1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 2: Cell Architecture and Growth

Peptidoglycan: Structure, Synthesis, and Regulation

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    342.72 Kb
  • PDF
    33.07 MB
  • HTML
    302.02 Kb
  • Authors: Shambhavi Garde1,2, Pavan Kumar Chodisetti3,4, and Manjula Reddy5
  • Editor: James M. Slauch6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500007; 2: These authors contributed equally.; 3: CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500007; 4: These authors contributed equally.; 5: CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500007; 6: The School of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL
  • Received 21 September 2020 Accepted 21 December 2020 Published 20 January 2021
  • Address correspondence to Manjula Reddy, [email protected]
image of Peptidoglycan: Structure, Synthesis, and Regulation
    Preview this reference work article:
    Preview Magnify
    Zoom in
    Zoomout

    Peptidoglycan: Structure, Synthesis, and Regulation, Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/9/2/ESP-0010-2020-1.gif /docserver/preview/fulltext/ecosalplus/9/2/ESP-0010-2020-2.gif

  • Abstract:

    Peptidoglycan is a defining feature of the bacterial cell wall. Initially identified as a target of the revolutionary beta-lactam antibiotics, peptidoglycan has become a subject of much interest for its biology, its potential for the discovery of novel antibiotic targets, and its role in infection. Peptidoglycan is a large polymer that forms a mesh-like scaffold around the bacterial cytoplasmic membrane. Peptidoglycan synthesis is vital at several stages of the bacterial cell cycle: for expansion of the scaffold during cell elongation and for formation of a septum during cell division. It is a complex multifactorial process that includes formation of monomeric precursors in the cytoplasm, their transport to the periplasm, and polymerization to form a functional peptidoglycan sacculus. These processes require spatio-temporal regulation for successful assembly of a robust sacculus to protect the cell from turgor and determine cell shape. A century of research has uncovered the fundamentals of peptidoglycan biology, and recent studies employing advanced technologies have shed new light on the molecular interactions that govern peptidoglycan synthesis. Here, we describe the peptidoglycan structure, synthesis, and regulation in rod-shaped bacteria, particularly , with a few examples from and other diverse organisms. We focus on the pathway of peptidoglycan sacculus elongation, with special emphasis on discoveries of the past decade that have shaped our understanding of peptidoglycan biology.

  • Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020

References

1. Fleming A. 1922. On a remarkable bacteriolytic element found in tissues and secretions. Proc R Soc Lond 93:306–317.
2. Fleming A. 1929. On the antibacterial action of cultures of a Penicillium, with special reference to their use in the isolation of B. influenzae. Br J Exp Pathol 10:226–236.
3. Cooper PD. 1955. The site of action of penicillin: some properties of the penicillin-binding component of Staphylococcus aureus. J Gen Microbiol 12:100–106 http://dx.doi.org/10.1099/00221287-12-1-100. [PubMed]
4. Park JT, Strominger JL. 1957. Mode of action of penicillin. Science 125:99–101 http://dx.doi.org/10.1126/science.125.3238.99. [PubMed]
5. Lederberg J. 1957. Mechanism of action of penicillin. J Bacteriol 73:144–144 http://dx.doi.org/10.1128/JB.73.1.144-144.1957. [PubMed]
6. Tipper DJ, Strominger JL. 1965. Mechanism of action of penicillins: a proposal based on their structural similarity to acyl- d-alanyl- d-alanine. Proc Natl Acad Sci USA 54:1133–1141 http://dx.doi.org/10.1073/pnas.54.4.1133. [PubMed]
7. Tomasz A. 1979. The mechanism of the irreversible antimicrobial effects of penicillins: how the beta-lactam antibiotics kill and lyse bacteria. Annu Rev Microbiol 33:113–137 http://dx.doi.org/10.1146/annurev.mi.33.100179.000553. [PubMed]
8. Weidel W, Frank H, Martin HH. 1960. The rigid layer of the cell wall of Escherichia coli strain B. J Gen Microbiol 22:158–166 http://dx.doi.org/10.1099/00221287-22-1-158. [PubMed]
9. Salton MRJ, Pavlik JG. 1960. Studies of the bacterial cell wall. VI. Wall composition and sensitivity to lysozyme. Biochim Biophys Acta 39:398–407 http://dx.doi.org/10.1016/0006-3002(60)90191-8.
10. Ghuysen JM. 1968. Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol Rev 32:425–464 http://dx.doi.org/10.1128/BR.32.4_Pt_2.425-464.1968. [PubMed]
11. Weidel W, Pelzer H. 1964. Bag-shaped macromolecules: a new outlook on bacterial cell walls, p 193–232. In Nord FF (ed), Advances in Enzymology and Related Areas of Molecular Biology. John Wiley & Sons, Hoboken, NJ. [PubMed]
12. Höltje J-V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203 http://dx.doi.org/10.1128/MMBR.62.1.181-203.1998. [PubMed]
13. Vollmer W, Blanot D, de Pedro MA. 2008. Peptidoglycan structure and architecture. FEMS Microbiol Rev 32:149–167 http://dx.doi.org/10.1111/j.1574-6976.2007.00094.x. [PubMed]
14. Work E. 1961. The mucopeptides of bacterial cell walls. A review. J Gen Microbiol 25:169–189 http://dx.doi.org/10.1099/00221287-25-2-167. [PubMed]
15. Schleifer KH, Kandler O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477 http://dx.doi.org/10.1128/BR.36.4.407-477.1972. [PubMed]
16. Silhavy TJ, Kahne D, Walker S. 2010. The bacterial cell envelope. Cold Spring Harb Perspect Biol 2:a000414 http://dx.doi.org/10.1101/cshperspect.a000414. [PubMed]
17. Wheeler R, Chevalier G, Eberl G, Gomperts Boneca I. 2014. The biology of bacterial peptidoglycans and their impact on host immunity and physiology. Cell Microbiol 16:1014–1023 http://dx.doi.org/10.1111/cmi.12304. [PubMed]
18. Wolf AJ, Underhill DM. 2018. Peptidoglycan recognition by the innate immune system. Nat Rev Immunol 18:243–254 http://dx.doi.org/10.1038/nri.2017.136. [PubMed]
19. Zheng D, Liwinski T, Elinav E. 2020. Interaction between microbiota and immunity in health and disease. Cell Res 30:492–506 http://dx.doi.org/10.1038/s41422-020-0332-7. [PubMed]
20. Gonzalez-Santana A, Diaz Heijtz R. 2020. Bacterial peptidoglycans from microbiota in neurodevelopment and behavior. Trends Mol Med 26:729–743 http://dx.doi.org/10.1016/j.molmed.2020.05.003. [PubMed]
21. Vollmer W, Bertsche U. 2008. Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778:1714–1734 http://dx.doi.org/10.1016/j.bbamem.2007.06.007. [PubMed]
22. Turner RD, Vollmer W, Foster SJ. 2014. Different walls for rods and balls: the diversity of peptidoglycan. Mol Microbiol 91:862–874 http://dx.doi.org/10.1111/mmi.12513. [PubMed]
23. Typas A, Banzhaf M, Gross CA, Vollmer W. 2011. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 10:123–136 http://dx.doi.org/10.1038/nrmicro2677. [PubMed]
24. Zhao H, Patel V, Helmann JD, Dörr T. 2017. Don’t let sleeping dogmas lie: new views of peptidoglycan synthesis and its regulation. Mol Microbiol 106:847–860 http://dx.doi.org/10.1111/mmi.13853. [PubMed]
25. Egan AJF, Errington J, Vollmer W. 2020. Regulation of peptidoglycan synthesis and remodelling. Nat Rev Microbiol 18:446–460 http://dx.doi.org/10.1038/s41579-020-0366-3. [PubMed]
26. Nanninga N. 1998. Morphogenesis of Escherichia coli. Microbiol Mol Biol Rev 62:110–129 http://dx.doi.org/10.1128/MMBR.62.1.110-129.1998. [PubMed]
27. Park JT. 1987. Murein synthesis, p 663–671. In Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella typhimurium. American Society for Microbiology, Washington, DC.
28. Verwer RW, Nanninga N, Keck W, Schwarz U. 1978. Arrangement of glycan chains in the sacculus of Escherichia coli. J Bacteriol 136:723–729 http://dx.doi.org/10.1128/JB.136.2.723-729.1978. [PubMed]
29. Gan L, Chen S, Jensen GJ. 2008. Molecular organization of Gram-negative peptidoglycan. Proc Natl Acad Sci USA 105:18953–18957 http://dx.doi.org/10.1073/pnas.0808035105. [PubMed]
30. Labischinski H, Barnickel G, Naumann D, Keller P. 1985. Conformational and topological aspects of the three-dimensional architecture of bacterial peptidoglycan. Ann Inst Pasteur Microbiol 1985 136A:45–50 http://dx.doi.org/10.1016/S0769-2609(85)80020-X.
31. Glauner B, Höltje J-V, Schwarz U. 1988. The composition of the murein of Escherichia coli. J Biol Chem 263:10088–10095.
32. Koch AL. 1984. Shrinkage of growing Escherichia coli cells by osmotic challenge. J Bacteriol 159:919–924 http://dx.doi.org/10.1128/JB.159.3.919-924.1984. [PubMed]
33. Baldwin WW, Sheu MJ, Bankston PW, Woldringh CL. 1988. Changes in buoyant density and cell size of Escherichia coli in response to osmotic shocks. J Bacteriol 170:452–455 http://dx.doi.org/10.1128/JB.170.1.452-455.1988. [PubMed]
34. Yao X, Jericho M, Pink D, Beveridge T. 1999. Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy. J Bacteriol 181:6865–6875 http://dx.doi.org/10.1128/JB.181.22.6865-6875.1999. [PubMed]
35. Rojas E, Theriot JA, Huang KC. 2014. Response of Escherichia coli growth rate to osmotic shock. Proc Natl Acad Sci USA 111:7807–7812 http://dx.doi.org/10.1073/pnas.1402591111. [PubMed]
36. Braun V, Gnirke H, Henning U, Rehn K. 1973. Model for the structure of the shape-maintaining layer of the Escherichia coli cell envelope. J Bacteriol 114:1264–1270 http://dx.doi.org/10.1128/JB.114.3.1264-1270.1973. [PubMed]
37. Wientjes FB, Woldringh CL, Nanninga N. 1991. Amount of peptidoglycan in cell walls of Gram-negative bacteria. J Bacteriol 173:7684–7691 http://dx.doi.org/10.1128/JB.173.23.7684-7691.1991. [PubMed]
38. de Pedro MA, Quintela JC, Höltje JV, Schwarz H. 1997. Murein segregation in Escherichia coli. J Bacteriol 179:2823–2834 http://dx.doi.org/10.1128/JB.179.9.2823-2834.1997. [PubMed]
39. Matias VRF, Al-Amoudi A, Dubochet J, Beveridge TJ. 2003. Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185:6112–6118 http://dx.doi.org/10.1128/JB.185.20.6112-6118.2003. [PubMed]
40. Vollmer W, Höltje J-V. 2004. The architecture of the murein (peptidoglycan) in Gram-negative bacteria: vertical scaffold or horizontal layer(s)? J Bacteriol 186:5978–5987 http://dx.doi.org/10.1128/JB.186.18.5978-5987.2004. [PubMed]
41. Leduc M, Fréhel C, Siegel E, Van Heijenoort J. 1989. Multilayered distribution of peptidoglycan in the periplasmic space of Escherichia coli. J Gen Microbiol 135:1243–1254. [PubMed]
42. Labischinski H, Goodell EW, Goodell A, Hochberg ML. 1991. Direct proof of a “more-than-single-layered” peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study. J Bacteriol 173:751–756 http://dx.doi.org/10.1128/JB.173.2.751-756.1991. [PubMed]
43. Turner RD, Mesnage S, Hobbs JK, Foster SJ. 2018. Molecular imaging of glycan chains couples cell-wall polysaccharide architecture to bacterial cell morphology. Nat Commun 9:1263 http://dx.doi.org/10.1038/s41467-018-03551-y. [PubMed]
44. Demchick P, Koch AL. 1996. The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J Bacteriol 178:768–773 http://dx.doi.org/10.1128/JB.178.3.768-773.1996. [PubMed]
45. Braun V, Rehn K. 1969. Chemical characterization, spatial distribution and function of a lipoprotein (murein-lipoprotein) of the E. coli cell wall. The specific effect of trypsin on the membrane structure. Eur J Biochem 10:426–438 http://dx.doi.org/10.1111/j.1432-1033.1969.tb00707.x. [PubMed]
46. Li G-W, Burkhardt D, Gross C, Weissman JS. 2014. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–635 http://dx.doi.org/10.1016/j.cell.2014.02.033. [PubMed]
47. Magnet S, Bellais S, Dubost L, Fourgeaud M, Mainardi J-L, Petit-Frère S, Marie A, Mengin-Lecreulx D, Arthur M, Gutmann L. 2007. Identification of the l, d-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J Bacteriol 189:3927–3931 http://dx.doi.org/10.1128/JB.00084-07. [PubMed]
48. Inouye M, Shaw J, Shen C. 1972. The assembly of a structural lipoprotein in the envelope of Escherichia coli. J Biol Chem 247:8154–8159.
49. Cowles CE, Li Y, Semmelhack MF, Cristea IM, Silhavy TJ. 2011. The free and bound forms of Lpp occupy distinct subcellular locations in Escherichia coli. Mol Microbiol 79:1168–1181 http://dx.doi.org/10.1111/j.1365-2958.2011.07539.x. [PubMed]
50. Asmar AT, Ferreira JL, Cohen EJ, Cho S-H, Beeby M, Hughes KT, Collet J-F. 2017. Communication across the bacterial cell envelope depends on the size of the periplasm. PLoS Biol 15:e2004303 http://dx.doi.org/10.1371/journal.pbio.2004303. [PubMed]
51. Asmar AT, Collet J-F. 2018. Lpp, the Braun lipoprotein, turns 50: major achievements and remaining issues. FEMS Microbiol Lett 365:fny199 http://dx.doi.org/10.1093/femsle/fny199. [PubMed]
52. Sandoz KM, Moore RA, Beare PA, Patel AV, Smith RE, Bern M, Hwang H, Cooper CJ, Priola SA, Parks JM, Gumbart JC, Mesnage S, Heinzen RA. 2020. β-Barrel proteins tether the outer membrane in many Gram-negative bacteria. Nat Microbiol. Epub ahead of print http://dx.doi.org/10.1038/s41564-020-00798-4. [PubMed]
53. Godessart P, Lannoy A, Dieu M, Van der Verren SE, Soumillion P, Collet JF, Remaut H, Renard P, De Bolle X. 2020. β-Barrels covalently link peptidoglycan and the outer membrane in the α-proteobacterium Brucella abortus. Nat Microbiol; Epub ahead of print http://dx.doi.org/10.1038/s41564-020-00799-3. [PubMed]
54. Desmarais SM, Tropini C, Miguel A, Cava F, Monds RD, de Pedro MA, Huang KC. 2015. High-throughput, highly sensitive analyses of bacterial morphogenesis using ultra performance liquid chromatography. J Biol Chem 290:31090–31100 http://dx.doi.org/10.1074/jbc.M115.661660. [PubMed]
55. Vollmer W. 2008. Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32:287–306 http://dx.doi.org/10.1111/j.1574-6976.2007.00088.x. [PubMed]
56. Yadav AK, Espaillat A, Cava F. 2018. Bacterial strategies to preserve cell wall integrity against environmental threats. Front Microbiol 9:2064 http://dx.doi.org/10.3389/fmicb.2018.02064. [PubMed]
57. Sychantha D, Brott AS, Jones CS, Clarke AJ. 2018. Mechanistic pathways for peptidoglycan O-acetylation and de- O-acetylation. Front Microbiol 9:2332 http://dx.doi.org/10.3389/fmicb.2018.02332. [PubMed]
58. Richaud C, Higgins W, Mengin-Lecreulx D, Stragier P. 1987. Molecular cloning, characterization, and chromosomal localization of dapF, the Escherichia coli gene for diaminopimelate epimerase. J Bacteriol 169:1454–1459 http://dx.doi.org/10.1128/JB.169.4.1454-1459.1987. [PubMed]
59. Mengin-Lecreulx D, Michaud C, Richaud C, Blanot D, van Heijenoort J. 1988. Incorporation of ll-diaminopimelic acid into peptidoglycan of Escherichia coli mutants lacking diaminopimelate epimerase encoded by dapF. J Bacteriol 170:2031–2039 http://dx.doi.org/10.1128/JB.170.5.2031-2039.1988. [PubMed]
60. Parveen S, Reddy M. 2017. Identification of YfiH (PgeF) as a factor contributing to the maintenance of bacterial peptidoglycan composition. Mol Microbiol 105:705–720 http://dx.doi.org/10.1111/mmi.13730. [PubMed]
61. Gally D, Cooper S. 1993. Peptidoglycan synthesis in Salmonella typhimurium 2616. J Gen Microbiol 139:1469–1476 http://dx.doi.org/10.1099/00221287-139-7-1469. [PubMed]
62. Bernal-Cabas M, Ayala JA, Raivio TL. 2015. The Cpx envelope stress response modifies peptidoglycan cross-linking via the l, d-transpeptidase LdtD and the novel protein YgaU. J Bacteriol 197:603–614 http://dx.doi.org/10.1128/JB.02449-14. [PubMed]
63. Delhaye A, Collet J-F, Laloux G. 2016. Fine-tuning of the Cpx envelope stress response is required for cell wall homeostasis in Escherichia coli. MBio 7:e00047-16 http://dx.doi.org/10.1128/mBio.00047-16. [PubMed]
64. Morè N, Martorana AM, Biboy J, Otten C, Winkle M, Serrano CKG, Montón Silva A, Atkinson L, Yau H, Breukink E, den Blaauwen T, Vollmer W, Polissi A. 2019. Peptidoglycan remodeling enables Escherichia coli to survive severe outer membrane assembly defect. MBio 10:e02729-18 http://dx.doi.org/10.1128/mBio.02729-18. [PubMed]
65. Quintela JC, de Pedro MA, Zöllner P, Allmaier G, Garcia-del Portillo F. 1997. Peptidoglycan structure of Salmonella typhimurium growing within cultured mammalian cells. Mol Microbiol 23:693–704 http://dx.doi.org/10.1046/j.1365-2958.1997.2561621.x. [PubMed]
