lysozyme. Moreover, MurNAc over-O-acetylation was shown to activate autolysis through the putative N-acetylmuramoyl-L-alanine amidase LytH enzyme. Our data indicate that in L. plantarum, two different O-acetyltransferases play original and antagonistic roles in the modulation of the activity of endogenous autolysins.

Document type Article de périodique (Journal article) – Article de recherche – Journal Article, Research Support, Non-U.S. Gov't
Access type Accès libre
Publication date 2011
Language Anglais
Journal information "The Journal of biological chemistry" - Vol. 286, no. 27, p. 23950-8 (2011)
Peer reviewed yes
issn 0021-9258
e-issn 1083-351X
Publication status Publié
Affiliations UCL - SST/ISV - Institut des sciences de la vie
UCL - SST/LIBST - Louvain Institute of Biomolecular Science and Technology
MESH Subject Acetylation ; Acetylglucosamine - genetics, metabolism ; Peptidoglycan - genetics, metabolism ; Acetyltransferases - genetics, metabolism ; Anti-Infective Agents - pharmacology ; Bacterial Proteins - genetics, metabolism ; Drug Resistance, Bacterial - drug effects, physiology ; Lactobacillus plantarum - genetics, metabolism ; Muramic Acids - metabolism ; Muramidase - pharmacology ; N-Acetylmuramoyl-L-alanine Amidase - genetics, metabolism
Links
  1. Bera Agnieszka, Herbert Silvia, Jakob Andreas, Vollmer Waldemar, Götz Friedrich, Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus : Lysozyme resistance of S. aureus, 10.1111/j.1365-2958.2004.04446.x
  2. Delcour Jean, Ferain Thierry, Deghorain Marie, Palumbo Emmanuelle, Hols Pascal, 10.1023/a:1002089722581
  3. Boneca Ivo G., Dussurget Olivier, Cabanes Didier, Nahori Marie-Anne, Sousa Sandra, Lecuit Marc, Psylinakis Emmanuel, Bouriotis Vassilis, Hugot Jean-Pierre, Giovannini Marco, Coyle Anthony, Bertin John, Namane Abdelkader, Rousselle Jean-Claude, Cayet Nadège, Prévost Marie-Christine, Balloy Viviane, Chignard Michel, Philpott Dana J., Cossart Pascale, Girardin Stephen E., A critical role for peptidoglycan N-deacetylation inListeriaevasion from the host innate immune system, 10.1073/pnas.0609672104
  4. Clarke Anthony J., Dupont Claude, O-Acetylated peptidoglycan: its occurrence, pathobiological significance, and biosynthesis, 10.1139/m92-014
  5. Crisostomo M. Ines, Vollmer Waldemar, Kharat Arun S., Inhulsen Silja, Gehre Florian, Buckenmaier Stephan, Tomasz Alexander, Attenuation of penicillin resistance in a peptidoglycan O-acetyl transferase mutant of Streptococcus pneumoniae, 10.1111/j.1365-2958.2006.05340.x
  6. Hebert L., Courtin P., Torelli R., Sanguinetti M., Chapot-Chartier M.-P., Auffray Y., Benachour A., Enterococcus faecalis Constitutes an Unusual Bacterial Model in Lysozyme Resistance, 10.1128/iai.00571-07
  7. Meyrand M., Boughammoura A., Courtin P., Mezange C., Guillot A., Chapot-Chartier M.-P., Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis, 10.1099/mic.0.2007/005835-0
  8. Moynihan Patrick J., Clarke Anthony J., O-Acetylation of Peptidoglycan in Gram-negative Bacteria : IDENTIFICATION AND CHARACTERIZATION OF PEPTIDOGLYCAN O-ACETYLTRANSFERASE IN NEISSERIA GONORRHOEAE, 10.1074/jbc.m110.107086
  9. Pfeffer J. M., Strating H., Weadge J. T., Clarke A. J., Peptidoglycan O Acetylation and Autolysin Profile of Enterococcus faecalis in the Viable but Nonculturable State, 10.1128/jb.188.3.902-908.2006
  10. Veiga Patrick, Bulbarela-Sampieri Carmen, Furlan Sylviane, Maisons Aurélie, Chapot-Chartier Marie-Pierre, Erkelenz Michael, Mervelet Peggy, Noirot Philippe, Frees Dorte, Kuipers Oscar P., Kok Jan, Gruss Alexandra, Buist Girbe, Kulakauskas Saulius, SpxB RegulatesO-Acetylation-dependent Resistance ofLactococcus lactisPeptidoglycan to Hydrolysis, 10.1074/jbc.m611308200
  11. Vollmer Waldemar, Tomasz Alexander, ThepgdAGene Encodes for a PeptidoglycanN-Acetylglucosamine Deacetylase inStreptococcus pneumoniae, 10.1074/jbc.m910189199
  12. Vollmer Waldemar, Structural variation in the glycan strands of bacterial peptidoglycan, 10.1111/j.1574-6976.2007.00088.x
  13. Vollmer Waldemar, Blanot Didier, De Pedro Miguel A., Peptidoglycan structure and architecture, 10.1111/j.1574-6976.2007.00094.x
  14. Blackburn Neil T., Clarke Anthony J., Characterization of Soluble and Membrane-Bound Family 3 Lytic Transglycosylases fromPseudomonas aeruginosa†, 10.1021/bi011833k
