Abstract
The peptidoglycan sacculus is a net-like polymer that surrounds the cytoplasmic membrane in most bacteria. It is essential to maintain the bacterial cell shape and protect from turgor. The peptidoglycan has a basic composition, common to all bacteria, with species-specific variations that can modify its biophysical properties or the pathogenicity of the bacteria. The synthesis of peptidoglycan starts in the cytoplasm and the precursor lipid II is flipped across the cytoplasmic membrane. The new peptidoglycan strands are synthesised and incorporated into the pre-existing sacculus by the coordinated activities of peptidoglycan synthases and hydrolases. In the model organism Escherichia coli there are two complexes required for the elongation and division. Each of them is regulated by different proteins from both the cytoplasmic and periplasmic sides that ensure the well-coordinated synthesis of new peptidoglycan.
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References
Alcorlo M, Martinez-Caballero S, Molina R, Hermoso JA (2017) Carbohydrate recognition and lysis by bacterial peptidoglycan hydrolases. Curr Opin Struct Biol 44:87–100
Alexeeva S, Gadella Tw Jr, Verheul J, Verhoeven GS, Den Blaauwen T (2010) Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol Microbiol 77:384–389
Amanuma H, Strominger JL (1980) Purification and properties of penicillin-binding proteins 5 and 6 from Escherichia coli membranes. J Biol Chem 255:11173–11180
Aramini JM, Rossi P, Huang YJ, Zhao L, Jiang M, Maglaqui M, Xiao R, Locke J, Nair R, Rost B, Acton TB, Inouye M, Montelione GT (2008) Solution NMR structure of the NlpC/P60 domain of lipoprotein Spr from Escherichia coli: structural evidence for a novel cysteine peptidase catalytic triad. Biochemistry 47:9715–9717
Arthur M, Molinas C, Depardieu F, Courvalin P (1993) Characterization of Tn1546, a Tn3-related transposon conferring glycopeptide resistance by synthesis of depsipeptide peptidoglycan precursors in Enterococcus faecium BM4147. J Bacteriol 175:117–127
Arthur M, Reynolds P, Courvalin P (1996) Glycopeptide resistance in enterococci. Trends Microbiol 4:401–407
Atrih A, Bacher G, Allmaier G, Williamson MP, Foster SJ (1999) Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol 181:3956–3966
Aubry C, Goulard C, Nahori MA, Cayet N, Decalf J, Sachse M, Boneca IG, Cossart P, Dussurget O (2011) OatA, a peptidoglycan O-acetyltransferase involved in Listeria monocytogenes immune escape, is critical for virulence. J Infect Dis 204:731–740
Auer GK, Lee TK, Rajendram M, Cesar S, Miguel A, Huang KC, Weibel DB (2016) Mechanical genomics identifies diverse modulators of bacterial cell stiffness. Cell Syst 2:402–411
Bailey MW, Bisicchia P, Warren BT, Sherratt DJ, Mannik J (2014a) Evidence for divisome localization mechanisms independent of the min system and SlmA in Escherichia coli. PLoS Genet 10:e1004504
Bailey RG, Turner RD, Mullin N, Clarke N, Foster SJ, Hobbs JK (2014b) The interplay between cell wall mechanical properties and the cell cycle in Staphylococcus aureus. Biophys J 107:2538–2545
Banzhaf M, van den berg van saparoea B, Terrak M, Fraipont C, Egan A, Philippe J, Zapun A, Breukink E, Nguyen-Disteche M, den Blaauwen T, Vollmer W (2012) Cooperativity of peptidoglycan synthases active in bacterial cell elongation. Mol Microbiol 85:179–194
Barreteau H, Kovac A, Boniface A, Sova M, Gobec S, Blanot D (2008) Cytoplasmic steps of peptidoglycan biosynthesis. FEMS Microbiol Rev 32:168–207
Barrett DS, Chen L, Litterman NK, Walker S (2004) Expression and characterization of the isolated glycosyltransferase module of Escherichia coli PBP1b. Biochemistry 43:12375–12381
Beeby M, Gumbart JC, Roux B, Jensen GJ (2013) Architecture and assembly of the Gram-positive cell wall. Mol Microbiol 88:664–672
Benachour A, Ladjouzi R, le Jeune A, Hebert L, Thorpe S, Courtin P, Chapot-Chartier MP, Prajsnar TK, Foster SJ, Mesnage S (2012) The lysozyme-induced peptidoglycan N-acetylglucosamine deacetylase PgdA (EF1843) is required for Enterococcus faecalis virulence. J Bacteriol 194:6066–6073
Bendezu FO, de Boer PA (2008) Conditional lethality, division defects, membrane involution, and endocytosis in mre and mrd shape mutants of Escherichia coli. J Bacteriol 190:1792–1811
Bera A, Herbert S, Jakob A, Vollmer W, Gotz F (2005) Why are pathogenic staphylococci so lysozyme resistant? the peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol Microbiol 55:778–787
Berezuk AM, Glavota S, Roach EJ, Goodyear MC, Krieger JR, Khursigara CM (2018) Outer membrane lipoprotein RlpA is a novel periplasmic interaction partner of the cell division protein FtsK in Escherichia coli. Sci Rep 8:12933
Bernal-Cabas M, Ayala JA, Raivio TL (2015) The Cpx envelope stress response modifies peptidoglycan cross-linking via the ld-transpeptidase LdtD and the novel protein YgaU. J Bacteriol 197:603–614
Bernard CS, Sadasivam M, Shiomi D, Margolin W (2007) An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol Microbiol 64:1289–1305
Bernard E, Rolain T, Courtin P, Guillot A, Langella P, Hols P, Chapot-Chartier MP (2011) Characterization of O-acetylation of N-acetylglucosamine: a novel structural variation of bacterial peptidoglycan. J Biol Chem 286:23950–23958
Bernard E, Rolain T, David B, Andre G, Dupres V, Dufrene YF, Hallet B, Chapot-Chartier MP, Hols P (2012) Dual role for the O-acetyltransferase OatA in peptidoglycan modification and control of cell septation in Lactobacillus plantarum. PLoS ONE 7:e47893
Bernhardt TG, de Boer PA (2003) The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol Microbiol 48:1171–1182