66. Rico-Pérez G, Pezza A, Pucciarelli MG, de Pedro MA, Soncini FC, García-del Portillo F. 2016. A novel peptidoglycan d, l-endopeptidase induced by Salmonella inside eukaryotic cells contributes to virulence. Mol Microbiol 99:546–556 http://dx.doi.org/10.1111/mmi.13248. [PubMed]
67. Geiger T, Pazos M, Lara-Tejero M, Vollmer W, Galán JE. 2018. Peptidoglycan editing by a specific ld-transpeptidase controls the muramidase-dependent secretion of typhoid toxin. Nat Microbiol 3:1243–1254 http://dx.doi.org/10.1038/s41564-018-0248-x. [PubMed]
68. Burman LG, Reichler J, Park JT. 1983. Evidence for multisite growth of Escherichia coli murein involving concomitant endopeptidase and transpeptidase activities. J Bacteriol 156:386–392 http://dx.doi.org/10.1128/JB.156.1.386-392.1983. [PubMed]
69. Goodell EW, Schwarz U. 1983. Cleavage and resynthesis of peptide cross bridges in Escherichia coli murein. J Bacteriol 156:136–140 http://dx.doi.org/10.1128/JB.156.1.136-140.1983. [PubMed]
70. Burman LG, Park JT. 1984. Molecular model for elongation of the murein sacculus of Escherichia coli. Proc Natl Acad Sci USA 81:1844–1848 http://dx.doi.org/10.1073/pnas.81.6.1844. [PubMed]
71. Cooper S, Hsieh ML, Guenther B. 1988. Mode of peptidoglycan synthesis in Salmonella typhimurium: single-strand insertion. J Bacteriol 170:3509–3512 http://dx.doi.org/10.1128/JB.170.8.3509-3512.1988. [PubMed]
72. de Jonge BL, Wientjes FB, Jurida I, Driehuis F, Wouters JT, Nanninga N. 1989. Peptidoglycan synthesis during the cell cycle of Escherichia coli: composition and mode of insertion. J Bacteriol 171:5783–5794 http://dx.doi.org/10.1128/JB.171.11.5783-5794.1989. [PubMed]
73. Kuru E, Hughes HV, Brown PJ, Hall E, Tekkam S, Cava F, de Pedro MA, Brun YV, VanNieuwenhze MS. 2012. In situ probing of newly synthesized peptidoglycan in live bacteria with fluorescent d-amino acids. Angew Chem Int Ed Engl 51:12519–12523 http://dx.doi.org/10.1002/anie.201206749. [PubMed]
74. Kuru E, Tekkam S, Hall E, Brun YV, Van Nieuwenhze MS. 2015. Synthesis of fluorescent d-amino acids and their use for probing peptidoglycan synthesis and bacterial growth in situ. Nat Protoc 10:33–52 http://dx.doi.org/10.1038/nprot.2014.197. [PubMed]
75. Hsu Y-P, Hall E, Booher G, Murphy B, Radkov AD, Yablonowski J, Mulcahey C, Alvarez L, Cava F, Brun YV, Kuru E, VanNieuwenhze MS. 2019. Fluorogenic d-amino acids enable real-time monitoring of peptidoglycan biosynthesis and high-throughput transpeptidation assays. Nat Chem 11:335–341 http://dx.doi.org/10.1038/s41557-019-0217-x. [PubMed]
76. Radkov AD, Hsu Y-P, Booher G, VanNieuwenhze MS. 2018. Imaging bacterial cell wall biosynthesis. Annu Rev Biochem 87:991–1014 http://dx.doi.org/10.1146/annurev-biochem-062917-012921. [PubMed]
77. van Heijenoort J. 2007. Lipid intermediates in the biosynthesis of bacterial peptidoglycan. Microbiol Mol Biol Rev 71:620–635 http://dx.doi.org/10.1128/MMBR.00016-07. [PubMed]
78. Barreteau H, Kovač A, Boniface A, Sova M, Gobec S, Blanot D. 2008. Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev 32:168–207 http://dx.doi.org/10.1111/j.1574-6976.2008.00104.x. [PubMed]
79. Badet B, Vermoote P, Haumont PY, Lederer F, LeGoffic F. 1987. Glucosamine synthetase from Escherichia coli: purification, properties, and glutamine-utilizing site location. Biochemistry 26:1940–1948 http://dx.doi.org/10.1021/bi00381a023. [PubMed]
80. Mengin-Lecreulx D, van Heijenoort J. 1993. Identification of the glmU gene encoding N-acetylglucosamine- 1-phosphate uridyltransferase in Escherichia coli. J Bacteriol 175:6150–6157 http://dx.doi.org/10.1128/JB.175.19.6150-6157.1993. [PubMed]
81. Mengin-Lecreulx D, van Heijenoort J. 1994. Copurification of glucosamine-1-phosphate acetyltransferase and N-acetylglucosamine-1-phosphate uridyltransferase activities of Escherichia coli: characterization of the glmU gene product as a bifunctional enzyme catalyzing two subsequent steps in the pathway for UDP- N-acetylglucosamine synthesis. J Bacteriol 176:5788–5795 http://dx.doi.org/10.1128/JB.176.18.5788-5795.1994. [PubMed]
82. Mengin-Lecreulx D, van Heijenoort J. 1996. Characterization of the essential gene glmM encoding phosphoglucosamine mutase in Escherichia coli. J Biol Chem 271:32–39 http://dx.doi.org/10.1074/jbc.271.1.32.
83. Marquardt JL, Siegele DA, Kolter R, Walsh CT. 1992. Cloning and sequencing of Escherichia coli murZ and purification of its product, a UDP- N-acetylglucosamine enolpyruvyl transferase. J Bacteriol 174:5748–5752 http://dx.doi.org/10.1128/JB.174.17.5748-5752.1992. [PubMed]
84. Benson TE, Marquardt JL, Marquardt AC, Etzkorn FA, Walsh CT. 1993. Overexpression, purification, and mechanistic study of UDP- N-acetylenolpyruvylglucosamine reductase. Biochemistry 32:2024–2030 http://dx.doi.org/10.1021/bi00059a019. [PubMed]
85. Kahan FM, Kahan JS, Cassidy PJ, Kropp H. 1974. The mechanism of action of fosfomycin (phosphonomycin). Ann N Y Acad Sci 235:364–386 http://dx.doi.org/10.1111/j.1749-6632.1974.tb43277.x. [PubMed]
86. Liger D, Masson A, Blanot D, van Heijenoort J, Parquet C. 1995. Over-production, purification and properties of the uridine-diphosphate- N-acetylmuramate: l-alanine ligase from Escherichia coli. Eur J Biochem 230:80–87 http://dx.doi.org/10.1111/j.1432-1033.1995.0080i.x. [PubMed]
87. Doublet P, van Heijenoort J, Bohin JP, Mengin-Lecreulx D. 1993. The murI gene of Escherichia coli is an essential gene that encodes a glutamate racemase activity. J Bacteriol 175:2970–2979 http://dx.doi.org/10.1128/JB.175.10.2970-2979.1993. [PubMed]
88. Pratviel-Sosa F, Mengin-Lecreulx D, van Heijenoort J. 1991. Over-production, purification and properties of the uridine diphosphate N-acetylmuramoyl- l-alanine: d-glutamate ligase from Escherichia coli. Eur J Biochem 202:1169–1176 http://dx.doi.org/10.1111/j.1432-1033.1991.tb16486.x. [PubMed]
89. Michaud C, Mengin-Lecreulx D, van Heijenoort J, Blanot D. 1990. Over-production, purification and properties of the uridine-diphosphate- N-acetylmuramoyl- l-alanyl- d-glutamate: meso-2,6-diaminopimelate ligase from Escherichia coli. Eur J Biochem 194:853–861 http://dx.doi.org/10.1111/j.1432-1033.1990.tb19479.x. [PubMed]
90. Duncan K, van Heijenoort J, Walsh CT. 1990. Purification and characterization of the d-alanyl- d-alanine-adding enzyme from Escherichia coli. Biochemistry 29:2379–2386 http://dx.doi.org/10.1021/bi00461a023. [PubMed]
91. Wild J, Hennig J, Lobocka M, Walczak W, Kłopotowski T. 1985. Identification of the dadX gene coding for the predominant isozyme of alanine racemase in Escherichia coli K12. Mol Gen Genet 198:315–322 http://dx.doi.org/10.1007/BF00383013. [PubMed]
92. Wijsman HJ. 1972. The characterization of an alanine racemase mutant of Escherichia coli. Genet Res 20:269–277 http://dx.doi.org/10.1017/S001667230001380X. [PubMed]
93. Zawadzke LE, Bugg TDH, Walsh CT. 1991. Existence of two d-alanine: d-alanine ligases in Escherichia coli: cloning and sequencing of the ddlA gene and purification and characterization of the DdlA and DdlB enzymes. Biochemistry 30:1673–1682 http://dx.doi.org/10.1021/bi00220a033. [PubMed]
94. Neuhaus FC, Lynch JL. 1964. The enzymatic synthesis of d-alanyl- d-alanine: on the inhibition of d-alanyl- d-alanine synthetase by the antibiotic d-cycloserine. Biochemistry 3:471–480 http://dx.doi.org/10.1021/bi00892a001. [PubMed]
95. Park JT, Uehara T. 2008. How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol Mol Biol Rev 72:211–227 http://dx.doi.org/10.1128/MMBR.00027-07. [PubMed]
96. Mengin-Lecreulx D, van Heijenoort J, Park JT. 1996. Identification of the mpl gene encoding UDP- N-acetylmuramate: l-alanyl-γ- d-glutamyl-meso-diaminopimelate ligase in Escherichia coli and its role in recycling of cell wall peptidoglycan. J Bacteriol 178:5347–5352 http://dx.doi.org/10.1128/JB.178.18.5347-5352.1996. [PubMed]
97. Ikeda M, Wachi M, Jung HK, Ishino F, Matsuhashi M. 1991. The Escherichia coli mraY gene encoding UDP- N-acetylmuramoyl-pentapeptide: undecaprenyl-phosphate phospho- N-acetylmuramoyl-pentapeptide transferase. J Bacteriol 173:1021–1026 http://dx.doi.org/10.1128/JB.173.3.1021-1026.1991. [PubMed]
98. Fujisaki S, Nishino T, Katsuki H. 1986. Isoprenoid synthesis in Escherichia coli. Separation and partial purification of four enzymes involved in the synthesis. J Biochem 99:1327–1337 http://dx.doi.org/10.1093/oxfordjournals.jbchem.a135600. [PubMed]
99. El Ghachi M, Bouhss A, Blanot D, Mengin-Lecreulx D. 2004. The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity. J Biol Chem 279:30106–30113 http://dx.doi.org/10.1074/jbc.M401701200. [PubMed]
100. El Ghachi M, Derbise A, Bouhss A, Mengin-Lecreulx D. 2005. Identification of multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP) activity in Escherichia coli. J Biol Chem 280:18689–18695 http://dx.doi.org/10.1074/jbc.M412277200. [PubMed]
101. TouzÉ T, Mengin-Lecreulx D. 2008. Undecaprenyl phosphate synthesis. Ecosal Plus 3:3 http://dx.doi.org/10.1128/ecosalplus.4.7.1.7. [PubMed]
102. Stone KJ, Strominger JL. 1971. Mechanism of action of bacitracin: complexation with metal ion and C 55-isoprenyl pyrophosphate. Proc Natl Acad Sci USA 68:3223–3227 http://dx.doi.org/10.1073/pnas.68.12.3223. [PubMed]
103. Tamura G, Sasaki T, Matsuhashi M, Takatsuki A, Yamasaki M. 1975. Tunicamycin inhibits the formation of lipid intermediate in cell-free peptidoglycan synthesis of bacteria. Agric Biol Chem 40:447–449.
104. Mengin-Lecreulx D, Texier L, Rousseau M, van Heijenoort J. 1991. The murG gene of Escherichia coli codes for the UDP- N-acetylglucosamine: N-acetylmuramyl-(pentapeptide) pyrophosphoryl-undecaprenol N-acetylglucosamine transferase involved in the membrane steps of peptidoglycan synthesis. J Bacteriol 173:4625–4636 http://dx.doi.org/10.1128/JB.173.15.4625-4636.1991. [PubMed]
105. Bupp K, van Heijenoort J. 1993. The final step of peptidoglycan subunit assembly in Escherichia coli occurs in the cytoplasm. J Bacteriol 175:1841–1843 http://dx.doi.org/10.1128/JB.175.6.1841-1843.1993. [PubMed]
106. Mohammadi T, Karczmarek A, Crouvoisier M, Bouhss A, Mengin-Lecreulx D, den Blaauwen T. 2007. The essential peptidoglycan glycosyltransferase MurG forms a complex with proteins involved in lateral envelope growth as well as with proteins involved in cell division in Escherichia coli. Mol Microbiol 65:1106–1121 http://dx.doi.org/10.1111/j.1365-2958.2007.05851.x. [PubMed]
107. Bugg TDH, Walsh CT. 1992. Intracellular steps of bacterial cell wall peptidoglycan biosynthesis: enzymology, antibiotics, and antibiotic resistance. Nat Prod Rep 9:199–215 http://dx.doi.org/10.1039/np9920900199. [PubMed]
108. van Heijenoort J. 2001. Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nat Prod Rep 18:503–519 http://dx.doi.org/10.1039/a804532a. [PubMed]
109. Bouhss A, Trunkfield AE, Bugg TDH, Mengin-Lecreulx D. 2008. The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 32:208–233 http://dx.doi.org/10.1111/j.1574-6976.2007.00089.x. [PubMed]
110. Ikeda M, Sato T, Wachi M, Jung HK, Ishino F, Kobayashi Y, Matsuhashi M. 1989. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J Bacteriol 171:6375–6378 http://dx.doi.org/10.1128/JB.171.11.6375-6378.1989. [PubMed]
111. Inoue A, Murata Y, Takahashi H, Tsuji N, Fujisaki S, Kato J. 2008. Involvement of an essential gene, mviN, in murein synthesis in Escherichia coli. J Bacteriol 190:7298–7301 http://dx.doi.org/10.1128/JB.00551-08. [PubMed]
112. Ruiz N. 2008. Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. Proc Natl Acad Sci USA 105:15553–15557 http://dx.doi.org/10.1073/pnas.0808352105. [PubMed]
113. Ehlert K, Höltje JV. 1996. Role of precursor translocation in coordination of murein and phospholipid synthesis in Escherichia coli. J Bacteriol 178:6766–6771 http://dx.doi.org/10.1128/JB.178.23.6766-6771.1996. [PubMed]
114. Sham L-T, Butler EK, Lebar MD, Kahne D, Bernhardt TG, Ruiz N. 2014. Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345:220–222 http://dx.doi.org/10.1126/science.1254522. [PubMed]
115. Hvorup RN, Winnen B, Chang AB, Jiang Y, Zhou X-F, Saier MH Jr. 2003. The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. Eur J Biochem 270:799–813 http://dx.doi.org/10.1046/j.1432-1033.2003.03418.x. [PubMed]
116. Ruiz N. 2016. Lipid flippases for bacterial peptidoglycan biosynthesis. Lipid Insights 8(Suppl 1) :21–31 . [PubMed]
117. Kumar S, Rubino FA, Mendoza AG, Ruiz N. 2019. The bacterial lipid II flippase MurJ functions by an alternating-access mechanism. J Biol Chem 294:981–990 http://dx.doi.org/10.1074/jbc.RA118.006099. [PubMed]
118. Kuk ACY, Hao A, Guan Z, Lee S-Y. 2019. Visualizing conformation transitions of the lipid II flippase MurJ. Nat Commun 10:1736 http://dx.doi.org/10.1038/s41467-019-09658-0. [PubMed]
119. Zheng S, Sham L-T, Rubino FA, Brock KP, Robins WP, Mekalanos JJ, Marks DS, Bernhardt TG, Kruse AC. 2018. Structure and mutagenic analysis of the lipid II flippase MurJ from Escherichia coli. Proc Natl Acad Sci USA 115:6709–6714 http://dx.doi.org/10.1073/pnas.1802192115. [PubMed]
120. Rubino FA, Kumar S, Ruiz N, Walker S, Kahne DE. 2018. Membrane potential is required for MurJ function. J Am Chem Soc 140:4481–4484 http://dx.doi.org/10.1021/jacs.8b00942. [PubMed]
121. Mohammadi T, van Dam V, Sijbrandi R, Vernet T, Zapun A, Bouhss A, Diepeveen-de Bruin M, Nguyen-Distèche M, de Kruijff B, Breukink E. 2011. Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J 30:1425–1432 http://dx.doi.org/10.1038/emboj.2011.61. [PubMed]
