Previous Article | Next Article 
Journal of Bacteriology, July 1999, p. 3956-3966, Vol. 181, No. 13
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Analysis of Peptidoglycan Structure from Vegetative
Cells of Bacillus subtilis 168 and Role of PBP 5 in
Peptidoglycan Maturation
Abdelmadjid
Atrih,1
Gerold
Bacher,2
Günter
Allmaier,2
Michael P.
Williamson,1 and
Simon
J.
Foster1,*
Department of Molecular Biology and
Biotechnology, University of Sheffield, Sheffield, S10 2TN, United
Kingdom,1 and Institute for
Analytical Chemistry, University of Vienna, A-1090 Vienna,
Austria2
Received 1 March 1999/Accepted 26 April 1999
The composition and fine structure of the vegetative cell wall
peptidoglycan from Bacillus subtilis were determined by
analysis of its constituent muropeptides. The structures of 39 muropeptides, representing 97% of the total peptidoglycan, were
elucidated. About 99% analyzed muropeptides in B. subtilis
vegetative cell peptidoglycan have the free carboxylic group of
diaminopimelic acid amidated. Anhydromuropeptides and products missing
a glucosamine at the nonreducing terminus account for 0.4 and 1.5%,
respectively, of the total muropeptides. These two types of
muropeptides are suggested to end glycan strands. An unexpected feature
of B. subtilis muropeptides was the occurrence of a glycine
residue in position 5 of the peptide side chain on monomers or
oligomers, which account for 2.7% of the total muropeptides. This
amount is, however, dependent on the composition of the growth media.
Potential attachment sites for anionic polymers to peptidoglycan occur
on dominant muropeptides and account for 2.1% of the total. B. subtilis peptidoglycan is incompletely digested by lysozyme due
to de-N-acetylation of glucosamine, which occurs on 17.3% of
muropeptides. The cross-linking index of the polymer changes with the
growth phase. It is highest in late stationary phase, with a value of
33.2 or 44% per muramic acid residue, as determined by reverse-phase
high-pressure liquid chromatography or gel filtration, respectively.
Analysis of the muropeptide composition of a dacA (PBP 5)
mutant shows a dramatic decrease of muropeptides with tripeptide side
chains and an increase or appearance of muropeptides with pentapeptide
side chains in monomers or oligomers. The total muropeptides with
pentapeptide side chains accounts for almost 82% in the
dacA mutant. This major low-molecular-weight PBP
(DD-carboxypeptidase) is suggested to play a role in
peptidoglycan maturation.
*
Corresponding author. Mailing address: Department of
Molecular Biology and Biotechnology, University of Sheffield, Firth
Court, Western Bank, Sheffield, S10 2TN, United Kingdom. Phone: 44 114 222 4411. Fax: 44 114 272 8697. E-mail:
s.foster{at}sheffield.ac.uk.
Journal of Bacteriology, July 1999, p. 3956-3966, Vol. 181, No. 13
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Vasudevan, P., McElligott, J., Attkisson, C., Betteken, M., Popham, D. L.
(2009). Homologues of the Bacillus subtilis SpoVB Protein Are Involved in Cell Wall Metabolism. J. Bacteriol.
191: 6012-6019
[Abstract]
[Full Text]
-
Hayhurst, E. J., Kailas, L., Hobbs, J. K., Foster, S. J.
(2008). Cell wall peptidoglycan architecture in Bacillus subtilis. Proc. Natl. Acad. Sci. USA
105: 14603-14608
[Abstract]
[Full Text]
-
Dowd, M. M., Orsburn, B., Popham, D. L.
(2008). Cortex Peptidoglycan Lytic Activity in Germinating Bacillus anthracis Spores. J. Bacteriol.
190: 4541-4548
[Abstract]
[Full Text]
-
Absalon, C., Hamze, K., Blanot, D., Frehel, C., Carballido-Lopez, R., Holland, B. I., van Heijenoort, J., Seror, S. J.
(2008). The GTPase CpgA Is Implicated in the Deposition of the Peptidoglycan Sacculus in Bacillus subtilis. J. Bacteriol.
190: 3786-3790
[Abstract]
[Full Text]
-
Fukushima, T., Kitajima, T., Yamaguchi, H., Ouyang, Q., Furuhata, K., Yamamoto, H., Shida, T., Sekiguchi, J.
(2008). Identification and Characterization of Novel Cell Wall Hydrolase CwlT: A TWO-DOMAIN AUTOLYSIN EXHIBITING N-ACETYLMURAMIDASE AND DL-ENDOPEPTIDASE ACTIVITIES. J. Biol. Chem.