  15. Laaberki Maria-Halima, Pfeffer John, Clarke Anthony J., Dworkin Jonathan, O-Acetylation of Peptidoglycan Is Required for Proper Cell Separation and S-layer Anchoring inBacillus anthracis, 10.1074/jbc.m110.183236
  16. Emirian Aurélie, Fromentin Sophie, Eckert Catherine, Chau Françoise, Dubost Lionel, Delepierre Muriel, Gutmann Laurent, Arthur Michel, Mesnage Stéphane, Impact of peptidoglycanO-acetylation on autolytic activities of theEnterococcus faecalis N-acetylglucosaminidase AtlA andN-acetylmuramidase AtlB, 10.1016/j.febslet.2009.08.010
  17. Sambrook J. Russel D. W. (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
  18. Dower W. J., Miller J. F., Ragsdale C. W., High efficiency transformation of E.coli by high voltage electroporation, 10.1093/nar/16.13.6127
  19. Aukrust, Methods Mol. Biol., 47, 201 (1995)
  20. Lambert J. M., Bongers R. S., Kleerebezem M., Cre-lox-Based System for Multiple Gene Deletions and Selectable-Marker Removal in Lactobacillus plantarum, 10.1128/aem.01473-06
  21. Kuipers Oscar P, de Ruyter Pascalle G.G.A, Kleerebezem Michiel, de Vos Willem M, Quorum sensing-controlled gene expression in lactic acid bacteria, 10.1016/s0168-1656(98)00100-x
  22. Courtin P., Miranda G., Guillot A., Wessner F., Mezange C., Domakova E., Kulakauskas S., Chapot-Chartier M.-P., Peptidoglycan Structure Analysis of Lactococcus lactis Reveals the Presence of an L,D-Carboxypeptidase Involved in Peptidoglycan Maturation, 10.1128/jb.00285-06
  23. Cornett, J. Bacteriol., 135, 153 (1978)
  24. Schleifer, Bacteriol. Rev., 36, 407 (1972)
  25. Huard C., Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis, 10.1099/mic.0.25875-0
  26. Stöver Ben C, Müller Kai F, TreeGraph 2: Combining and visualizing evidence from different phylogenetic analyses, 10.1186/1471-2105-11-7
  27. Simossis V. A., Heringa J., PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information, 10.1093/nar/gki390
  28. Tusnady G. E., Simon I., The HMMTOP transmembrane topology prediction server, 10.1093/bioinformatics/17.9.849
  29. Wu Sitao, Zhang Yang, LOMETS: A local meta-threading-server for protein structure prediction, 10.1093/nar/gkm251
  30. Veiga P., Erkelenz M., Bernard E., Courtin P., Kulakauskas S., Chapot-Chartier M.-P., Identification of the Asparagine Synthase Responsible for D-Asp Amidation in the Lactococcus lactis Peptidoglycan Interpeptide Crossbridge, 10.1128/jb.00126-09
  31. Kleerebezem M., Boekhorst J., van Kranenburg R., Molenaar D., Kuipers O. P., Leer R., Tarchini R., Peters S. A., Sandbrink H. M., Fiers M. W. E. J., Stiekema W., Lankhorst R. M. K., Bron P. A., Hoffer S. M., Groot M. N. N., Kerkhoven R., de Vries M., Ursing B., de Vos W. M., Siezen R. J., Complete genome sequence of Lactobacillus plantarum WCFS1, 10.1073/pnas.0337704100
  32. Deghorain M., Goffin P., Fontaine L., Mainardi J.-L., Daniel R., Errington J., Hallet B., Hols P., Selectivity for D-Lactate Incorporation into the Peptidoglycan Precursors of Lactobacillus plantarum: Role of Aad, a VanX-Like D-Alanyl-D-Alanine Dipeptidase, 10.1128/jb.01829-06
  33. Ferain T, Hobbs J N, Richardson J, Bernard N, Garmyn D, Hols P, Allen N E, Delcour J, Knockout of the two ldh genes has a major impact on peptidoglycan precursor synthesis in Lactobacillus plantarum., 10.1128/jb.178.18.5431-5437.1996
  34. Goffin P., Deghorain M., Mainardi J.-L., Tytgat I., Champomier-Verges M.-C., Kleerebezem M., Hols P., Lactate Racemization as a Rescue Pathway for Supplying D-Lactate to the Cell Wall Biosynthesis Machinery in Lactobacillus plantarum, 10.1128/jb.187.19.6750-6761.2005
  35. Vollmer Waldemar, Joris Bernard, Charlier Paulette, Foster Simon, Bacterial peptidoglycan (murein) hydrolases, 10.1111/j.1574-6976.2007.00099.x
  36. Chapot-Chartier M. P. (2010) in Prokaryotic Cell Wall Compounds ( König H. Claus H. Varma A. eds) pp. 383–406, Springer Verlag Berlin, Heidelberg, Germany
  37. Sauvage Eric, Kerff Frédéric, Terrak Mohammed, Ayala Juan A., Charlier Paulette, The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis, 10.1111/j.1574-6976.2008.00105.x
Bibliographic reference Bernard, Elvis ; Rolain, Thomas ; Courtin, Pascal ; Guillot, Alain ; Langella, Philippe ; et. al. Characterization of O-acetylation of N-acetylglucosamine : a novel structural variation of bacterial peptidoglycan.. In: The Journal of biological chemistry, Vol. 286, no. 27, p. 23950-8 (2011)
Permanent URL http://hdl.handle.net/2078.1/110481