122. Liu X, Meiresonne NY, Bouhss A, den Blaauwen T. 2018. FtsW activity and lipid II synthesis are required for recruitment of MurJ to midcell during cell division in Escherichia coli. Mol Microbiol 109:855–884 http://dx.doi.org/10.1111/mmi.14104. [PubMed]
123. Taguchi A, Welsh MA, Marmont LS, Lee W, Sjodt M, Kruse AC, Kahne D, Bernhardt TG, Walker S. 2019. FtsW is a peptidoglycan polymerase that is functional only in complex with its cognate penicillin-binding protein. Nat Microbiol 4:587–594 http://dx.doi.org/10.1038/s41564-018-0345-x. [PubMed]
124. Reichmann NT, Tavares AC, Saraiva BM, Jousselin A, Reed P, Pereira AR, Monteiro JM, Sobral RG, VanNieuwenhze MS, Fernandes F, Pinho MG. 2019. SEDS-bPBP pairs direct lateral and septal peptidoglycan synthesis in Staphylococcus aureus. Nat Microbiol 4:1368–1377 http://dx.doi.org/10.1038/s41564-019-0437-2. [PubMed]
125. Welsh MA, Schaefer K, Taguchi A, Kahne D, Walker S. 2019. Direction of chain growth and substrate preferences of shape, elongation, division, and sporulation-family peptidoglycan glycosyltransferases. J Am Chem Soc 141:12994–12997 http://dx.doi.org/10.1021/jacs.9b06358. [PubMed]
126. Bertsche U, Breukink E, Kast T, Vollmer W. 2005. In vitro murein peptidoglycan synthesis by dimers of the bifunctional transglycosylase-transpeptidase PBP1B from Escherichia coli. J Biol Chem 280:38096–38101 http://dx.doi.org/10.1074/jbc.M508646200. [PubMed]
127. Hernández-Rocamora VM, Otten CF, Radkov A, Simorre J-P, Breukink E, VanNieuwenhze M, Vollmer W. 2018. Coupling of polymerase and carrier lipid phosphatase prevents product inhibition in peptidoglycan synthesis. Cell Surf 2:1–13 http://dx.doi.org/10.1016/j.tcsw.2018.04.002. [PubMed]
128. van Dam V, Sijbrandi R, Kol M, Swiezewska E, de Kruijff B, Breukink E. 2007. Transmembrane transport of peptidoglycan precursors across model and bacterial membranes. Mol Microbiol 64:1105–1114 http://dx.doi.org/10.1111/j.1365-2958.2007.05722.x. [PubMed]
129. Ling LL, Schneider T, Peoples AJ, Spoering AL, Engels I, Conlon BP, Mueller A, Schäberle TF, Hughes DE, Epstein S, Jones M, Lazarides L, Steadman VA, Cohen DR, Felix CR, Fetterman KA, Millett WP, Nitti AG, Zullo AM, Chen C, Lewis K. 2015. A new antibiotic kills pathogens without detectable resistance. Nature 517:455–459 http://dx.doi.org/10.1038/nature14098. [PubMed]
130. El Ghachi M, Bouhss A, Barreteau H, Touzé T, Auger G, Blanot D, Mengin-Lecreulx D. 2006. Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J Biol Chem 281:22761–22772 http://dx.doi.org/10.1074/jbc.M602834200. [PubMed]
131. Manat G, Roure S, Auger R, Bouhss A, Barreteau H, Mengin-Lecreulx D, Touzé T. 2014. Deciphering the metabolism of undecaprenyl-phosphate: the bacterial cell-wall unit carrier at the membrane frontier. Microb Drug Resist 20:199–214 http://dx.doi.org/10.1089/mdr.2014.0035. [PubMed]
132. Jorgenson MA, Young KD. 2016. Interrupting biosynthesis of O antigen or the lipopolysaccharide core produces morphological defects in Escherichia coli by sequestering undecaprenyl phosphate. J Bacteriol 198:3070–3079 http://dx.doi.org/10.1128/JB.00550-16. [PubMed]
133. Jorgenson MA, Kannan S, Laubacher ME, Young KD. 2016. Dead-end intermediates in the enterobacterial common antigen pathway induce morphological defects in Escherichia coli by competing for undecaprenyl phosphate. Mol Microbiol 100:1–14 http://dx.doi.org/10.1111/mmi.13284. [PubMed]
134. Paradis-Bleau C, Kritikos G, Orlova K, Typas A, Bernhardt TG. 2014. A genome-wide screen for bacterial envelope biogenesis mutants identifies a novel factor involved in cell wall precursor metabolism. PLoS Genet 10:e1004056 http://dx.doi.org/10.1371/journal.pgen.1004056. [PubMed]
135. Grabowicz M, Andres D, Lebar MD, Malojčić G, Kahne D, Silhavy TJ. 2014. A mutant Escherichia coli that attaches peptidoglycan to lipopolysaccharide and displays cell wall on its surface. eLife 3:e05334 http://dx.doi.org/10.7554/eLife.05334. [PubMed]
136. Jiang X, Tan WB, Shrivastava R, Seow DCS, Chen SL, Guan XL, Chng S. 2020. Mutations in enterobacterial common antigen biosynthesis restore outer membrane barrier function in Escherichia coli tol-pal mutants. Mol Microbiol. Epub ahead of print. [PubMed]
137. den Blaauwen T, de Pedro MA, Nguyen-Distèche M, Ayala JA. 2008. Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 32:321–344 http://dx.doi.org/10.1111/j.1574-6976.2007.00090.x. [PubMed]
138. Matsuzawa H, Hayakawa K, Sato T, Imahori K. 1973. Characterization and genetic analysis of a mutant of Escherichia coli K-12 with rounded morphology. J Bacteriol 115:436–442 http://dx.doi.org/10.1128/JB.115.1.436-442.1973. [PubMed]
139. Stoker NG, Pratt JM, Spratt BG. 1983. Identification of the rodA gene product of Escherichia coli. J Bacteriol 155:854–859 http://dx.doi.org/10.1128/JB.155.2.854-859.1983. [PubMed]
140. Ishino F, Park W, Tomioka S, Tamaki S, Takase I, Kunugita A, Matsuzawa H, Asoh S, Ohta T, Spratt BG, Matsuhashi M. 1986. Peptidoglycan synthetic activities in membranes of Escherichia coli caused by overproduction of penicillin-binding protein 2 and RodA protein. J Biol Chem 261:7024–7031.
141. Meeske AJ, Riley EP, Robins WP, Uehara T, Mekalanos JJ, Kahne D, Walker S, Kruse AC, Bernhardt TG, Rudner DZ. 2016. SEDS proteins are a widespread family of bacterial cell wall polymerases. Nature 537:634–638 http://dx.doi.org/10.1038/nature19331. [PubMed]
142. Emami K, Guyet A, Kawai Y, Devi J, Wu LJ, Allenby N, Daniel RA, Errington J. 2017. RodA as the missing glycosyltransferase in Bacillus subtilis and antibiotic discovery for the peptidoglycan polymerase pathway. Nat Microbiol 2:16253 http://dx.doi.org/10.1038/nmicrobiol.2016.253. [PubMed]
143. Cho H, Wivagg CN, Kapoor M, Barry Z, Rohs PDA, Suh H, Marto JA, Garner EC, Bernhardt TG. 2016. Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously. Nat Microbiol 1:16172 http://dx.doi.org/10.1038/nmicrobiol.2016.172. [PubMed]
144. Henriques AO, Glaser P, Piggot PJ, Moran CP Jr. 1998. Control of cell shape and elongation by the rodA gene in Bacillus subtilis. Mol Microbiol 28:235–247 http://dx.doi.org/10.1046/j.1365-2958.1998.00766.x. [PubMed]
145. Spratt BG. 1975. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc Natl Acad Sci USA 72:2999–3003 http://dx.doi.org/10.1073/pnas.72.8.2999. [PubMed]
146. Spratt BG, Pardee AB. 1975. Penicillin-binding proteins and cell shape in E. coli. Nature 254:516–517 http://dx.doi.org/10.1038/254516a0. [PubMed]
147. Den Blaauwen T, Aarsman ME, Vischer NO, Nanninga N. 2003. Penicillin-binding protein PBP2 of Escherichia coli localizes preferentially in the lateral wall and at mid-cell in comparison with the old cell pole. Mol Microbiol 47:539–547 http://dx.doi.org/10.1046/j.1365-2958.2003.03316.x. [PubMed]
148. Perkins HR. 1969. Specificity of combination between mucopeptide precursors and vancomycin or ristocetin. Biochem J 111:195–205 http://dx.doi.org/10.1042/bj1110195. [PubMed]
149. Cho H, Uehara T, Bernhardt TG. 2014. Beta-lactam antibiotics induce a lethal malfunctioning of the bacterial cell wall synthesis machinery. Cell 159:1300–1311 http://dx.doi.org/10.1016/j.cell.2014.11.017. [PubMed]
150. Lai GC, Cho H, Bernhardt TG. 2017. The mecillinam resistome reveals a role for peptidoglycan endopeptidases in stimulating cell wall synthesis in Escherichia coli. PLoS Genet 13:e1006934 http://dx.doi.org/10.1371/journal.pgen.1006934. [PubMed]
151. Sjodt M, Brock K, Dobihal G, Rohs PDA, Green AG, Hopf TA, Meeske AJ, Srisuknimit V, Kahne D, Walker S, Marks DS, Bernhardt TG, Rudner DZ, Kruse AC. 2018. Structure of the peptidoglycan polymerase RodA resolved by evolutionary coupling analysis. Nature 556:118–121 http://dx.doi.org/10.1038/nature25985. [PubMed]
152. Sjodt M, Rohs PDA, Gilman MSA, Erlandson SC, Zheng S, Green AG, Brock KP, Taguchi A, Kahne D, Walker S, Marks DS, Rudner DZ, Bernhardt TG, Kruse AC. 2020. Structural coordination of polymerization and crosslinking by a SEDS-bPBP peptidoglycan synthase complex. Nat Microbiol 5:813–820 http://dx.doi.org/10.1038/s41564-020-0687-z. [PubMed]
153. Banzhaf M, van den Berg van Saparoea B, Terrak M, Fraipont C, Egan A, Philippe J, Zapun A, Breukink E, Nguyen-Distèche M, den Blaauwen T, Vollmer W. 2012. Cooperativity of peptidoglycan synthases active in bacterial cell elongation. Mol Microbiol 85:179–194 http://dx.doi.org/10.1111/j.1365-2958.2012.08103.x. [PubMed]
154. Morgenstein RM, Bratton BP, Nguyen JP, Ouzounov N, Shaevitz JW, Gitai Z. 2015. RodZ links MreB to cell wall synthesis to mediate MreB rotation and robust morphogenesis. Proc Natl Acad Sci USA 112:12510–12515 http://dx.doi.org/10.1073/pnas.1509610112. [PubMed]
155. Doi M, Wachi M, Ishino F, Tomioka S, Ito M, Sakagami Y, Suzuki A, Matsuhashi M. 1988. Determinations of the DNA sequence of the mreB gene and of the gene products of the mre region that function in formation of the rod shape of Escherichia coli cells. J Bacteriol 170:4619–4624 http://dx.doi.org/10.1128/JB.170.10.4619-4624.1988. [PubMed]
156. Jones LJF, Carballido-López R, Errington J. 2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913–922 http://dx.doi.org/10.1016/S0092-8674(01)00287-2.
157. Kruse T, Møller-Jensen J, Løbner-Olesen A, Gerdes K. 2003. Dysfunctional MreB inhibits chromosome segregation in Escherichia coli. EMBO J 22:5283–5292 http://dx.doi.org/10.1093/emboj/cdg504. [PubMed]
158. Shih Y-L, Rothfield L. 2006. The bacterial cytoskeleton. Microbiol Mol Biol Rev 70:729–754 http://dx.doi.org/10.1128/MMBR.00017-06. [PubMed]
159. Wang S, Arellano-Santoyo H, Combs PA, Shaevitz JW. 2010. Actin-like cytoskeleton filaments contribute to cell mechanics in bacteria. Proc Natl Acad Sci USA 107:9182–9185 http://dx.doi.org/10.1073/pnas.0911517107. [PubMed]
160. van den Ent F, Amos LA, Löwe J. 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413:39–44 http://dx.doi.org/10.1038/35092500. [PubMed]
161. Chastanet A, Carballido-Lopez R. 2012. The actin-like MreB proteins in Bacillus subtilis: a new turn. Front Biosci (Schol Ed) 4:1582–1606. [PubMed]
162. Hussain S, Wivagg CN, Szwedziak P, Wong F, Schaefer K, Izoré T, Renner LD, Holmes MJ, Sun Y, Bisson-Filho AW, Walker S, Amir A, Löwe J, Garner EC. 2018. MreB filaments align along greatest principal membrane curvature to orient cell wall synthesis. eLife 7:e32471 http://dx.doi.org/10.7554/eLife.32471. [PubMed]
163. Billaudeau C, Yao Z, Cornilleau C, Carballido-López R, Chastanet A. 2019. MreB forms subdiffraction nanofilaments during active growth in Bacillus subtilis. MBio 10:01879-18 http://dx.doi.org/10.1128/mBio.01879-18. [PubMed]
164. Kruse T, Bork-Jensen J, Gerdes K. 2005. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55:78–89 http://dx.doi.org/10.1111/j.1365-2958.2004.04367.x. [PubMed]
165. Kruse T, Blagoev B, Løbner-Olesen A, Wachi M, Sasaki K, Iwai N, Mann M, Gerdes K. 2006. Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev 20:113–124 http://dx.doi.org/10.1101/gad.366606. [PubMed]
166. Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L. 2005. MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120:329–341 http://dx.doi.org/10.1016/j.cell.2005.01.007. [PubMed]
167. Takacs CN, Poggio S, Charbon G, Pucheault M, Vollmer W, Jacobs-Wagner C. 2010. MreB drives de novo rod morphogenesis in Caulobacter crescentus via remodeling of the cell wall. J Bacteriol 192:1671–1684 http://dx.doi.org/10.1128/JB.01311-09. [PubMed]
168. Wachi M, Osaka K, Kohama T, Sasaki K, Ohtsu I, Iwai N, Takada A, Nagai K. 2006. Transcriptional analysis of the Escherichia coli mreBCD genes responsible for morphogenesis and chromosome segregation. Biosci Biotechnol Biochem 70:2712–2719 http://dx.doi.org/10.1271/bbb.60315. [PubMed]
169. Bendezú FO, Hale CA, Bernhardt TG, de Boer PAJ. 2009. RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J 28:193–204 http://dx.doi.org/10.1038/emboj.2008.264. [PubMed]
170. Shiomi D, Sakai M, Niki H. 2008. Determination of bacterial rod shape by a novel cytoskeletal membrane protein. EMBO J 27:3081–3091 http://dx.doi.org/10.1038/emboj.2008.234. [PubMed]
171. Alyahya SA, Alexander R, Costa T, Henriques AO, Emonet T, Jacobs-Wagner C. 2009. RodZ, a component of the bacterial core morphogenic apparatus. Proc Natl Acad Sci USA 106:1239–1244 http://dx.doi.org/10.1073/pnas.0810794106. [PubMed]
172. van den Ent F, Johnson CM, Persons L, de Boer P, Löwe J. 2010. Bacterial actin MreB assembles in complex with cell shape protein RodZ. EMBO J 29:1081–1090 http://dx.doi.org/10.1038/emboj.2010.9. [PubMed]
173. Colavin A, Shi H, Huang KC. 2018. RodZ modulates geometric localization of the bacterial actin MreB to regulate cell shape. Nat Commun 9:1280 http://dx.doi.org/10.1038/s41467-018-03633-x. [PubMed]
174. Contreras-Martel C, Martins A, Ecobichon C, Trindade DM, Matteï P-J, Hicham S, Hardouin P, Ghachi ME, Boneca IG, Dessen A. 2017. Molecular architecture of the PBP2-MreC core bacterial cell wall synthesis complex. Nat Commun 8:776 http://dx.doi.org/10.1038/s41467-017-00783-2. [PubMed]
175. Rohs PDA, Buss J, Sim SI, Squyres GR, Srisuknimit V, Smith M, Cho H, Sjodt M, Kruse AC, Garner EC, Walker S, Kahne DE, Bernhardt TG. 2018. A central role for PBP2 in the activation of peptidoglycan polymerization by the bacterial cell elongation machinery. PLoS Genet 14:e1007726 http://dx.doi.org/10.1371/journal.pgen.1007726. [PubMed]