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
Bisson-Filho AW, Hsu YP, Squyres GR, Kuru E, Wu F, Jukes C, Sun Y, Dekker C, Holden S, Vannieuwenhze MS, Brun YV, Garner EC (2017) Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355:739–743
Bolla JR, Sauer JB, Wu D, Mehmood S, Allison TM, Robinson CV (2018) Direct observation of the influence of cardiolipin and antibiotics on lipid II binding to MurJ. Nat Chem 10:363–371
Boneca IG, Dussurget O, Cabanes D, Nahori MA, Sousa S, Lecuit M, Psylinakis E, Bouriotis V, Hugot JP, Giovannini M, Coyle A, Bertin J, Namane A, Rousselle JC, Cayet N, Prevost MC, Balloy V, Chignard M, Philpott DJ, Cossart P, Girardin SE (2007) A critical role for peptidoglycan N-deacetylation in Listeria evasion from the host innate immune system. Proc Natl Acad Sci USA 104:997–1002
Bonnet J, Durmort C, Jacq M, Mortier-Barriere I, Campo N, Vannieuwenhze MS, Brun YV, Arthaud C, Gallet B, Moriscot C, Morlot C, Vernet T, di Guilmi AM (2017) Peptidoglycan O-acetylation is functionally related to cell wall biosynthesis and cell division in Streptococcus pneumoniae. Mol Microbiol 106:832–846
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
Boyle-Vavra S, Labischinski H, Ebert CC, Ehlert K, Daum RS (2001) A spectrum of changes occurs in peptidoglycan composition of glycopeptide-intermediate clinical Staphylococcus aureus isolates. Antimicrob Agents Chemother 45:280–287
Brammer LAB, Ghosh A, Pan Y, Jakoncic J, Lloyd EP, Townsend CA, Lamichhane G, Bianchet MA (2015) Loss of a functionally and structurally distinct ld-transpeptidase, LdtMt5, compromises cell wall integrity in Mycobacterium tuberculosis. J Biol Chem 290:25670–25685
Bratton BP, Shaevitz JW, Gitai Z, Morgenstein RM (2018) MreB polymers and curvature localization are enhanced by RodZ and predict E. coli’s cylindrical uniformity. Nat Commun 9:2797
Bui NK, Eberhardt A, Vollmer D, Kern T, Bougault C, Tomasz A, Simorre JP, Vollmer W (2012) Isolation and analysis of cell wall components from Streptococcus pneumoniae. Anal Biochem 421:657–666
Buist G, Steen A, Kok J, Kuipers OP (2008) LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 68:838–847
Busiek KK, Eraso JM, Wang Y, Margolin W (2012) The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J Bacteriol 194:1989–2000
Busiek KK, Margolin W (2014) A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN. Mol Microbiol 92:1212–1226
Butler EK, Davis RM, Bari V, Nicholson PA, Ruiz N (2013) Structure-function analysis of MurJ reveals a solvent-exposed cavity containing residues essential for peptidoglycan biogenesis in Escherichia coli. J Bacteriol 195:4639–4649
Butler EK, Tan WB, Joseph H, Ruiz N (2014) Charge requirements of lipid II flippase activity in Escherichia coli. J Bacteriol 196:4111–4119
Cao L, Liang D, Hao P, Song Q, Xue E, Caiyin Q, Cheng Z, Qiao J (2018) The increase of O-acetylation and N-deacetylation in cell wall promotes acid resistance and nisin production through improving cell wall integrity in Lactococcus lactis. J Ind Microbiol Biotechnol
Cascales E, Bernadac A, Gavioli M, Lazzaroni JC, Lloubes R (2002) Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184:754–759
Cascales E, Gavioli M, Sturgis JN, Lloubes R (2000) Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol Microbiol 38:904–915
Cascales E, Lloubes R, Sturgis JN (2001) The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42:795–807
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
Cayley DS, Guttman HJ, Record MT Jr (2000) Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys J 78:1748–1764
Chamakura KR, Sham LT, Davis RM, Min L, Cho H, Ruiz N, Bernhardt TG, Young R (2017) A viral protein antibiotic inhibits lipid II flippase activity. Nat Microbiol 2:1480–1484
Chang JD, Foster EE, Wallace AG, Kim SJ (2017) Peptidoglycan O-acetylation increases in response to vancomycin treatment in vancomycin-resistant Enterococcus faecalis. Sci Rep 7:46500
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
Cho H, Wivagg CN, Kapoor M, Barry Z, Rohs PD, 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 16172
Clarke TB, Kawai F, Park SY, Tame JR, Dowson CG, Roper DI (2009) Mutational analysis of the substrate specificity of Escherichia coli penicillin binding protein 4. Biochemistry 48:2675–2683
Colavin A, Shi H, Huang KC (2018) RodZ modulates geometric localization of the bacterial actin MreB to regulate cell shape. Nat Commun 9:1280
Coltharp C, Buss J, Plumer TM, Xiao J (2016) Defining the rate-limiting processes of bacterial cytokinesis. Proc Natl Acad Sci USA 113:E1044–E1053
Contreras-Martel C, Martins A, Ecobichon C, Trindade DM, Mattei PJ, 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
Coulombe F, Divangahi M, Veyrier F, de Leseleuc L, Gleason JL, Yang Y, Kelliher MA, Pandey AK, Sassetti CM, Reed MB, Behr MA (2009) Increased NOD2-mediated recognition of N-glycolyl muramyl dipeptide. J Exp Med 206:1709–1716
Dajkovic A, Tesson B, Chauhan S, Courtin P, Keary R, Flores P, Marliere C, Filipe SR, Chapot-Chartier MP, Carballido-Lopez R (2017) Hydrolysis of peptidoglycan is modulated by amidation of meso-diaminopimelic acid and Mg2+ in Bacillus subtilis. Mol Microbiol 104:972–988
de Leeuw E, Graham B, Phillips GJ, Ten Hagen-Jongman CM, Oudega B, Luirink J (1999) Molecular characterization of Escherichia coli FtsE and FtsX. Mol Microbiol 31:983–993
de Pedro MA, Quintela JC, Höltje JV, Schwarz H (1997) Murein segregation in Escherichia coli. J Bacteriol 179:2823–2834
Delhaye A, Collet JF, Laloux G (2016) Fine-tuning of the Cpx envelope stress response is required for cell wall homeostasis in Escherichia coli. MBio 7:e00047–16