283: 11117-11125
[Abstract]
[Full Text]
-
Yuan, Z.-C., Liu, P., Saenkham, P., Kerr, K., Nester, E. W.
(2008). Transcriptome Profiling and Functional Analysis of Agrobacterium tumefaciens Reveals a General Conserved Response to Acidic Conditions (pH 5.5) and a Complex Acid-Mediated Signaling Involved in Agrobacterium-Plant Interactions. J. Bacteriol.
190: 494-507
[Abstract]
[Full Text]
-
Mahapatra, S., Crick, D. C., McNeil, M. R., Brennan, P. J.
(2008). Unique Structural Features of the Peptidoglycan of Mycobacterium leprae. J. Bacteriol.
190: 655-661
[Abstract]
[Full Text]
-
van Heijenoort, J.
(2007). Lipid Intermediates in the Biosynthesis of Bacterial Peptidoglycan. Microbiol. Mol. Biol. Rev.
71: 620-635
[Abstract]
[Full Text]
-
Stapleton, M. R., Horsburgh, M. J., Hayhurst, E. J., Wright, L., Jonsson, I.-M., Tarkowski, A., Kokai-Kun, J. F., Mond, J. J., Foster, S. J.
(2007). Characterization of IsaA and SceD, Two Putative Lytic Transglycosylases of Staphylococcus aureus. J. Bacteriol.
189: 7316-7325
[Abstract]
[Full Text]
-
Meyrand, M., Boughammoura, A., Courtin, P., Mezange, C., Guillot, A., Chapot-Chartier, M.-P.
(2007). Peptidoglycan N-acetylglucosamine deacetylation decreases autolysis in Lactococcus lactis. Microbiology
153: 3275-3285
[Abstract]
[Full Text]
-
Marraffini, L. A., Schneewind, O.
(2007). Sortase C-Mediated Anchoring of BasI to the Cell Wall Envelope of Bacillus anthracis. J. Bacteriol.
189: 6425-6436
[Abstract]
[Full Text]
-
Courtin, P., Miranda, G., Guillot, A., Wessner, F., Mezange, C., Domakova, E., Kulakauskas, S., Chapot-Chartier, M.-P.
(2006). Peptidoglycan Structure Analysis of Lactococcus lactis Reveals the Presence of an L,D-Carboxypeptidase Involved in Peptidoglycan Maturation.. J. Bacteriol.
188: 5293-5298
[Abstract]
[Full Text]
-
Masumoto, J., Yang, K., Varambally, S., Hasegawa, M., Tomlins, S. A., Qiu, S., Fujimoto, Y., Kawasaki, A., Foster, S. J., Horie, Y., Mak, T. W., Nunez, G., Chinnaiyan, A. M., Fukase, K., Inohara, N.
(2006). Nod1 acts as an intracellular receptor to stimulate chemokine production and neutrophil recruitment in vivo. JEM
203: 203-213
[Abstract]
[Full Text]
-
Scheffers, D.-J., Pinho, M. G.
(2005). Bacterial Cell Wall Synthesis: New Insights from Localization Studies. Microbiol. Mol. Biol. Rev.
69: 585-607
[Abstract]
[Full Text]
-
Psylinakis, E., Boneca, I. G., Mavromatis, K., Deli, A., Hayhurst, E., Foster, S. J., Varum, K. M., Bouriotis, V.
(2005). Peptidoglycan N-Acetylglucosamine Deacetylases from Bacillus cereus, Highly Conserved Proteins in Bacillus anthracis. J. Biol. Chem.
280: 30856-30863
[Abstract]
[Full Text]
-
Dhalluin, A., Bourgeois, I., Pestel-Caron, M., Camiade, E., Raux, G., Courtin, P., Chapot-Chartier, M.-P., Pons, J.-L.
(2005). Acd, a peptidoglycan hydrolase of Clostridium difficile with N-acetylglucosaminidase activity. Microbiology
151: 2343-2351
[Abstract]
[Full Text]
-
Mengin-Lecreulx, D., Lemaitre, B.
(2005). Structure and metabolism of peptidoglycan and molecular requirements allowing its detection by the Drosophila innate immune system. Innate Immunity
11: 105-111
[Abstract]
-
Huard, C., Miranda, G., Redko, Y., Wessner, F., Foster, S. J., Chapot-Chartier, M.-P.
(2004). Analysis of the Peptidoglycan Hydrolase Complement of Lactococcus lactis: Identification of a Third N-Acetylglucosaminidase, AcmC. Appl. Environ. Microbiol.