176. Özbaykal G, Wollrab E, Simon F, Vigouroux A, Cordier B, Aristov A, Chaze T, Matondo M, van Teeffelen S. 2020. The transpeptidase PBP2 governs initial localization and activity of the major cell-wall synthesis machinery in E. coli. eLife 9:e50629 http://dx.doi.org/10.7554/eLife.50629. [PubMed]
177. van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS, Shaevitz JW, Gitai Z. 2011. The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci USA 108:15822–15827 http://dx.doi.org/10.1073/pnas.1108999108. [PubMed]
178. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:222–225 http://dx.doi.org/10.1126/science.1203285. [PubMed]
179. Domínguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Söldner R, Carballido-López R. 2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:225–228 http://dx.doi.org/10.1126/science.1203466. [PubMed]
180. Furchtgott L, Wingreen NS, Huang KC. 2011. Mechanisms for maintaining cell shape in rod-shaped Gram-negative bacteria. Mol Microbiol 81:340–353 http://dx.doi.org/10.1111/j.1365-2958.2011.07616.x. [PubMed]
181. Vigouroux A, Cordier B, Aristov A, Alvarez L, Özbaykal G, Chaze T, Oldewurtel ER, Matondo M, Cava F, Bikard D, van Teeffelen S. 2020. Class-A penicillin binding proteins do not contribute to cell shape but repair cell-wall defects. eLife 9:e51998 http://dx.doi.org/10.7554/eLife.51998. [PubMed]
182. Sun Y, Garner E. 2020. PrkC modulates MreB filament density and cellular growth rate by monitoring cell wall precursors. bioRxiv 2020.08.28.272336.
183. Bendezú FO, de Boer PAJ. 2008. Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J Bacteriol 190:1792–1811 http://dx.doi.org/10.1128/JB.01322-07. [PubMed]
184. Vinella D, Cashel M, D’Ari R. 2000. Selected amplification of the cell division genes ftsQ- ftsA- ftsZ in Escherichia coli. Genetics 156:1483–1492.
185. Daniel RA, Errington J. 2003. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776 http://dx.doi.org/10.1016/S0092-8674(03)00421-5.
186. Yousif SY, Broome-Smith JK, Spratt BG. 1985. Lysis of Escherichia coli by beta-lactam antibiotics: deletion analysis of the role of penicillin-binding proteins 1A and 1B. J Gen Microbiol 131:2839–2845. [PubMed]
187. Denome SA, Elf PK, Henderson TA, Nelson DE, Young KD. 1999. Escherichia coli mutants lacking all possible combinations of eight penicillin binding proteins: viability, characteristics, and implications for peptidoglycan synthesis. J Bacteriol 181:3981–3993 http://dx.doi.org/10.1128/JB.181.13.3981-3993.1999. [PubMed]
188. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. 2008. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32:234–258 http://dx.doi.org/10.1111/j.1574-6976.2008.00105.x. [PubMed]
189. Schiffer G, Höltje J-V. 1999. Cloning and characterization of PBP 1C, a third member of the multimodular class A penicillin-binding proteins of Escherichia coli. J Biol Chem 274:32031–32039 http://dx.doi.org/10.1074/jbc.274.45.32031. [PubMed]
190. Nakagawa J, Tamaki S, Tomioka S, Matsuhashi M. 1984. Functional biosynthesis of cell wall peptidoglycan by polymorphic bifunctional polypeptides. Penicillin-binding protein 1Bs of Escherichia coli with activities of transglycosylase and transpeptidase. J Biol Chem 259:13937–13946.
191. Schwartz B, Markwalder JA, Wang Y. 2001. Lipid II: total synthesis of the bacterial cell wall precursor and utilization as a substrate for glycosyltransfer and transpeptidation by penicillin binding protein (PBP) 1b of Escherichia coli. J Am Chem Soc 123:11638–11643 http://dx.doi.org/10.1021/ja0166848. [PubMed]
192. Born P, Breukink E, Vollmer W. 2006. In vitro synthesis of cross-linked murein and its attachment to sacculi by PBP1A from Escherichia coli. J Biol Chem 281:26985–26993 http://dx.doi.org/10.1074/jbc.M604083200. [PubMed]
193. Leclercq S, Derouaux A, Olatunji S, Fraipont C, Egan AJF, Vollmer W, Breukink E, Terrak M. 2017. Interplay between penicillin-binding proteins and SEDS proteins promotes bacterial cell wall synthesis. Sci Rep 7:43306 http://dx.doi.org/10.1038/srep43306. [PubMed]
194. Müller P, Ewers C, Bertsche U, Anstett M, Kallis T, Breukink E, Fraipont C, Terrak M, Nguyen-Distèche M, Vollmer W. 2007. The essential cell division protein FtsN interacts with the murein (peptidoglycan) synthase PBP1B in Escherichia coli. J Biol Chem 282:36394–36402 http://dx.doi.org/10.1074/jbc.M706390200. [PubMed]
195. Mueller EA, Egan AJ, Breukink E, Vollmer W, Levin PA. 2019. Plasticity of Escherichia coli cell wall metabolism promotes fitness and antibiotic resistance across environmental conditions. eLife 8:e40754 http://dx.doi.org/10.7554/eLife.40754. [PubMed]
196. Yunck R, Cho H, Bernhardt TG. 2016. Identification of MltG as a potential terminase for peptidoglycan polymerization in bacteria. Mol Microbiol 99:700–718 http://dx.doi.org/10.1111/mmi.13258. [PubMed]
197. Vollmer W, von Rechenberg M, Höltje J-V. 1999. Demonstration of molecular interactions between the murein polymerase PBP1B, the lytic transglycosylase MltA, and the scaffolding protein MipA of Escherichia coli. J Biol Chem 274:6726–6734 http://dx.doi.org/10.1074/jbc.274.10.6726. [PubMed]
198. Ranjit DK, Jorgenson MA, Young KD. 2017. PBP1B glycosyltransferase and transpeptidase activities play different essential roles during the de novo regeneration of rod morphology in Escherichia coli. J Bacteriol 199:e00612–e00616 http://dx.doi.org/10.1128/JB.00612-16. [PubMed]
199. Gray AN, Egan AJ, Van’t Veer IL, Verheul J, Colavin A, Koumoutsi A, Biboy J, Altelaar AFM, Damen MJ, Huang KC, Simorre J-P, Breukink E, den Blaauwen T, Typas A, Gross CA, Vollmer W. 2015. Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division. eLife 4:e07118 http://dx.doi.org/10.7554/eLife.07118. [PubMed]
200. Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S, Kahne DE, Bernhardt TG. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:1110–1120 http://dx.doi.org/10.1016/j.cell.2010.11.037. [PubMed]
201. Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J, Nichols RJ, Zietek M, Beilharz K, Kannenberg K, von Rechenberg M, Breukink E, den Blaauwen T, Gross CA, Vollmer W. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097–1109 http://dx.doi.org/10.1016/j.cell.2010.11.038. [PubMed]
202. Lupoli TJ, Lebar MD, Markovski M, Bernhardt T, Kahne D, Walker S. 2014. Lipoprotein activators stimulate Escherichia coli penicillin-binding proteins by different mechanisms. J Am Chem Soc 136:52–55 http://dx.doi.org/10.1021/ja410813j. [PubMed]
203. Jean NL, Bougault CM, Lodge A, Derouaux A, Callens G, Egan AJF, Ayala I, Lewis RJ, Vollmer W, Simorre J-P. 2014. Elongated structure of the outer-membrane activator of peptidoglycan synthesis LpoA: implications for PBP1A stimulation. Structure 22:1047–1054 http://dx.doi.org/10.1016/j.str.2014.04.017. [PubMed]
204. Egan AJF, Jean NL, Koumoutsi A, Bougault CM, Biboy J, Sassine J, Solovyova AS, Breukink E, Typas A, Vollmer W, Simorre J-P. 2014. Outer-membrane lipoprotein LpoB spans the periplasm to stimulate the peptidoglycan synthase PBP1B. Proc Natl Acad Sci USA 111:8197–8202 http://dx.doi.org/10.1073/pnas.1400376111. [PubMed]
205. Sung M-T, Lai Y-T, Huang C-Y, Chou L-Y, Shih H-W, Cheng W-C, Wong C-H, Ma C. 2009. Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli. Proc Natl Acad Sci USA 106:8824–8829 http://dx.doi.org/10.1073/pnas.0904030106.
206. Markovski M, Bohrhunter JL, Lupoli TJ, Uehara T, Walker S, Kahne DE, Bernhardt TG. 2016. Cofactor bypass variants reveal a conformational control mechanism governing cell wall polymerase activity. Proc Natl Acad Sci USA 113:4788–4793 http://dx.doi.org/10.1073/pnas.1524538113. [PubMed]
207. Egan AJF, Maya-Martinez R, Ayala I, Bougault CM, Banzhaf M, Breukink E, Vollmer W, Simorre J-P. 2018. Induced conformational changes activate the peptidoglycan synthase PBP1B. Mol Microbiol 110:335–356 http://dx.doi.org/10.1111/mmi.14082. [PubMed]
208. Greene NG, Fumeaux C, Bernhardt TG. 2018. Conserved mechanism of cell-wall synthase regulation revealed by the identification of a new PBP activator in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 115:3150–3155 http://dx.doi.org/10.1073/pnas.1717925115. [PubMed]
209. Dörr T, Lam H, Alvarez L, Cava F, Davis BM, Waldor MK. 2014. A novel peptidoglycan binding protein crucial for PBP1A-mediated cell wall biogenesis in Vibrio cholerae. PLoS Genet 10:e1004433 http://dx.doi.org/10.1371/journal.pgen.1004433. [PubMed]
210. Wong F, Renner LD, Özbaykal G, Paulose J, Weibel DB, van Teeffelen S, Amir A. 2017. Mechanical strain sensing implicated in cell shape recovery in Escherichia coli. Nat Microbiol 2:17115 http://dx.doi.org/10.1038/nmicrobiol.2017.115. [PubMed]
211. Dion MF, Kapoor M, Sun Y, Wilson S, Ryan J, Vigouroux A, van Teeffelen S, Oldenbourg R, Garner EC. 2019. Bacillus subtilis cell diameter is determined by the opposing actions of two distinct cell wall synthetic systems. Nat Microbiol 4:1294–1305 http://dx.doi.org/10.1038/s41564-019-0439-0. [PubMed]
212. van Teeffelen S, Renner LD. 2018. Recent advances in understanding how rod-like bacteria stably maintain their cell shapes. F1000 Res 7:241 http://dx.doi.org/10.12688/f1000research.12663.1. [PubMed]
213. Hugonnet J-E, Mengin-Lecreulx D, Monton A, den Blaauwen T, Carbonnelle E, Veckerlé C, Brun YV, van Nieuwenhze M, Bouchier C, Tu K, Rice LB, Arthur M. 2016. Factors essential for l, d-transpeptidase-mediated peptidoglycan cross-linking and β-lactam resistance in Escherichia coli. eLife 5:e19469 http://dx.doi.org/10.7554/eLife.19469. [PubMed]
214. Lavollay M, Arthur M, Fourgeaud M, Dubost L, Marie A, Veziris N, Blanot D, Gutmann L, Mainardi JL. 2008. The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by l, d-transpeptidation. J Bacteriol 190:4360–4366 http://dx.doi.org/10.1128/JB.00239-08. [PubMed]
215. Baranowski C, Welsh MA, Sham LT, Eskandarian HA, Lim HC, Kieser KJ, Wagner JC, McKinney JD, Fantner GE, Ioerger TR, Walker S, Bernhardt TG, Rubin EJ, Rego EH. 2018. Maturing Mycobacterium smegmatis peptidoglycan requires non-canonical crosslinks to maintain shape. eLife 7:e37516 http://dx.doi.org/10.7554/eLife.37516. [PubMed]
216. Koch AL. 1990. Additional arguments for the key role of “smart” autolysins in the enlargement of the wall of Gram-negative bacteria. Res Microbiol 141:529–541 http://dx.doi.org/10.1016/0923-2508(90)90017-K.
217. Tomasz A. 1974. The role of autolysins in cell death. Ann N Y Acad Sci 235:439–447 http://dx.doi.org/10.1111/j.1749-6632.1974.tb43282.x. [PubMed]
218. Vollmer W, Joris B, Charlier P, Foster S. 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32:259–286 http://dx.doi.org/10.1111/j.1574-6976.2007.00099.x. [PubMed]
219. Do T, Page JE, Walker S. 2020. Uncovering the activities, biological roles, and regulation of bacterial cell wall hydrolases and tailoring enzymes. J Biol Chem 295:3347–3361 http://dx.doi.org/10.1074/jbc.REV119.010155. [PubMed]
220. Heidrich C, Ursinus A, Berger J, Schwarz H, Höltje J-V. 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 http://dx.doi.org/10.1128/JB.184.22.6093-6099.2002. [PubMed]
221. Singh SK, SaiSree L, Amrutha RN, Reddy M. 2012. Three redundant murein endopeptidases catalyse an essential cleavage step in peptidoglycan synthesis of Escherichia coli K12. Mol Microbiol 86:1036–1051 http://dx.doi.org/10.1111/mmi.12058. [PubMed]
222. Chodisetti PK, Reddy M. 2019. Peptidoglycan hydrolase of an unusual cross-link cleavage specificity contributes to bacterial cell wall synthesis. Proc Natl Acad Sci USA 116:7825–7830 http://dx.doi.org/10.1073/pnas.1816893116. [PubMed]
223. Dörr T, Cava F, Lam H, Davis BM, Waldor MK. 2013. Substrate specificity of an elongation-specific peptidoglycan endopeptidase and its implications for cell wall architecture and growth of Vibrio cholerae. Mol Microbiol 89:949–962 http://dx.doi.org/10.1111/mmi.12323. [PubMed]
224. Hashimoto M, Ooiwa S, Sekiguchi J. 2012. Synthetic lethality of the lytE cwlO genotype in Bacillus subtilis is caused by lack of d, l-endopeptidase activity at the lateral cell wall. J Bacteriol 194:796–803 http://dx.doi.org/10.1128/JB.05569-11. [PubMed]
225. Ng W-L, Kazmierczak KM, Winkler ME. 2004. Defective cell wall synthesis in Streptococcus pneumoniae R6 depleted for the essential PcsB putative murein hydrolase or the VicR (YycF) response regulator. Mol Microbiol 53:1161–1175 http://dx.doi.org/10.1111/j.1365-2958.2004.04196.x. [PubMed]
226. Vestö K, Huseby DL, Snygg I, Wang H, Hughes D, Rhen M. 2018. Muramyl endopeptidase Spr contributes to intrinsic vancomycin resistance in Salmonella enterica serovar Typhimurium. Front Microbiol 9:2941 http://dx.doi.org/10.3389/fmicb.2018.02941. [PubMed]
227. Singh SK, Parveen S, SaiSree L, Reddy M. 2015. Regulated proteolysis of a cross-link-specific peptidoglycan hydrolase contributes to bacterial morphogenesis. Proc Natl Acad Sci USA 112:10956–10961 http://dx.doi.org/10.1073/pnas.1507760112. [PubMed]
228. Bisicchia P, Noone D, Lioliou E, Howell A, Quigley S, Jensen T, Jarmer H, Devine KM. 2007. The essential YycFG two-component system controls cell wall metabolism in Bacillus subtilis. Mol Microbiol 65:180–200 http://dx.doi.org/10.1111/j.1365-2958.2007.05782.x. [PubMed]
229. Dobihal GS, Brunet YR, Flores-Kim J, Rudner DZ. 2019. Homeostatic control of cell wall hydrolysis by the WalRK two-component signaling pathway in Bacillus subtilis. eLife 8:e52088 http://dx.doi.org/10.7554/eLife.52088. [PubMed]