Demchick P, Koch AL (1996) The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J Bacteriol 178:768–773
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
di Lallo G, Fagioli M, Barionovi D, Ghelardini P, Paolozzi L (2003) Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149:3353–3359
Dik DA, Fisher JF, Mobashery S (2018) Cell-wall recycling of the Gram-negative bacteria and the nexus to antibiotic resistance. Chem Rev 118:5952–5984
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
Dillard JP, Hackett KT (2005) Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect Immun 73:5697–5705
Dutta M, Kar D, Bansal A, Chakraborty S, Ghosh AS (2015) A single amino acid substitution in the Omega-like loop of E. coli PBP5 disrupts its ability to maintain cell shape and intrinsic beta-lactam resistance. Microbiology 161:895–902
Egan AJ, Jean NL, Koumoutsi A, Bougault CM, Biboy J, Sassine J, Solovyova AS, Breukink E, Typas A, Vollmer W, Simorre JP (2014) Outer-membrane lipoprotein LpoB spans the periplasm to stimulate the peptidoglycan synthase PBP1B. Proc Natl Acad Sci USA 111:8197–8202
Egan AJ, Vollmer W (2013) The physiology of bacterial cell division. Ann N Y Acad Sci 1277:8–28
Egan AJF, Maya-Martinez R, Ayala I, Bougault CM, Banzhaf M, Breukink E, Vollmer W, Simorre JP (2018) Induced conformational changes activate the peptidoglycan synthase PBP1B. Mol Microbiol 110:335–356
el Ghachi M, Howe N, Huang CY, Olieric V, Warshamanage R, Touze T, Weichert D, Stansfeld PJ, Wang M, Kerff F, Caffrey M (2018) Crystal structure of undecaprenyl-pyrophosphate phosphatase and its role in peptidoglycan biosynthesis. Nat Commun 9:1078
Elhenawy W, Davis RM, Fero J, Salama NR, Felman MF, Ruiz N (2016) The O-antigen flippase Wzk can substitute for MurJ in peptidoglycan synthesis in Helicobacter pylori and Escherichia coli. PLoS ONE 11:e0161587
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
Engel H, van Leeuwen A, Dijkstra A, Keck W (1992) Enzymatic preparation of 1,6-anhydro-muropeptides by immobilized murein hydrolases from Escherichia coli fused to staphylococcal protein A. Appl Microbiol Biotechnol 37:772–783
Errington J (2015) Bacterial morphogenesis and the enigmatic MreB helix. Nat Rev Microbiol 13:241–248
Espaillat A, Forsmo O, el Biari K, Bjork R, Lemaitre B, Trygg J, Canada FJ, de Pedro MA, Cava F (2016) Chemometric analysis of bacterial peptidoglycan reveals atypical modifications that empower the cell wall against predatory enzymes and fly innate immunity. J Am Chem Soc 138:9193–9204
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
Fan J, Jiang D, Zhao Y, Liu J, Zhang XC (2014) Crystal structure of lipid phosphatase Escherichia coli phosphatidylglycerophosphate phosphatase B. Proc Natl Acad Sci USA 111:7636–7640
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
Figueiredo TA, Sobral RG, Ludovice AM, Almeida JM, Bui NK, Vollmer W, de Lencastre H, Tomasz A (2012) Identification of genetic determinants and enzymes involved with the amidation of glutamic acid residues in the peptidoglycan of Staphylococcus aureus. PLoS Pathog 8:e1002508
Filipe SR, Tomasz A (2000) Inhibition of the expression of penicillin resistance in Streptococcus pneumoniae by inactivation of cell wall muropeptide branching genes. Proc Natl Acad Sci USA 97:4891–4896
Firczuk M, Bochtler M (2007) Mutational analysis of peptidoglycan amidase MepA. Biochemistry 46:120–128
Fraipont C, Alexeeva S, Wolf B, van der Ploeg R, Schloesser M, den Blaauwen T, Nguyen-Disteche M (2011) The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli. Microbiology 157:251–259
Gallant CV, Daniels C, Leung JM, Ghosh AS, Young KD, Kotra LP, Burrows LL (2005) Common beta-lactamases inhibit bacterial biofilm formation. Mol Microbiol 58:1012–1024
Garcia-Bustos J, Tomasz A (1990) A biological price of antibiotic resistance: major changes in the peptidoglycan structure of penicillin-resistant pneumococci. Proc Natl Acad Sci USA 87:5415–5419
Garcia Del Portillo F, De Pedro MA (1990) Differential effect of mutational impairment of penicillin-binding proteins 1A and 1B on Escherichia coli strains harboring thermosensitive mutations in the cell division genes ftsA, ftsQ, ftsZ, and pbpB. J Bacteriol 172:5863–5870
Garcia Del Portillo F, De Pedro MA (1991) Penicillin-binding protein 2 is essential for the integrity of growing cells of Escherichia coli ponB strains. J Bacteriol 173:4530–4532
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
Geiger T, Pazos M, Lara-Tejero M, Vollmer W, Galan JE (2018). Peptidoglycan editing by a specific ld-transpeptidase controls the muramidase-dependent secretion of typhoid toxin. Nat Microbiol
Gerding MA, Liu B, Bendezu FO, Hale CA, Bernhardt TG, de Boer PA (2009) Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J Bacteriol 191:7383–7401
Glauner B, Höltje JV, Schwarz U (1988) The composition of the murein of Escherichia coli. J Biol Chem 263:10088–10095
Gonzalez-Leiza SM, de Pedro MA, Ayala JA (2011) AmpH, a bifunctional dd-endopeptidase and dd-carboxypeptidase of Escherichia coli. J Bacteriol 193:6887–6894
Govindarajan S, Amster-Choder O (2017) The bacterial Sec system is required for the organization and function of the MreB cytoskeleton. PLoS Genet 13:e1007017
Gray AN, Egan AJ, Van’t Veer IL, Verheul J, Colavin A, Koumoutsi A, Biboy J, Altelaar AF, Damen MJ, Huang KC, Simorre JP, 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
Gupta R, Lavollay M, Mainardi JL, Arthur M, Bishai WR, Lamichhane G (2010) The Mycobacterium tuberculosis protein LdtMt2 is a nonclassical transpeptidase required for virulence and resistance to amoxicillin. Nat Med 16:466–469