70: 3493-3499
[Abstract]
[Full Text]
-
Gilmore, M. E., Bandyopadhyay, D., Dean, A. M., Linnstaedt, S. D., Popham, D. L.
(2004). Production of Muramic {delta}-Lactam in Bacillus subtilis Spore Peptidoglycan. J. Bacteriol.
186: 80-89
[Abstract]
[Full Text]
-
Neuhaus, F. C., Baddiley, J.
(2003). A Continuum of Anionic Charge: Structures and Functions of D-Alanyl-Teichoic Acids in Gram-Positive Bacteria. Microbiol. Mol. Biol. Rev.
67: 686-723
[Abstract]
[Full Text]
-
Girardin, S. E., Travassos, L. H., Herve, M., Blanot, D., Boneca, I. G., Philpott, D. J., Sansonetti, P. J., Mengin-Lecreulx, D.
(2003). Peptidoglycan Molecular Requirements Allowing Detection by Nod1 and Nod2. J. Biol. Chem.
278: 41702-41708
[Abstract]
[Full Text]
-
Wei, Y., Havasy, T., McPherson, D. C., Popham, D. L.
(2003). Rod Shape Determination by the Bacillus subtilis Class B Penicillin-Binding Proteins Encoded by pbpA and pbpH. J. Bacteriol.
185: 4717-4726
[Abstract]
[Full Text]
-
Horsburgh, G. J., Atrih, A., Foster, S. J.
(2003). Characterization of LytH, a Differentiation-Associated Peptidoglycan Hydrolase of Bacillus subtilis Involved in Endospore Cortex Maturation. J. Bacteriol.
185: 3813-3820
[Abstract]
[Full Text]
-
Huard, C., Miranda, G., Wessner, F., Bolotin, A., Hansen, J., Foster, S. J., Chapot-Chartier, M.-P.
(2003). Characterization of AcmB, an N-acetylglucosaminidase autolysin from Lactococcus lactis. Microbiology
149: 695-705
[Abstract]
[Full Text]
-
McPherson, D. C., Popham, D. L.
(2003). Peptidoglycan Synthesis in the Absence of Class A Penicillin-Binding Proteins in Bacillus subtilis. J. Bacteriol.
185: 1423-1431
[Abstract]
[Full Text]
-
Inohara, N., Ogura, Y., Fontalba, A., Gutierrez, O., Pons, F., Crespo, J., Fukase, K., Inamura, S., Kusumoto, S., Hashimoto, M., Foster, S. J., Moran, A. P., Fernandez-Luna, J. L., Nunez, G.
(2003). Host Recognition of Bacterial Muramyl Dipeptide Mediated through NOD2. IMPLICATIONS FOR CROHN'S DISEASE. J. Biol. Chem.
278: 5509-5512
[Abstract]
[Full Text]
-
Vollmer, W., Tomasz, A.
(2002). Peptidoglycan N-Acetylglucosamine Deacetylase, a Putative Virulence Factor in Streptococcus pneumoniae. Infect. Immun.
70: 7176-7178
[Abstract]
[Full Text]
-
Catalano, F. A., Meador-Parton, J., Popham, D. L., Driks, A.
(2001). Amino Acids in the Bacillus subtilis Morphogenetic Protein SpoIVA with Roles in Spore Coat and Cortex Formation. J. Bacteriol.
183: 1645-1654
[Abstract]
[Full Text]
-
Grohs, P., Gutmann, L., Legrand, R., Schoot, B., Mainardi, J. L.
(2000). Vancomycin Resistance Is Associated with Serine-Containing Peptidoglycan in Enterococcus gallinarum. J. Bacteriol.
182: 6228-6232
[Abstract]
[Full Text]
-
Meador-Parton, J., Popham, D. L.
(2000). Structural Analysis of Bacillus subtilis Spore Peptidoglycan during Sporulation. J. Bacteriol.
182: 4491-4499
[Abstract]
[Full Text]
-
Sun, Y.-L., Sharp, M. D., Pogliano, K.
(2000). A Dispensable Role for Forespore-Specific Gene Expression in Engulfment of the Forespore during Sporulation of Bacillus subtilis. J. Bacteriol.
182: 2919-2927
[Abstract]
[Full Text]
-
Smith, T. J., Blackman, S. A., Foster, S. J.
(2000). Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology
146: 249-262
[Full Text]
-
Vollmer, W., Tomasz, A.
(2000). The pgdA Gene Encodes for a Peptidoglycan N-Acetylglucosamine Deacetylase in Streptococcus pneumoniae. J. Biol. Chem.
275: 20496-20501
[Abstract]
[Full Text]