230. Murphy SG, Alvarez L, Adams MC, Liu S, Chappie JS, Cava F, Dörr T. 2019. Endopeptidase regulation as a novel function of the Zur-dependent zinc starvation response. mBio10:e02620-18. [PubMed]
231. Vats P, Rothfield L. 2007. Duplication and segregation of the actin (MreB) cytoskeleton during the prokaryotic cell cycle. Proc Natl Acad Sci USA 104:17795–17800 http://dx.doi.org/10.1073/pnas.0708739104. [PubMed]
232. Varma A, Young KD. 2009. In Escherichia coli, MreB and FtsZ direct the synthesis of lateral cell wall via independent pathways that require PBP 2. J Bacteriol 191:3526–3533 http://dx.doi.org/10.1128/JB.01812-08. [PubMed]
233. Fenton AK, Gerdes K. 2013. Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBO J 32:1953–1965 http://dx.doi.org/10.1038/emboj.2013.129. [PubMed]
234. den Blaauwen T, Hamoen LW, Levin PA. 2017. The divisome at 25: the road ahead. Curr Opin Microbiol 36:85–94 http://dx.doi.org/10.1016/j.mib.2017.01.007. [PubMed]
235. Du S, Lutkenhaus J. 2019. At the heart of bacterial cytokinesis: the Z ring. Trends Microbiol 27:781–791 http://dx.doi.org/10.1016/j.tim.2019.04.011. [PubMed]
236. Mercer KLN, Weiss DS. 2002. The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site. J Bacteriol 184:904–912 http://dx.doi.org/10.1128/jb.184.4.904-912.2002. [PubMed]
237. Fraipont C, Alexeeva S, Wolf B, van der Ploeg R, Schloesser M, den Blaauwen T, Nguyen-Distèche M. 2011. The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli. Microbiol Read 157:251–259 http://dx.doi.org/10.1099/mic.0.040071-0. [PubMed]
238. Derouaux A, Wolf B, Fraipont C, Breukink E, Nguyen-Distèche M, Terrak M. 2008. The monofunctional glycosyltransferase of Escherichia coli localizes to the cell division site and interacts with penicillin-binding protein 3, FtsW, and FtsN. J Bacteriol 190:1831–1834 http://dx.doi.org/10.1128/JB.01377-07. [PubMed]
239. Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J, Schwarz H, de Pedro MA, Höltje JV. 2001. Involvement of N-acetylmuramyl- l-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol 41:167–178 http://dx.doi.org/10.1046/j.1365-2958.2001.02499.x. [PubMed]
240. Wang T-SA, Manning SA, Walker S, Kahne D. 2008. Isolated peptidoglycan glycosyltransferases from different organisms produce different glycan chain lengths. J Am Chem Soc 130:14068–14069 http://dx.doi.org/10.1021/ja806016y. [PubMed]
241. Höltje JV, Mirelman D, Sharon N, Schwarz U. 1975. Novel type of murein transglycosylase in Escherichia coli. J Bacteriol 124:1067–1076 http://dx.doi.org/10.1128/JB.124.3.1067-1076.1975. [PubMed]
242. Blackburn NT, Clarke AJ. 2001. Identification of four families of peptidoglycan lytic transglycosylases. J Mol Evol 52:78–84 http://dx.doi.org/10.1007/s002390010136. [PubMed]
243. Yakhnina AA, Bernhardt TG. 2020. The Tol-Pal system is required for peptidoglycan-cleaving enzymes to complete bacterial cell division. Proc Natl Acad Sci USA 117:6777–6783 http://dx.doi.org/10.1073/pnas.1919267117. [PubMed]
244. Jorgenson MA, Chen Y, Yahashiri A, Popham DL, Weiss DS. 2014. The bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod shape and daughter cell separation in Pseudomonas aeruginosa. Mol Microbiol 93:113–128 http://dx.doi.org/10.1111/mmi.12643. [PubMed]
245. Dik DA, Marous DR, Fisher JF, Mobashery S. 2017. Lytic transglycosylases: concinnity in concision of the bacterial cell wall. Crit Rev Biochem Mol Biol 52:503–542 http://dx.doi.org/10.1080/10409238.2017.1337705. [PubMed]
246. Spratt BG, Strominger JL. 1976. Identification of the major penicillin-binding proteins of Escherichia coli as d-alanine carboxypeptidase IA. J Bacteriol 127:660–663 http://dx.doi.org/10.1128/JB.127.1.660-663.1976. [PubMed]
247. Tamura T, Imae Y, Strominger JL. 1976. Purification to homogeneity and properties of two d-alanine carboxypeptidases I from Escherichia coli. J Biol Chem 251:414–423.
248. Amanuma H, Strominger JL. 1984. Purification and properties of penicillin-binding proteins 5 and 6 from the dacA mutant strain of Escherichia coli (JE 11191). J Biol Chem 259:1294–1298.
249. Baquero MR, Bouzon M, Quintela JC, Ayala JA, Moreno F. 1996. dacD, an Escherichia coli gene encoding a novel penicillin-binding protein (PBP6b) with dd-carboxypeptidase activity. J Bacteriol 178:7106–7111 http://dx.doi.org/10.1128/JB.178.24.7106-7111.1996. [PubMed]
250. Nelson DE, Young KD. 2000. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J Bacteriol 182:1714–1721 http://dx.doi.org/10.1128/JB.182.6.1714-1721.2000. [PubMed]
251. Nelson DE, Young KD. 2001. Contributions of PBP 5 and dd-carboxypeptidase penicillin binding proteins to maintenance of cell shape in Escherichia coli. J Bacteriol 183:3055–3064 http://dx.doi.org/10.1128/JB.183.10.3055-3064.2001. [PubMed]
252. Magnet S, Dubost L, Marie A, Arthur M, Gutmann L. 2008. Identification of the l, d-transpeptidases for peptidoglycan cross-linking in Escherichia coli. J Bacteriol 190:4782–4785 http://dx.doi.org/10.1128/JB.00025-08. [PubMed]
253. Lupoli TJ, Tsukamoto H, Doud EH, Wang T-SA, Walker S, Kahne D. 2011. Transpeptidase-mediated incorporation of d-amino acids into bacterial peptidoglycan. J Am Chem Soc 133:10748–10751 http://dx.doi.org/10.1021/ja2040656. [PubMed]
254. Cava F, de Pedro MA, Lam H, Davis BM, Waldor MK. 2011. Distinct pathways for modification of the bacterial cell wall by non-canonical d-amino acids. EMBO J 30:3442–3453 http://dx.doi.org/10.1038/emboj.2011.246. [PubMed]
255. Lam H, Oh D-C, Cava F, Takacs CN, Clardy J, de Pedro MA, Waldor MK. 2009. d-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552–1555 http://dx.doi.org/10.1126/science.1178123. [PubMed]
256. Mainardi J-L, Villet R, Bugg TD, Mayer C, Arthur M. 2008. Evolution of peptidoglycan biosynthesis under the selective pressure of antibiotics in Gram-positive bacteria. FEMS Microbiol Rev 32:386–408 http://dx.doi.org/10.1111/j.1574-6976.2007.00097.x. [PubMed]
257. Hernández SB, Dörr T, Waldor MK, Cava F. 2020. Modulation of peptidoglycan synthesis by recycled cell wall tetrapeptides. Cell Rep 31:107578 http://dx.doi.org/10.1016/j.celrep.2020.107578. [PubMed]
258. Aliashkevich A, Alvarez L, Cava F. 2018. New insights into the mechanisms and biological roles of d-amino acids in complex eco-systems. Front Microbiol 9:683 http://dx.doi.org/10.3389/fmicb.2018.00683. [PubMed]
259. Uehara T, Park JT. 2008. Peptidoglycan recycling. Ecosal Plus 3:3 http://dx.doi.org/10.1128/ecosalplus.4.7.1.5. [PubMed]
260. Joseleau-Petit D, Liébart J-C, Ayala JA, D’Ari R. 2007. Unstable Escherichia coli L forms revisited: growth requires peptidoglycan synthesis. J Bacteriol 189:6512–6520 http://dx.doi.org/10.1128/JB.00273-07. [PubMed]
261. Ranjit DK, Young KD. 2013. The Rcs stress response and accessory envelope proteins are required for de novo generation of cell shape in Escherichia coli. J Bacteriol 195:2452–2462 http://dx.doi.org/10.1128/JB.00160-13. [PubMed]
262. Kawai Y, Mercier R, Errington J. 2014. Bacterial cell morphogenesis does not require a preexisting template structure. Curr Biol 24:863–867 http://dx.doi.org/10.1016/j.cub.2014.02.053. [PubMed]
263. Lederberg J, St Clair J. 1958. Protoplasts and L-type growth of Escherichia coli. J Bacteriol 75:143–160 http://dx.doi.org/10.1128/JB.75.2.143-160.1958. [PubMed]
264. Allan EJ, Hoischen C, Gumpert J. 2009. Bacterial L-forms. Adv Appl Microbiol 68:1–39.
265. Klieneberger E. 1935. The natural occurrence of pleuropneumonia-like organism in apparent symbiosis with Streptobacillus moniliformis and other bacteria. J Pathol Bacteriol 40:93–105 http://dx.doi.org/10.1002/path.1700400108.
266. Errington J. 2013. L-form bacteria, cell walls and the origins of life. Open Biol 3:120143 http://dx.doi.org/10.1098/rsob.120143. [PubMed]
267. Mercier R, Kawai Y, Errington J. 2013. Excess membrane synthesis drives a primitive mode of cell proliferation. Cell 152:997–1007 http://dx.doi.org/10.1016/j.cell.2013.01.043. [PubMed]
268. Leaver M, Domínguez-Cuevas P, Coxhead JM, Daniel RA, Errington J. 2009. Life without a wall or division machine in Bacillus subtilis. Nature 457:849–853 http://dx.doi.org/10.1038/nature07742. [PubMed]
269. Mercier R, Kawai Y, Errington J. 2016. Wall proficient E. coli capable of sustained growth in the absence of the Z-ring division machine. Nat Microbiol 1:16091 http://dx.doi.org/10.1038/nmicrobiol.2016.91. [PubMed]
270. Errington J. 2017. Cell wall-deficient, L-form bacteria in the 21st century: a personal perspective. Biochem Soc Trans 45:287–295 http://dx.doi.org/10.1042/BST20160435. [PubMed]
271. Young KD. 2007. Reforming L forms: they need part of a wall after all? J Bacteriol 189:6509–6511 http://dx.doi.org/10.1128/JB.01035-07. [PubMed]
272. Urban JH, Papenfort K, Thomsen J, Schmitz RA, Vogel J. 2007. A conserved small RNA promotes discoordinate expression of the glmUS operon mRNA to activate GlmS synthesis. J Mol Biol 373:521–528 http://dx.doi.org/10.1016/j.jmb.2007.07.035. [PubMed]
273. Kalamorz F, Reichenbach B, März W, Rak B, Görke B. 2007. Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli. Mol Microbiol 65:1518–1533 http://dx.doi.org/10.1111/j.1365-2958.2007.05888.x. [PubMed]
274. Reichenbach B, Maes A, Kalamorz F, Hajnsdorf E, Görke B. 2008. The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli. Nucleic Acids Res 36:2570–2580 http://dx.doi.org/10.1093/nar/gkn091. [PubMed]
275. Göpel Y, Papenfort K, Reichenbach B, Vogel J, Görke B. 2013. Targeted decay of a regulatory small RNA by an adaptor protein for RNase E and counteraction by an anti-adaptor RNA. Genes Dev 27:552–564 http://dx.doi.org/10.1101/gad.210112.112. [PubMed]
276. Göpel Y, Khan MA, Görke B. 2014. Ménage à trois: post-transcriptional control of the key enzyme for cell envelope synthesis by a base-pairing small RNA, an RNase adaptor protein, and a small RNA mimic. RNA Biol 11:433–442 http://dx.doi.org/10.4161/rna.28301. [PubMed]
277. Urban JH, Vogel J. 2008. Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6:e64 http://dx.doi.org/10.1371/journal.pbio.0060064. [PubMed]
278. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. 2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281–286 http://dx.doi.org/10.1038/nature02362. [PubMed]
279. Plumbridge J. 1995. Co-ordinated regulation of amino sugar biosynthesis and degradation: the NagC repressor acts as both an activator and a repressor for the transcription of the glmUS operon and requires two separated NagC binding sites. EMBO J 14:3958–3965 http://dx.doi.org/10.1002/j.1460-2075.1995.tb00067.x. [PubMed]
280. Mizyed S, Oddone A, Byczynski B, Hughes DW, Berti PJ. 2005. UDP- N-acetylmuramic acid (UDP-MurNAc) is a potent inhibitor of MurA (enolpyruvyl-UDP-GlcNAc synthase). Biochemistry 44:4011–4017 http://dx.doi.org/10.1021/bi047704w. [PubMed]
281. Vollmer W. 2012. Bacterial growth does require peptidoglycan hydrolases. Mol Microbiol 86:1031–1035 http://dx.doi.org/10.1111/mmi.12059. [PubMed]
282. Lee TK, Huang KC. 2013. The role of hydrolases in bacterial cell-wall growth. Curr Opin Microbiol 16:760–766 http://dx.doi.org/10.1016/j.mib.2013.08.005. [PubMed]
283. Wheeler R, Turner RD, Bailey RG, Salamaga B, Mesnage S, Mohamad SAS, Hayhurst EJ, Horsburgh M, Hobbs JK, Foster SJ. 2015. Bacterial cell enlargement requires control of cell wall stiffness mediated by peptidoglycan hydrolases. MBio 6:e00660-15 http://dx.doi.org/10.1128/mBio.00660-15. [PubMed]
284. Su M-Y, Som N, Wu C-Y, Su S-C, Kuo Y-T, Ke L-C, Ho M-R, Tzeng S-R, Teng C-H, Mengin-Lecreulx D, Reddy M, Chang C-I. 2017. Structural basis of adaptor-mediated protein degradation by the tail-specific PDZ-protease Prc. Nat Commun 8:1516 http://dx.doi.org/10.1038/s41467-017-01697-9. [PubMed]
285. Srivastava D, Seo J, Rimal B, Kim SJ, Zhen S, Darwin AJ. 2018. A proteolytic complex targets multiple cell wall hydrolases in Pseudomonas aeruginosa. MBio 9:e00972-18 http://dx.doi.org/10.1128/mBio.00972-18. [PubMed]
286. Shin J-H, Sulpizio AG, Kelley A, Alvarez L, Murphy SG, Fan L, Cava F, Mao Y, Saper MA, Dörr T. 2020. Structural basis of peptidoglycan endopeptidase regulation. Proc Natl Acad Sci USA 117:11692–11702 http://dx.doi.org/10.1073/pnas.2001661117. [PubMed]
287. Hsu P-C, Chen C-S, Wang S, Hashimoto M, Huang W-C, Teng C-H. 2020. Identification of MltG as a Prc protease substrate whose dysregulation contributes to the conditional growth defect of Prc-deficient Escherichia coli. Front Microbiol 11:2000 http://dx.doi.org/10.3389/fmicb.2020.02000. [PubMed]
288. Hara H, Nishimura Y, Kato J, Suzuki H, Nagasawa H, Suzuki A, Hirota Y. 1989. Genetic analyses of processing involving C-terminal cleavage in penicillin-binding protein 3 of Escherichia coli. J Bacteriol 171:5882–5889 http://dx.doi.org/10.1128/JB.171.11.5882-5889.1989. [PubMed]
289. Banzhaf M, Yau HC, Verheul J, Lodge A, Kritikos G, Mateus A, Cordier B, Hov AK, Stein F, Wartel M, Pazos M, Solovyova AS, Breukink E, van Teeffelen S, Savitski MM, den Blaauwen T, Typas A, Vollmer W. 2020. Outer membrane lipoprotein NlpI scaffolds peptidoglycan hydrolases within multi-enzyme complexes in Escherichia coli. EMBO J 39:e102246 http://dx.doi.org/10.15252/embj.2019102246. [PubMed]