Ha R, Frirdich E, Sychantha D, Biboy J, Taveirne ME, Johnson JG, Dirita VJ, Vollmer W, Clarke AJ, Gaynor EC (2016) Accumulation of peptidoglycan O-acetylation leads to altered cell wall biochemistry and negatively impacts pathogenesis factors of Campylobacter jejuni. J Biol Chem 291:22686–22702
Hakulinen JK, Hering J, Branden G, Chen H, Snijder A, Ek M, Johansson P (2017) MraY-antibiotic complex reveals details of tunicamycin mode of action. Nat Chem Biol 13:265–267
Hansen JM, Golchin SA, Veyrier FJ, Domenech P, Boneca IG, Azad AK, Rajaram MV, Schlesinger LS, Divangahi M, Reed MB, Behr MA (2014) N-glycolylated peptidoglycan contributes to the immunogenicity but not pathogenicity of Mycobacterium tuberculosis. J Infect Dis 209:1045–1054
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
Heidrich C, Ursinus A, Berger J, Schwarz H, Höltje JV (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
Henderson TA, Dombrosky PM, Young KD (1994) Artifactual processing of penicillin-binding proteins 7 and 1b by the OmpT protease of Escherichia coli. J Bacteriol 176:256–259
Henderson TA, Templin M, Young KD (1995) Identification and cloning of the gene encoding penicillin-binding protein 7 of Escherichia coli. J Bacteriol 177:2074–2079
Henderson TA, Young KD, Denome SA, Elf PK (1997) AmpC and AmpH, proteins related to the class C beta-lactamases, bind penicillin and contribute to the normal morphology of Escherichia coli. J Bacteriol 179:6112–6121
Holden S (2018) Probing the mechanistic principles of bacterial cell division with super-resolution microscopy. Curr Opin Microbiol 43:84–91
Höltje JV (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203
Hrast M, Sosic I, Sink R, Gobec S (2014) Inhibitors of the peptidoglycan biosynthesis enzymes MurA-F. Bioorg Chem 55:2–15
Hsu YP, Rittichier J, Kuru E, Yablonowski J, Pasciak E, Tekkam S, Hall E, Murphy B, Lee TK, Garner EC, Huang KC, Brun YV, Vannieuwenhze MS (2017) Full color palette of fluorescent d-amino acids for in situ labeling of bacterial cell walls. Chem Sci 8:6313–6321
Hughes RC, Thurman PF, Stokes E (1975) Estimates of the porosity of Bacillus licheniformis and Bacillus subtilis cell walls. Z Immunitatsforsch Exp Klin Immunol 149:126–135
Hugonnet JE, Mengin-Lecreulx D, Monton A, Den Blaauwen T, Carbonnelle E, Veckerle C, Brun YV, Van Nieuwenhze M, Bouchier C, Tu K, Rice LB, Arthur M (2016). Factors essential for ld-transpeptidase-mediated peptidoglycan cross-linking and beta-lactam resistance in Escherichia coli. Elife 5
Iida K, Hirota Y, Schwarz U (1983) Mutants of Escherichia coli defective in penicillin-insensitive murein dd-endopeptidase. Mol Gen Genet 189:215–221
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
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
Ishino F, Jung HK, Ikeda M, Doi M, Wachi M, Matsuhashi M (1989) New mutations fts-36, lts-33, and ftsW clustered in the mra region of the Escherichia coli chromosome induce thermosensitive cell growth and division. J Bacteriol 171:5523–5530
Ize B, Stanley NR, Buchanan G, Palmer T (2003) Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol Microbiol 48:1183–1193
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
Jacobs C, Joris B, Jamin M, Klarsov K, van Beeumen J, Mengin-Lecreulx D, van Heijenoort J, Park JT, Normark S, Frere JM (1995) AmpD, essential for both beta-lactamase regulation and cell wall recycling, is a novel cytosolic N-acetylmuramyl-l-alanine amidase. Mol Microbiol 15:553–559
Jacoby GH, Young KD (1988) Unequal distribution of penicillin-binding proteins among inner membrane vesicles of Escherichia coli. J Bacteriol 170:3660–3667
Jean NL, Bougault CM, Lodge A, Derouaux A, Callens G, Egan AJ, Ayala I, Lewis RJ, Vollmer W, Simorre JP (2014) Elongated structure of the outer-membrane activator of peptidoglycan synthesis LpoA: implications for PBP1A stimulation. Structure 22:1047–1054
Jeong JH, Kim YS, Rojviriya C, Ha SC, Kang BS, Kim YG (2013) Crystal structures of bifunctional penicillin-binding protein 4 from Listeria monocytogenes. Antimicrob Agents Chemother 57:3507–3512
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
Juan C, Torrens G, Gonzalez-Nicolau M, Oliver A (2017) Diversity and regulation of intrinsic beta-lactamases from non-fermenting and other Gram-negative opportunistic pathogens. FEMS Microbiol Rev 41:781–815
Kaoukab-Raji A, Biskri L, Bernardini ML, Allaoui A (2012) Characterization of SfPgdA, a Shigella flexneri peptidoglycan deacetylase required for bacterial persistence within polymorphonuclear neutrophils. Microbes Infect 14:619–627
Kar D, Pandey SD, Mallick S, Dutta M, Ghosh AS (2018) Substitution of alanine at position 184 with glutamic acid in Escherichia coli PBP5 omega-like loop introduces a moderate cephalosporinase activity. Protein J 37:122–131
Karimova G, Dautin N, Ladant D (2005) Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187:2233–2243
Kato J, Suzuki H, Hirota Y (1985) Dispensability of either penicillin-binding protein-1a or -1b involved in the essential process for cell elongation in Escherichia coli. Mol Gen Genet 200:272–277
Kawazura T, Matsumoto K, Kojima K, Kato F, Kanai T, Niki H, Shiomi D (2017) Exclusion of assembled MreB by anionic phospholipids at cell poles confers cell polarity for bidirectional growth. Mol Microbiol 104:472–486
Keck W, Schwarz U (1979) Escherichia coli murein-dd-endopeptidase insensitive to beta-lactam antibiotics. J Bacteriol 139:770–774
Keck W, van Leeuwen AM, Huber M, Goodell EW (1990) Cloning and characterization of mepA, the structural gene of the penicillin-insensitive murein endopeptidase from Escherichia coli. Mol Microbiol 4:209–219