290. Meisner J, Montero Llopis P, Sham L-T, Garner E, Bernhardt TG, Rudner DZ. 2013. FtsEX is required for CwlO peptidoglycan hydrolase activity during cell wall elongation in Bacillus subtilis. Mol Microbiol 89:1069–1083 http://dx.doi.org/10.1111/mmi.12330. [PubMed]
291. Mavrici D, Marakalala MJ, Holton JM, Prigozhin DM, Gee CL, Zhang YJ, Rubin EJ, Alber T. 2014. Mycobacterium tuberculosis FtsX extracellular domain activates the peptidoglycan hydrolase, RipC. Proc Natl Acad Sci USA 111:8037–8042 http://dx.doi.org/10.1073/pnas.1321812111. [PubMed]
292. Sham L-T, Barendt SM, Kopecky KE, Winkler ME. 2011. Essential PcsB putative peptidoglycan hydrolase interacts with the essential FtsX Spn cell division protein in Streptococcus pneumoniae D39. Proc Natl Acad Sci USA 108:E1061–E1069 http://dx.doi.org/10.1073/pnas.1108323108. [PubMed]
293. Carballido-López R, Formstone A, Li Y, Ehrlich SD, Noirot P, Errington J. 2006. Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11:399–409 http://dx.doi.org/10.1016/j.devcel.2006.07.017. [PubMed]
294. Patel Y, Zhao H, Helmann JD. 2020. A regulatory pathway that selectively up-regulates elongasome function in the absence of class A PBPs. eLife 9:e57902 http://dx.doi.org/10.7554/eLife.57902. [PubMed]
295. Guinote IB, Moreira RN, Barahona S, Freire P, Vicente M, Arraiano CM. 2014. Breaking through the stress barrier: the role of BolA in Gram-negative survival. World J Microbiol Biotechnol 30:2559–2566 http://dx.doi.org/10.1007/s11274-014-1702-4. [PubMed]
296. Santos JM, Lobo M, Matos APA, De Pedro MA, Arraiano CM. 2002. The gene bolA regulates dacA (PBP5), dacC (PBP6) and ampC (AmpC), promoting normal morphology in Escherichia coli. Mol Microbiol 45:1729–1740 http://dx.doi.org/10.1046/j.1365-2958.2002.03131.x. [PubMed]
297. Lange R, Hengge-Aronis R. 1991. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J Bacteriol 173:4474–4481 http://dx.doi.org/10.1128/JB.173.14.4474-4481.1991. [PubMed]
298. Freire P, Moreira RN, Arraiano CM. 2009. BolA inhibits cell elongation and regulates MreB expression levels. J Mol Biol 385:1345–1351 http://dx.doi.org/10.1016/j.jmb.2008.12.026. [PubMed]
299. Delhaye A, Collet J-F, Laloux G. 2019. A fly on the wall: how stress response systems can sense and respond to damage to peptidoglycan. Front Cell Infect Microbiol 9:380 http://dx.doi.org/10.3389/fcimb.2019.00380. [PubMed]
300. Macritchie DM, Raivio TL. 2009. Envelope stress responses. Ecosal Plus 2009. doi:10.1128/ecosalplus.5.4.7. http://dx.doi.org/10.1128/ecosalplus.5.4.7. [PubMed]
301. Grabowicz M, Silhavy TJ. 2017. Redefining the essential trafficking pathway for outer membrane lipoproteins. Proc Natl Acad Sci USA 114:4769–4774 http://dx.doi.org/10.1073/pnas.1702248114. [PubMed]
302. Sailer FC, Meberg BM, Young KD. 2003. β-Lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol Lett 226:245–249 http://dx.doi.org/10.1016/S0378-1097(03)00616-5.
303. Ize B, Porcelli I, Lucchini S, Hinton JC, Berks BC, Palmer T. 2004. Novel phenotypes of Escherichia coli tat mutants revealed by global gene expression and phenotypic analysis. J Biol Chem 279:47543–47554 http://dx.doi.org/10.1074/jbc.M406910200. [PubMed]
304. Laubacher ME, Ades SE. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J Bacteriol 190:2065–2074 http://dx.doi.org/10.1128/JB.01740-07. [PubMed]
305. Bury-Moné S, Nomane Y, Reymond N, Barbet R, Jacquet E, Imbeaud S, Jacq A, Bouloc P. 2009. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5:e1000651 http://dx.doi.org/10.1371/journal.pgen.1000651. [PubMed]
306. Ferrières L, Clarke DJ. 2003. The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol Microbiol 50:1665–1682 http://dx.doi.org/10.1046/j.1365-2958.2003.03815.x. [PubMed]
307. Carballès F, Bertrand C, Bouché JP, Cam K. 1999. Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol 34:442–450 http://dx.doi.org/10.1046/j.1365-2958.1999.01605.x. [PubMed]
308. Evans KL, Kannan S, Li G, de Pedro MA, Young KD. 2013. Eliminating a set of four penicillin binding proteins triggers the Rcs phosphorelay and Cpx stress responses in Escherichia coli. J Bacteriol 195:4415–4424 http://dx.doi.org/10.1128/JB.00596-13. [PubMed]
309. Raivio TL, Leblanc SKD, Price NL. 2013. The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. J Bacteriol 195:2755–2767 http://dx.doi.org/10.1128/JB.00105-13. [PubMed]
310. Lonergan ZR, Nairn BL, Wang J, Hsu YP, Hesse LE, Beavers WN, Chazin WJ, Trinidad JC, VanNieuwenhze MS, Giedroc DP, Skaar EP. 2019. An Acinetobacter baumannii, zinc-regulated peptidase maintains cell wall integrity during immune-mediated nutrient sequestration. Cell Rep 26:2009–2018.e6 http://dx.doi.org/10.1016/j.celrep.2019.01.089. [PubMed]
311. Höltje J-V. 1993. “Three for one”: a simple growth mechanism that guarantees a precise copy of the thin, rod-shaped murein sacculus of Escherichia coli, p 419–426. In de Pedro MA, Höltje J-V, Löffelhardt W (ed), Bacterial growth and lysis: metabolism and structure of the bacterial sacculus. Springer US, Boston, MA.
312. Park JT. 1996. The murein sacculus, p 48–57. In Neidhardt FC (ed), Escherichia coli and Salmonella. ASM Press, Washington, DC.
313. Tomasz A. 1984. Building and breaking of bonds in the cell wall of bacteria: the role for autolysins, p 3–12. In Nombela C (ed), Microbial cell wall synthesis and autolysis. Elsevier, Amsterdam, The Netherlands.
314. Koch AL. 1998. The three-for-one model for Gram-negative wall growth: a problem and a possible solution. FEMS Microbiol Lett 162:127–134 http://dx.doi.org/10.1111/j.1574-6968.1998.tb12989.x. [PubMed]
315. Lee TK, Meng K, Shi H, Huang KC. 2016. Single-molecule imaging reveals modulation of cell wall synthesis dynamics in live bacterial cells. Nat Commun 7:13170 http://dx.doi.org/10.1038/ncomms13170. [PubMed]
316. den Blaauwen T, Luirink J. 2019. Checks and balances in bacterial cell division. MBio 10:e00149-19 http://dx.doi.org/10.1128/mBio.00149-19. [PubMed]
317. Hirano T, Tanidokoro K, Shimizu Y, Kawarabayasi Y, Ohshima T, Sato M, Tadano S, Ishikawa H, Takio S, Takechi K, Takano H. 2016. Moss chloroplasts are surrounded by a peptidoglycan wall containing d-amino acids. Plant Cell 28:1521–1532. [PubMed]
318. Kiefel BR, Gilson PR, Beech PL. 2004. Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. Protist 155:105–115 http://dx.doi.org/10.1078/1434461000168. [PubMed]
319. Leger MM, Petrů M, Žárský V, Eme L, Vlček Č, Harding T, Lang BF, Eliáš M, Doležal P, Roger AJ. 2015. An ancestral bacterial division system is widespread in eukaryotic mitochondria. Proc Natl Acad Sci USA 112:10239–10246 http://dx.doi.org/10.1073/pnas.1421392112.
320. Irazoki O, Hernandez SB, Cava F. 2019. Peptidoglycan muropeptides: release, perception, and functions as signaling molecules. Front Microbiol 10:500 http://dx.doi.org/10.3389/fmicb.2019.00500. [PubMed]
321. Rangan KJ, Pedicord VA, Wang Y-C, Kim B, Lu Y, Shaham S, Mucida D, Hang HC. 2016. A secreted bacterial peptidoglycan hydrolase enhances tolerance to enteric pathogens. Science 353:1434–1437 http://dx.doi.org/10.1126/science.aaf3552. [PubMed]
322. Rine J, Hansen W, Hardeman E, Davis RW. 1983. Targeted selection of recombinant clones through gene dosage effects. Proc Natl Acad Sci USA 80:6750–6754 http://dx.doi.org/10.1073/pnas.80.22.6750. [PubMed]
323. Culp EJ, Waglechner N, Wang W, Fiebig-Comyn AA, Hsu Y-P, Koteva K, Sychantha D, Coombes BK, Van Nieuwenhze MS, Brun YV, Wright GD. 2020. Evolution-guided discovery of antibiotics that inhibit peptidoglycan remodelling. Nature 578:582–587 http://dx.doi.org/10.1038/s41586-020-1990-9. [PubMed]
324. Shukla R, Medeiros-Silva J, Parmar A, Vermeulen BJA, Das S, Paioni AL, Jekhmane S, Lorent J, Bonvin AMJJ, Baldus M, Lelli M, Veldhuizen EJA, Breukink E, Singh I, Weingarth M. 2020. Mode of action of teixobactins in cellular membranes. Nat Commun 11:2848 http://dx.doi.org/10.1038/s41467-020-16600-2. [PubMed]
325. Touzé T, Barreteau H, El Ghachi M, Bouhss A, Barnéoud-Arnoulet A, Patin D, Sacco E, Blanot D, Arthur M, Duché D, Lloubès R, Mengin-Lecreulx D. 2012. Colicin M, a peptidoglycan lipid-II-degrading enzyme: potential use for antibacterial means? Biochem Soc Trans 40:1522–1527 http://dx.doi.org/10.1042/BST20120189. [PubMed]
326. Fung-Tomc JC, Lincourt W, Thater C, Kessler RE. 1988. Comparison of the inhibitory and bactericidal activity of aztreonam and amikacin against Gram negative aerobic bacilli. Ann Clin Lab Sci 18:463–467.
327. Brown K, Pompeo F, Dixon S, Mengin-Lecreulx D, Cambillau C, Bourne Y. 1999. Crystal structure of the bifunctional N-acetylglucosamine 1-phosphate uridyltransferase from Escherichia coli: a paradigm for the related pyrophosphorylase superfamily. EMBO J 18:4096–4107 http://dx.doi.org/10.1093/emboj/18.15.4096. [PubMed]
328. Liger D, Blanot D, van Heijenoort J. 1991. Effect of various alanine analogues on the l-alanine-adding enzyme from Escherichia coli. FEMS Microbiol Lett 64:111–115 http://dx.doi.org/10.1016/0378-1097(91)90218-Y.
329. Uehara T, Park JT. 2007. An anhydro- N-acetylmuramyl- l-alanine amidase with broad specificity tethered to the outer membrane of Escherichia coli. J Bacteriol 189:5634–5641 http://dx.doi.org/10.1128/JB.00446-07. [PubMed]
330. Dietz H, Pfeifle D, Wiedemann B. 1996. Location of N-acetylmuramyl- l-alanyl- d-glutamylmesodiaminopimelic acid, presumed signal molecule for beta-lactamase induction, in the bacterial cell. Antimicrob Agents Chemother 40:2173–2177 http://dx.doi.org/10.1128/AAC.40.9.2173. [PubMed]
331. Jacobs C, Huang LJ, Bartowsky E, Normark S, Park JT. 1994. Bacterial cell wall recycling provides cytosolic muropeptides as effectors for beta-lactamase induction. EMBO J 13:4684–4694 http://dx.doi.org/10.1002/j.1460-2075.1994.tb06792.x. [PubMed]
332. Templin MF, Ursinus A, Höltje JV. 1999. A defect in cell wall recycling triggers autolysis during the stationary growth phase of Escherichia coli. EMBO J 18:4108–4117 http://dx.doi.org/10.1093/emboj/18.15.4108. [PubMed]
333. Lessard IAD, Walsh CT. 1999. VanX, a bacterial d-alanyl- d-alanine dipeptidase: resistance, immunity, or survival function? Proc Natl Acad Sci USA 96:11028–11032 http://dx.doi.org/10.1073/pnas.96.20.11028.
334. Cheng Q, Li H, Merdek K, Park JT. 2000. Molecular characterization of the beta- N-acetylglucosaminidase of Escherichia coli and its role in cell wall recycling. J Bacteriol 182:4836–4840 http://dx.doi.org/10.1128/JB.182.17.4836-4840.2000. [PubMed]
335. Uehara T, Park JT. 2003. Identification of MpaA, an amidase in Escherichia coli that hydrolyzes the gamma- d-glutamyl-meso-diaminopimelate bond in murein peptides. J Bacteriol 185:679–682 http://dx.doi.org/10.1128/JB.185.2.679-682.2003. [PubMed]
336. Choi U, Park Y-H, Kim Y-R, Seok Y-J, Lee C-R. 2016. Increased expression of genes involved in uptake and degradation of murein tripeptide under nitrogen starvation in Escherichia coli. FEMS Microbiol Lett 363:363 http://dx.doi.org/10.1093/femsle/fnw136. [PubMed]
337. Schmidt DM, Hubbard BK, Gerlt JA. 2001. Evolution of enzymatic activities in the enolase superfamily: functional assignment of unknown proteins in Bacillus subtilis and Escherichia coli as l-Ala- d/ l-Glu epimerases. Biochemistry 40:15707–15715 http://dx.doi.org/10.1021/bi011640x. [PubMed]
338. Peters K, Pazos M, Edoo Z, Hugonnet J-E, Martorana AM, Polissi A, VanNieuwenhze MS, Arthur M, Vollmer W. 2018. Copper inhibits peptidoglycan ld-transpeptidases suppressing β-lactam resistance due to bypass of penicillin-binding proteins. Proc Natl Acad Sci USA 115:10786–10791 http://dx.doi.org/10.1073/pnas.1809285115. [PubMed]
339. van Heijenoort J. 2011. Peptidoglycan hydrolases of Escherichia coli. Microbiol Mol Biol Rev 75:636–663 http://dx.doi.org/10.1128/MMBR.00022-11. [PubMed]
340. Clarke TB, Kawai F, Park S-Y, Tame JRH, Dowson CG, Roper DI. 2009. Mutational analysis of the substrate specificity of Escherichia coli penicillin binding protein 4. Biochemistry 48:2675–2683 http://dx.doi.org/10.1021/bi801993x. [PubMed]
341. Peters K, Kannan S, Rao VA, Biboy J, Vollmer D, Erickson SW, Lewis RJ, Young KD, Vollmer W. 2016. The redundancy of peptidoglycan carboxypeptidases ensures robust cell shape maintenance in Escherichia coli. MBio 7:e00819-16 http://dx.doi.org/10.1128/mBio.00819-16. [PubMed]
342. Romeis T, Höltje JV. 1994. Penicillin-binding protein 7/8 of Escherichia coli is a dd-endopeptidase. Eur J Biochem 224:597–604 http://dx.doi.org/10.1111/j.1432-1033.1994.00597.x. [PubMed]
343. González-Leiza SM, de Pedro MA, Ayala JA. 2011. AmpH, a bifunctional dd-endopeptidase and dd-carboxypeptidase of Escherichia coli. J Bacteriol 193:6887–6894 http://dx.doi.org/10.1128/JB.05764-11. [PubMed]
344. Marcyjaniak M, Odintsov SG, Sabala I, Bochtler M. 2004. Peptidoglycan amidase MepA is a LAS metallopeptidase. J Biol Chem 279:43982–43989 http://dx.doi.org/10.1074/jbc.M406735200. [PubMed]
345. Silber KR, Keiler KC, Sauer RT. 1992. Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini. Proc Natl Acad Sci USA 89:295–299 http://dx.doi.org/10.1073/pnas.89.1.295. [PubMed]
346. Cader MZ, Boroviak K, Zhang Q, Assadi G, Kempster SL, Sewell GW, Saveljeva S, Ashcroft JW, Clare S, Mukhopadhyay S, Brown KP, Tschurtschenthaler M, Raine T, Doe B, Chilvers ER, Griffin JL, Kaneider NC, Floto RA, D’Amato M, Bradley A, Wakelam MJ, Dougan G, Kaser A. 2016. C13orf31 (FAMIN) is a central regulator of immunometabolic function. Nat Immunol 17:1046–1056 http://dx.doi.org/10.1038/ni.3532. [PubMed]
Loading

Article metrics loading...

/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0010-2020
2021-01-20
2021-05-14

Abstract:

Peptidoglycan is a defining feature of the bacterial cell wall. Initially identified as a target of the revolutionary beta-lactam antibiotics, peptidoglycan has become a subject of much interest for its biology, its potential for the discovery of novel antibiotic targets, and its role in infection. Peptidoglycan is a large polymer that forms a mesh-like scaffold around the bacterial cytoplasmic membrane. Peptidoglycan synthesis is vital at several stages of the bacterial cell cycle: for expansion of the scaffold during cell elongation and for formation of a septum during cell division. It is a complex multifactorial process that includes formation of monomeric precursors in the cytoplasm, their transport to the periplasm, and polymerization to form a functional peptidoglycan sacculus. These processes require spatio-temporal regulation for successful assembly of a robust sacculus to protect the cell from turgor and determine cell shape. A century of research has uncovered the fundamentals of peptidoglycan biology, and recent studies employing advanced technologies have shed new light on the molecular interactions that govern peptidoglycan synthesis. Here, we describe the peptidoglycan structure, synthesis, and regulation in rod-shaped bacteria, particularly , with a few examples from and other diverse organisms. We focus on the pathway of peptidoglycan sacculus elongation, with special emphasis on discoveries of the past decade that have shaped our understanding of peptidoglycan biology.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/ecosalplus/9/2/ESP-0010-2020.html?itemId=/content/journal/ecosalplus/10.1128/ecosalplus.ESP-0010-2020&mimeType=html&fmt=ahah
Comment has been disabled for this content
Submit comment
Close
Comment moderation successfully completed

Figures

Peptidoglycan: Structure, Synthesis, and Regulation
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-1,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-1,properties={foaf_givenname=Shambhavi, foaf_name=Shambhavi Garde, foaf_surname=Garde, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff1],com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-2,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-2,properties={foaf_givenname=Pavan Kumar, foaf_name=Pavan Kumar Chodisetti, foaf_surname=Chodisetti, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff3],com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-3,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-3,properties={foaf_givenname=Manjula, foaf_name=Manjula Reddy, foaf_surname=Reddy, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff5]]}]]
Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.fig1
Figure 1
The figure depicts a few important discoveries pertaining to peptidoglycan structure and synthesis from the past century. Selected significant developments of the past decade are highlighted.
ecosalplus/9/2/ESP-0010-2020_fig_001_thmb.gif
ecosalplus/9/2/ESP-0010-2020_fig_001.gif
Image of Figure 1

Click to view

Figure 1

The figure depicts a few important discoveries pertaining to peptidoglycan structure and synthesis from the past century. Selected significant developments of the past decade are highlighted.

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.fig2
Figure 2
(Top) Schematic of a rod-shaped cell with its peptidoglycan sacculus (blue mesh) located between the OM and IM. (Bottom) The zoomed-in rectangle depicts the composition of peptidoglycan. Glycan chains are made up of repeating disaccharide units of -acetylglucosamine (GlcNAc; gray hexagons) and -acetylmuramic acid (MurNAc; blue hexagons) with the peptide chains made up of amino acid residues (shaded blue circles), -alanine (-ala), -glutamic acid (-glu), meso-diaminopimelic acid (mDAP), and -alanine (-ala)–-ala. The glycan chains are linked to each other through peptide cross-linking between either -ala and mDAP or mDAP and mDAP residues to form a net-like sacculus. An OM lipoprotein (Braun’s lipoprotein, Lpp; orange helix) covalently tethers peptidoglycan to the OM. A GlcNAc-MurNAc pentapeptide is a single monomeric unit of peptidoglycan that is polymerized to form the functional sacculus. The terminal -ala is usually removed in the mature peptidoglycan.
ecosalplus/9/2/ESP-0010-2020_fig_002_thmb.gif
ecosalplus/9/2/ESP-0010-2020_fig_002.gif
Image of Figure 2

Click to view

Figure 2

(Top) Schematic of a rod-shaped cell with its peptidoglycan sacculus (blue mesh) located between the OM and IM. (Bottom) The zoomed-in rectangle depicts the composition of peptidoglycan. Glycan chains are made up of repeating disaccharide units of -acetylglucosamine (GlcNAc; gray hexagons) and -acetylmuramic acid (MurNAc; blue hexagons) with the peptide chains made up of amino acid residues (shaded blue circles), -alanine (-ala), -glutamic acid (-glu), meso-diaminopimelic acid (mDAP), and -alanine (-ala)–-ala. The glycan chains are linked to each other through peptide cross-linking between either -ala and mDAP or mDAP and mDAP residues to form a net-like sacculus. An OM lipoprotein (Braun’s lipoprotein, Lpp; orange helix) covalently tethers peptidoglycan to the OM. A GlcNAc-MurNAc pentapeptide is a single monomeric unit of peptidoglycan that is polymerized to form the functional sacculus. The terminal -ala is usually removed in the mature peptidoglycan.

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.fig3
Figure 3
Bacteria grown with HADA (emission maximum, 450 nm) are visualized as described previously ( 73 , 74 ). Zones of fluorescence represent the sites of active peptidoglycan synthesis. Predominantly sidewall and septal peptidoglycan synthesis is observed in , Typhimurium, and . In and , peptidoglycan synthesis is seen at a single pole. Scale bar = 5 µm. (Image courtesy of Michael VanNieuwenhze, Yves Brun, and Erkin Kuru).
ecosalplus/9/2/ESP-0010-2020_fig_003_thmb.gif
ecosalplus/9/2/ESP-0010-2020_fig_003.gif
Image of Figure 3

Click to view

Figure 3

Bacteria grown with HADA (emission maximum, 450 nm) are visualized as described previously ( 73 , 74 ). Zones of fluorescence represent the sites of active peptidoglycan synthesis. Predominantly sidewall and septal peptidoglycan synthesis is observed in , Typhimurium, and . In and , peptidoglycan synthesis is seen at a single pole. Scale bar = 5 µm. (Image courtesy of Michael VanNieuwenhze, Yves Brun, and Erkin Kuru).

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.fig4
Figure 4
Peptidoglycan precursors are synthesized in the cytoplasm by a series of enzymes, MurA, B, C, D, E, and F, that convert UDP-GlcNAc to form UDP-MurNAc-pentapeptide (also referred to as Park’s nucleotide), which is subsequently attached to the lipid transporter (undecaprenyl phosphate; C55P) by MraY to yield lipid-I that is converted to the final peptidoglycan precursor lipid-II, by addition of a GlcNAc moiety by MurG. A flippase MurJ transports lipid-II across the IM to the periplasm. Lipid-II is polymerized into the peptidoglycan by synthases, with C55P being recycled to the cytoplasm. TGase activity of RodA, FtsW, PBP1a, PBP1b, and MtgA catalyzes glycan polymerization, whereas TPase activity of PBP2, PBP3, PBP1a, and PBP1b contributes to peptide cross-link formation (refer to Box 1 ). Hydrolysis mediated by ,-endopeptidases, MepS, -M, and -H leads to cleavage of existing peptide cross-links to make space for the incorporation of nascent glycan strands. Anh-MurNAc (green hexagon) is the terminal residue in a glycan strand. The gray arrow indicates the direction of synthesis.
ecosalplus/9/2/ESP-0010-2020_fig_004_thmb.gif
ecosalplus/9/2/ESP-0010-2020_fig_004.gif
Image of Figure 4

Click to view

Figure 4

Peptidoglycan precursors are synthesized in the cytoplasm by a series of enzymes, MurA, B, C, D, E, and F, that convert UDP-GlcNAc to form UDP-MurNAc-pentapeptide (also referred to as Park’s nucleotide), which is subsequently attached to the lipid transporter (undecaprenyl phosphate; C55P) by MraY to yield lipid-I that is converted to the final peptidoglycan precursor lipid-II, by addition of a GlcNAc moiety by MurG. A flippase MurJ transports lipid-II across the IM to the periplasm. Lipid-II is polymerized into the peptidoglycan by synthases, with C55P being recycled to the cytoplasm. TGase activity of RodA, FtsW, PBP1a, PBP1b, and MtgA catalyzes glycan polymerization, whereas TPase activity of PBP2, PBP3, PBP1a, and PBP1b contributes to peptide cross-link formation (refer to Box 1 ). Hydrolysis mediated by ,-endopeptidases, MepS, -M, and -H leads to cleavage of existing peptide cross-links to make space for the incorporation of nascent glycan strands. Anh-MurNAc (green hexagon) is the terminal residue in a glycan strand. The gray arrow indicates the direction of synthesis.

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.fig5
Figure 5
(A) Schematic representation of elongation synthesis in a rod-shaped cell. The Rod complex (green circle) moves in helical fashion (purple) and synthesizes a scaffold, and aPBP-Lpos (orange dots) move in a diffusive manner (irregular blue lines) to fill the gaps, acting in concert to make a functional peptidoglycan sacculus. (B) Factors required for peptidoglycan elongation. Rod complex/elongasome is a multiprotein complex consisting of RodA, PBP2, RodZ, and MreBCD. The peptidoglycan synthase pair RodA-PBP2, guided by the MreBCD-RodZ complex, makes the peptidoglycan scaffold (red strands) around the cytoplasmic membrane. RodZ connects RodA-PBP2 with the cytoskeletal MreBCD to form the Rod complex, which moves circumferentially in the direction of peptidoglycan synthesis to form the scaffold (as shown in panel A). IM-localized PBP1a and PBP1b are activated by cognate OM lipoproteins LpoA and LpoB to complete the sidewall synthesis (black strands). LpoA and LpoB may traverse through the gaps in the peptidoglycan layer to interact and activate PBP1a and PBP1b. The activity of the major elongation-specific endopeptidase MepS may create space/gaps for interaction of aPBP-Lpo factors and to make space for incorporation of nascent peptidoglycan strands. MepS activity is kept in check by regulated proteolysis through its interaction with an adapter protein, NlpI, which brings the soluble periplasmic protease Prc. Nevertheless, the signal(s) that triggers sacculus expansion is not yet understood.
ecosalplus/9/2/ESP-0010-2020_fig_005_thmb.gif
ecosalplus/9/2/ESP-0010-2020_fig_005.gif
Image of Figure 5

Click to view

Figure 5

(A) Schematic representation of elongation synthesis in a rod-shaped cell. The Rod complex (green circle) moves in helical fashion (purple) and synthesizes a scaffold, and aPBP-Lpos (orange dots) move in a diffusive manner (irregular blue lines) to fill the gaps, acting in concert to make a functional peptidoglycan sacculus. (B) Factors required for peptidoglycan elongation. Rod complex/elongasome is a multiprotein complex consisting of RodA, PBP2, RodZ, and MreBCD. The peptidoglycan synthase pair RodA-PBP2, guided by the MreBCD-RodZ complex, makes the peptidoglycan scaffold (red strands) around the cytoplasmic membrane. RodZ connects RodA-PBP2 with the cytoskeletal MreBCD to form the Rod complex, which moves circumferentially in the direction of peptidoglycan synthesis to form the scaffold (as shown in panel A). IM-localized PBP1a and PBP1b are activated by cognate OM lipoproteins LpoA and LpoB to complete the sidewall synthesis (black strands). LpoA and LpoB may traverse through the gaps in the peptidoglycan layer to interact and activate PBP1a and PBP1b. The activity of the major elongation-specific endopeptidase MepS may create space/gaps for interaction of aPBP-Lpo factors and to make space for incorporation of nascent peptidoglycan strands. MepS activity is kept in check by regulated proteolysis through its interaction with an adapter protein, NlpI, which brings the soluble periplasmic protease Prc. Nevertheless, the signal(s) that triggers sacculus expansion is not yet understood.

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Peptidoglycan: Structure, Synthesis, and Regulation
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-1,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-1,properties={foaf_givenname=Shambhavi, foaf_name=Shambhavi Garde, foaf_surname=Garde, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff1],com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-2,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-2,properties={foaf_givenname=Pavan Kumar, foaf_name=Pavan Kumar Chodisetti, foaf_surname=Chodisetti, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff3],com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff4]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-3,webId=/content/author/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-3,properties={foaf_givenname=Manjula, foaf_name=Manjula Reddy, foaf_surname=Reddy, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/ecosalplus/10.1128/ecosalplus.ESP-0010-2020-aff5]]}]]
Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.T1
Table 1
Inhibitors of peptidoglycan synthesis
Generic image for table

Click to view

Table 1

Inhibitors of peptidoglycan synthesis

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.T2
Table 2
Genes involved in cytosolic peptidoglycan precursor synthesis and turnover in
Generic image for table

Click to view

Table 2

Genes involved in cytosolic peptidoglycan precursor synthesis and turnover in

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020
/content/ecosalplus/10.1128/ecosalplus.ESP-0010-2020.T3
Table 3
Proteins involved in peptidoglycan synthesis in the periplasm
Generic image for table

Click to view

Table 3

Proteins involved in peptidoglycan synthesis in the periplasm

Citation: Garde S, Chodisetti P, Reddy M. 2021. Peptidoglycan: Structure, Synthesis, and Regulation, EcoSal Plus 2021; doi:10.1128/ecosalplus.ESP-0010-2020

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error