Kerff F, Petrella S, Mercier F, Sauvage E, Herman R, Pennartz A, Zervosen A, Luxen A, Frere JM, Joris B, Charlier P (2010) Specific structural features of the N-acetylmuramoyl-l-alanine amidase AmiD from Escherichia coli and mechanistic implications for enzymes of this family. J Mol Biol 397:249–259
Kerr CH, Culham DE, Marom D, Wood JM (2014) Salinity-dependent impacts of ProQ, Prc, and Spr deficiencies on Escherichia coli cell structure. J Bacteriol 196:1286–1296
Khattar MM, Begg KJ, Donachie WD (1994) Identification of FtsW and characterization of a new ftsW division mutant of Escherichia coli. J Bacteriol 176:7140–7147
King DT, Lameignere E, Strynadka NC (2014) Structural insights into the lipoprotein outer membrane regulator of penicillin-binding protein 1B. J Biol Chem 289:19245–19253
King DT, Wasney GA, Nosella M, Fong A, Strynadka NC (2017) Structural insights into inhibition of Escherichia coli penicillin-binding protein 1B. J Biol Chem 292:979–993
Kishida H, Unzai S, Roper DI, Lloyd A, Park SY, Tame JR (2006) Crystal structure of penicillin binding protein 4 (dacB) from Escherichia coli, both in the native form and covalently linked to various antibiotics. Biochemistry 45:783–792
Koch AL (1988) Biophysics of bacterial walls viewed as stress-bearing fabric. Microbiol Rev 52:337–353
Korat B, Mottl H, Keck W (1991) Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dacB gene, controlled overexpression, and alterations in murein composition. Mol Microbiol 5:675–684
Kouidmi I, Levesque RC, Paradis-Bleau C (2014) The biology of Mur ligases as an antibacterial target. Mol Microbiol 94:242–253
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
Kuk AC, Mashalidis EH, Lee SY (2017) Crystal structure of the MOP flippase MurJ in an inward-facing conformation. Nat Struct Mol Biol 24:171–176
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
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
Lam H, Oh DC, 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
Lambert C, Lerner TR, Bui NK, Somers H, Aizawa S, Liddell S, Clark A, Vollmer W, Lovering AL, Sockett RE (2016) Interrupting peptidoglycan deacetylation during Bdellovibrio predator-prey interaction prevents ultimate destruction of prey wall, liberating bacterial-ghosts. Sci Rep 6:26010
Lara B, Ayala JA (2002) Topological characterization of the essential Escherichia coli cell division protein FtsW. FEMS Microbiol Lett 216:23–32
Lara B, Mengin-Lecreulx D, Ayala JA, van Heijenoort J (2005) Peptidoglycan precursor pools associated with MraY and FtsW deficiencies or antibiotic treatments. FEMS Microbiol Lett 250:195–200
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 ld-transpeptidation. J Bacteriol 190:4360–4366
Lavollay M, Fourgeaud M, Herrmann JL, Dubost L, Marie A, Gutmann L, Arthur M, Mainardi JL (2011) The peptidoglycan of Mycobacterium abscessus is predominantly cross-linked by ld-transpeptidases. J Bacteriol 193:778–782
Leclercq S, Derouaux A, Olatunji S, Fraipont C, Egan AJ, Vollmer W, Breukink E, Terrak M (2017) Interplay between penicillin-binding proteins and SEDS proteins promotes bacterial cell wall synthesis. Sci Rep 7:43306
Lee M, Batuecas MT, Tomoshige S, Dominguez-Gil T, Mahasenan KV, Dik DA, Hesek D, Millan C, Uson I, Lastochkin E, Hermoso JA, Mobashery S (2018) Exolytic and endolytic turnover of peptidoglycan by lytic transglycosylase Slt of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 115:4393–4398
Lee M, Hesek D, Llarrull LI, Lastochkin E, Pi H, Boggess B, Mobashery S (2013) Reactions of all Escherichia coli lytic transglycosylases with bacterial cell wall. J Am Chem Soc 135:3311–3314
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
Lee TK, Tropini C, Hsin J, Desmarais SM, Ursell TS, Gong E, Gitai Z, Monds RD, Huang KC (2014) A dynamically assembled cell wall synthesis machinery buffers cell growth. Proc Natl Acad Sci USA 111:4554–4559
Leidenix MJ, Jacoby GH, Henderson TA, Young KD (1989) Separation of Escherichia coli penicillin-binding proteins into different membrane vesicles by agarose electrophoresis and sizing chromatography. J Bacteriol 171:5680–5686
Levefaudes M, Patin D, De Sousa-D’auria C, Chami M, Blanot D, Herve M, Arthur M, Houssin C, Mengin-Lecreulx D (2015) Diaminopimelic acid amidation in corynebacteriales: new insights into the role of LtsA in peptidoglycan modification. J Biol Chem 290:13079–13094
Li GW, Burkhardt D, Gross C, Weissman JS (2014) Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 157:624–635
Li SY, Höltje JV, Young KD (2004) Comparison of high-performance liquid chromatography and fluorophore-assisted carbohydrate electrophoresis methods for analyzing peptidoglycan composition of Escherichia coli. Anal Biochem 326:1–12
Liechti G, Kuru E, Packiam M, Hsu YP, Tekkam S, Hall E, Rittichier JT, Vannieuwenhze M, Brun YV, Maurelli AT (2016) Pathogenic chlamydia lack a classical sacculus but synthesize a narrow, mid-cell peptidoglycan ring, regulated by MreB, for cell division. PLoS Pathog 12:e1005590
Liu B, Persons L, Lee L, de Boer PA (2015) Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in Escherichia coli. Mol Microbiol 95:945–970
Liu Y, Breukink E (2016) The membrane steps of bacterial cell wall synthesis as antibiotic targets. Antibiotics (Basel) 5
Loskill P, Pereira PM, Jung P, Bischoff M, Herrmann M, Pinho MG, Jacobs K (2014) Reduction of the peptidoglycan crosslinking causes a decrease in stiffness of the Staphylococcus aureus cell envelope. Biophys J 107:1082–1089
Lovering AL, de Castro LH, Lim D, Strynadka NC (2007) Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis. Science 315:1402–1405
Lu C, Reedy M, Erickson HP (2000) Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J Bacteriol 182:164–170
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
Lupoli TJ, Tsukamoto H, Doud EH, Wang TS, Walker S, Kahne D (2011) Transpeptidase-mediated incorporation of d-amino acids into bacterial peptidoglycan. J Am Chem Soc 133:10748–10751
Magnet S, Bellais S, Dubost L, Fourgeaud M, Mainardi JL, Petit-Frere S, Marie A, Mengin-Lecreulx D, Arthur M, Gutmann L (2007) Identification of the ld-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J Bacteriol 189:3927–3931
Magnet S, Dubost L, Marie A, Arthur M, Gutmann L (2008) Identification of the ld-transpeptidases for peptidoglycan cross-linking in Escherichia coli. J Bacteriol 190:4782–4785
Mahapatra S, Crick DC, Brennan PJ (2000) Comparison of the UDP-N-acetylmuramate:l-alanine ligase enzymes from Mycobacterium tuberculosis and Mycobacterium leprae. J Bacteriol 182:6827–6830
Mainardi JL, Fourgeaud M, Hugonnet JE, Dubost L, Brouard JP, Ouazzani J, Rice LB, Gutmann L, Arthur M (2005) A novel peptidoglycan cross-linking enzyme for a beta-lactam-resistant transpeptidation pathway. J Biol Chem 280:38146–38152
Mainardi JL, Hugonnet JE, Rusconi F, Fourgeaud M, Dubost L, Moumi AN, Delfosse V, Mayer C, Gutmann L, Rice LB, Arthur M (2007) Unexpected inhibition of peptidoglycan ld-transpeptidase from Enterococcus faecium by the beta-lactam imipenem. J Biol Chem 282:30414–30422
Mainardi JL, Legrand R, Arthur M, Schoot B, van Heijenoort J, Gutmann L (2000) Novel mechanism of beta-lactam resistance due to bypass of dd-transpeptidation in Enterococcus faecium. J Biol Chem 275:16490–16496
Mainardi JL, Morel V, Fourgeaud M, Cremniter J, Blanot D, Legrand R, Frehel C, Arthur M, van Heijenoort J, Gutmann L (2002) Balance between two transpeptidation mechanisms determines the expression of beta-lactam resistance in Enterococcus faecium. J Biol Chem 277:35801–35807
Manat G, el Ghachi M, Auger R, Baouche K, Olatunji S, Kerff F, Touze T, Mengin-Lecreulx D, Bouhss A (2015) Membrane topology and biochemical characterization of the Escherichia coli BacA undecaprenyl-pyrophosphate phosphatase. PLoS ONE 10:e0142870
Manat G, Roure S, Auger R, Bouhss A, Barreteau H, Mengin-Lecreulx D, Touze T (2014) Deciphering the metabolism of undecaprenyl-phosphate: the bacterial cell-wall unit carrier at the membrane frontier. Microb Drug Resist 20:199–214
Markiewicz Z, Broome-Smith JK, Schwarz U, Spratt BG (1982) Spherical E. coli due to elevated levels of d-alanine carboxypeptidase. Nature 297:702–704
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
Matias VR, 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
Matias VR, Beveridge TJ (2005) Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56:240–251
Meberg BM, Paulson AL, Priyadarshini R, Young KD (2004) Endopeptidase penicillin-binding proteins 4 and 7 play auxiliary roles in determining uniform morphology of Escherichia coli. J Bacteriol 186:8326–8336
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
Meeske AJ, Sham LT, Kimsey H, Koo BM, Gross CA, Bernhardt TG, Rudner DZ (2015) MurJ and a novel lipid II flippase are required for cell wall biogenesis in Bacillus subtilis. Proc Natl Acad Sci USA 112:6437–6442
Meiresonne NY, Van Der Ploeg R, Hink MA, Den Blaauwen (2017) Activity-related conformational changes in dd-carboxypeptidases revealed by in vivo periplasmic forster resonance energy transfer assay in Escherichia coli. MBio 8
Mohammadi T, Sijbrandi R, Lutters M, Verheul J, Martin NI, den Blaauwen T, de Kruijff B, Breukink E (2014) Specificity of the transport of lipid II by FtsW in Escherichia coli. J Biol Chem 289:14707–14718
Mohammadi T, Van Dam V, Sijbrandi R, Vernet T, Zapun A, Bouhss A, Diepeveen-De Bruin M, Nguyen-Disteche 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
Monteiro JM, Pereira AR, Reichmann NT, Saraiva BM, Fernandes PB, Veiga H, Tavares AC, Santos M, Ferreira MT, Macario V, Vannieuwenhze MS, Filipe SR, Pinho MG (2018) Peptidoglycan synthesis drives an FtsZ-treadmilling-independent step of cytokinesis. Nature 554:528–532
Morlot C, Straume D, Peters K, Hegnar OA, Simon N, Villard AM, Contreras-Martel C, Leisico F, Breukink E, Gravier-Pelletier C, le Corre L, Vollmer W, Pietrancosta N, Havarstein LS, Zapun A (2018) Structure of the essential peptidoglycan amidotransferase MurT/GatD complex from Streptococcus pneumoniae. Nat Commun 9:3180
Moynihan PJ, Clarke AJ (2010) O-acetylation of peptidoglycan in gram-negative bacteria: identification and characterization of peptidoglycan O-acetyltransferase in Neisseria gonorrhoeae. J Biol Chem 285:13264–13273
Müller P, Ewers C, Bertsche U, Anstett M, Kallis T, Breukink E, Fraipont C, Terrak M, Nguyen-Disteche 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
Münch D, Roemer T, Lee SH, Engeser M, Sahl HG, Schneider T (2012) Identification and in vitro analysis of the GatD/MurT enzyme-complex catalyzing lipid II amidation in Staphylococcus aureus. PLoS Pathog 8:e1002509
Nanninga N (1991) Cell division and peptidoglycan assembly in Escherichia coli. Mol Microbiol 5:791–795
Nelson DE, Ghosh AS, Paulson AL, Young KD (2002) Contribution of membrane-binding and enzymatic domains of penicillin binding protein 5 to maintenance of uniform cellular morphology of Escherichia coli. J Bacteriol 184:3630–3639
Nelson DE, Young KD (2000) Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J Bacteriol 182:1714–1721
Ngadjeua F, Braud E, Saidjalolov S, Iannazzo L, Schnappinger D, Ehrt S, Hugonnet JE, Mengin-Lecreulx D, Patin D, Etheve-Quelquejeu M, Fonvielle M, Arthur M (2018) Critical impact of peptidoglycan precursor amidation on the activity of ld-transpeptidases from Enterococcus faecium and Mycobacterium tuberculosis. Chemistry 24:5743–5747
Noldeke ER, Muckenfuss LM, Niemann V, Müller A, Stork E, Zocher G, Schneider T, Stehle T (2018) Structural basis of cell wall peptidoglycan amidation by the GatD/MurT complex of Staphylococcus aureus. Sci Rep 8:12953
Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320:792–794
Osawa M, Erickson HP (2013) Liposome division by a simple bacterial division machinery. Proc Natl Acad Sci USA 110:11000–11004
Packiam M, Weinrick B, Jacobs WR Jr, Maurelli AT (2015) Structural characterization of muropeptides from Chlamydia trachomatis peptidoglycan by mass spectrometry resolves “chlamydial anomaly”. Proc Natl Acad Sci USA 112:11660–11665
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
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 (table of contents)
Pastoret S, Fraipont C, den Blaauwen T, Wolf B, Aarsman ME, Piette A, Thomas A, Brasseur R, Nguyen-Disteche M (2004) Functional analysis of the cell division protein FtsW of Escherichia coli. J Bacteriol 186:8370–8379
Pazos M, Peters K, Casanova M, Palacios P, Vannieuwenhze M, Breukink E, Vicente M, Vollmer W (2018) Z-ring membrane anchors associate with cell wall synthases to initiate bacterial cell division. Nat Commun 9:5090
Pazos M, Peters K, Vollmer W (2017) Robust peptidoglycan growth by dynamic and variable multi-protein complexes. Curr Opin Microbiol 36:55–61
Peltier J, Courtin P, el Meouche I, Lemee L, Chapot-Chartier MP, Pons JL (2011) Clostridium difficile has an original peptidoglycan structure with a high level of N-acetylglucosamine deacetylation and mainly 3-3 cross-links. J Biol Chem 286:29053–29062
Pennartz A, Genereux C, Parquet C, Mengin-Lecreulx D, Joris B (2009) Substrate-induced inactivation of the Escherichia coli AmiD N-acetylmuramoyl-l-alanine amidase highlights a new strategy to inhibit this class of enzyme. Antimicrob Agents Chemother 53:2991–2997
Pepper ED, Farrell MJ, Finkel SE (2006) Role of penicillin-binding protein 1b in competitive stationary-phase survival of Escherichia coli. FEMS Microbiol Lett 263:61–67
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
Peters K, Pazos M, Edoo Z, Hugonnet JE, Martorana AM, Polissi A, Vannieuwenhze MS, Arthur M, Vollmer W (2018) Copper inhibits peptidoglycan ld-transpeptidases suppressing beta-lactam resistance due to bypass of penicillin-binding proteins. Proc Natl Acad Sci USA 115:10786–10791
Peters NT, Dinh T, Bernhardt TG (2011) A fail-safe mechanism in the septal ring assembly pathway generated by the sequential recruitment of cell separation amidases and their activators. J Bacteriol 193:4973–4983
Peters NT, Morlot C, Yang DC, Uehara T, Vernet T, Bernhardt TG (2013) Structure-function analysis of the LytM domain of EnvC, an activator of cell wall remodelling at the Escherichia coli division site. Mol Microbiol 89:690–701
Pichoff S, Du S, Lutkenhaus J (2015) The bypass of ZipA by overexpression of FtsN requires a previously unknown conserved FtsN motif essential for FtsA-FtsN interaction supporting a model in which FtsA monomers recruit late cell division proteins to the Z ring. Mol Microbiol 95:971–987
Pichoff S, Du S, Lutkenhaus J (2018) Disruption of divisome assembly rescued by FtsN-FtsA interaction in Escherichia coli. Proc Natl Acad Sci USA 115:E6855–E6862
Pilhofer M, Aistleitner K, Biboy J, Gray J, Kuru E, Hall E, Brun YV, Vannieuwenhze MS, Vollmer W, Horn M, Jensen GJ (2013) Discovery of chlamydial peptidoglycan reveals bacteria with murein sacculi but without FtsZ. Nat Commun 4:2856
Potluri L, Karczmarek A, Verheul J, Piette A, Wilkin JM, Werth N, Banzhaf M, Vollmer W, Young KD, Nguyen-Disteche M, den Blaauwen T (2010) Septal and lateral wall localization of PBP5, the major dd-carboxypeptidase of Escherichia coli, requires substrate recognition and membrane attachment. Mol Microbiol 77:300–323
Potluri LP, de Pedro MA, Young KD (2012a) Escherichia coli low-molecular-weight penicillin-binding proteins help orient septal FtsZ, and their absence leads to asymmetric cell division and branching. Mol Microbiol 84:203–224
Potluri LP, Kannan S, Young KD (2012b) ZipA is required for FtsZ-dependent preseptal peptidoglycan synthesis prior to invagination during cell division. J Bacteriol 194:5334–5342
Priyadarshini R, Popham DL, Young KD (2006) Daughter cell separation by penicillin-binding proteins and peptidoglycan amidases in Escherichia coli. J Bacteriol 188:5345–5355
Pushkaran AC, Nataraj N, Nair N, Gotz F, Biswas R, Mohan CG (2015) Understanding the structure-function relationship of lysozyme resistance in Staphylococcus aureus by peptidoglycan O-acetylation using molecular docking, dynamics, and lysis assay. J Chem Inf Model 55:760–770
Qiao Y, Srisuknimit V, Rubino F, Schaefer K, Ruiz N, Walker S, Kahne D (2017) Lipid II overproduction allows direct assay of transpeptidase inhibition by beta-lactams. Nat Chem Biol 13:793–798
Radkov AD, Hsu YP, Booher G, Vannieuwenhze MS (2018) Imaging bacterial cell wall biosynthesis. Annu Rev Biochem 87:991–1014
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
Rawat S, Zhu L, Lindner E, Dalbey RE, White SH (2015) SecA drives transmembrane insertion of RodZ, an unusual single-span membrane protein. J Mol Biol 427:1023–1037
Raymond JB, Mahapatra S, Crick DC, Pavelka MS Jr (2005) Identification of the namH gene, encoding the hydroxylase responsible for the N-glycolylation of the mycobacterial peptidoglycan. J Biol Chem 280:326–333
Rismondo J, Wamp S, Aldridge C, Vollmer W, Halbedel S (2018) Stimulation of PgdA-dependent peptidoglycan N-deacetylation by GpsB-PBP A1 in Listeria monocytogenes. Mol Microbiol 107:472–487
Rocaboy M, Herman R, Sauvage E, Remaut H, Moonens K, Terrak M, Charlier P, Kerff F (2013) The crystal structure of the cell division amidase AmiC reveals the fold of the AMIN domain, a new peptidoglycan binding domain. Mol Microbiol 90:267–277
Rojas ER, Billings G, Odermatt PD, Auer GK, Zhu L, Miguel A, Chang F, Weibel DB, Theriot JA, Huang KC (2018) The outer membrane is an essential load-bearing element in Gram-negative bacteria. Nature 559:617–621
Romeis T, Höltje JV (1994a) Penicillin-binding protein 7/8 of Escherichia coli is a dd-endopeptidase. Eur J Biochem 224:597–604
Romeis T, Höltje JV (1994b) Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylase in Escherichia coli. J Biol Chem 269:21603–21607
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
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
Ruiz N (2009) Streptococcus pyogenes YtgP (Spy_0390) complements Escherichia coli strains depleted of the putative peptidoglycan flippase MurJ. Antimicrob Agents Chemother 53:3604–3605
Salje J, van den Ent F, de Boer P, Lowe J (2011) Direct membrane binding by bacterial actin MreB. Mol Cell 43:478–487
Sanchez M, Kolar SL, Müller S, Reyes CN, Wolf AJ, Ogawa C, Singhania R, de Carvalho DD, Arditi M, Underhill DM, Martins GA, Liu GY (2017) O-acetylation of peptidoglycan limits helper T cell priming and permits Staphylococcus aureus reinfection. Cell Host Microbe 22(543–551):e4
Sanders AN, Pavelka MS (2013) Phenotypic analysis of Eschericia coli mutants lacking ld-transpeptidases. Microbiology 159:1842–1852
Sathiyamoorthy K, Vijayalakshmi J, Tirupati B, Fan L, Saper MA (2017) Structural analyses of the Haemophilus influenzae peptidoglycan synthase activator LpoA suggest multiple conformations in solution. J Biol Chem 292:17626–17642
Sauvage E, Derouaux A, Fraipont C, Joris M, Herman R, Rocaboy M, Schloesser M, Dumas J, Kerff F, Nguyen-Disteche M, Charlier P (2014) Crystal structure of penicillin-binding protein 3 (PBP3) from Escherichia coli. PLoS ONE 9:e98042
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
Schleifer KH, Kandler O (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477
Schoenemann KM, Margolin W (2017) Bacterial division: FtsZ treadmills to build a beautiful wall. Curr Biol 27:R301–R303
Schumacher MA (2017) Bacterial nucleoid occlusion: multiple mechanisms for preventing chromosome bisection during cell division. Subcell Biochem 84:267–298
Schwechheimer C, Rodriguez DL, Kuehn MJ (2015) NlpI-mediated modulation of outer membrane vesicle production through peptidoglycan dynamics in Escherichia coli. Microbiologyopen 4:375–389
Severin A, Figueiredo AM, Tomasz A (1996) Separation of abnormal cell wall composition from penicillin resistance through genetic transformation of Streptococcus pneumoniae. J Bacteriol 178:1788–1792
Sham LT, 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
Sham LT, Zheng S, Yakhnina AA, Kruse AC, Bernhardt TG (2018) Loss of specificity variants of WzxC suggest that substrate recognition is coupled with transporter opening in MOP-family flippases. Mol Microbiol 109:633–641
Sheikh J, Hicks S, Dall’Agnol M, Phillips AD, Nataro JP (2001) Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol 41:983–997
Shi H, Bratton BP, Gitai Z, Huang KC (2018) How to build a bacterial cell: MreB as the foreman of E. coli construction. Cell 172:1294–1305
Shimada T, Park BG, Wolf AJ, Brikos C, Goodridge HS, Becker CA, Reyes CN, Miao EA, Aderem A, Gotz F, Liu GY, Underhill DM (2010) Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7:38–49
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
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
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
Soderstrom B, Chan H, Shilling PJ, Skoglund U, Daley DO (2018) Spatial separation of FtsZ and FtsN during cell division. Mol Microbiol 107:387–401
Soderstrom B, Mirzadeh K, Toddo S, von Heijne G, Skoglund U, Daley DO (2016) Coordinated disassembly of the divisome complex in Escherichia coli. Mol Microbiol 101:425–438
Soderstrom B, Skoog K, Blom H, Weiss DS, von Heijne G, Daley DO (2014) Disassembly of the divisome in Escherichia coli: evidence that FtsZ dissociates before compartmentalization. Mol Microbiol 92:1–9
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
Stranden AM, Ehlert K, Labischinski H, Berger-Bachi B (1997) Cell wall monoglycine cross-bridges and methicillin hypersusceptibility in a femAB null mutant of methicillin-resistant Staphylococcus aureus. J Bacteriol 179:9–16
Su MY, Som N, Wu CY, Su SC, Kuo YT, Ke LC, Ho MR, Tzeng SR, Teng CH, Mengin-Lecreulx D, Reddy M, Chang CI (2017) Structural basis of adaptor-mediated protein degradation by the tail-specific PDZ-protease Prc. Nat Commun 8:1516
Sung MT, Lai YT, Huang CY, Chou LY, Shih HW, Cheng WC, Wong CH, Ma C (2009) Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli. Proc Natl Acad Sci USA 106:8824–8829
Sutterlin L, Edoo Z, Hugonnet JE, Mainardi JL, Arthur M (2018) Peptidoglycan cross-linking activity of ld-transpeptidases from Clostridium difficile and inactivation of these enzymes by beta-lactams. Antimicrob Agents Chemother 62
Taguchi A, Welsh MA, Marmont LS, Lee W, Kahne D, Bernhardt TG, Walker S (2018) FtsW is a peptidoglycan polymerase that is activated by its cognate penicillin-binding protein. Preprint at. https://www.biorxiv.org/content/early/2018/06/29/358663
Tatar LD, Marolda CL, Polischuk AN, van Leeuwen D, Valvano MA (2007) An Escherichia coli undecaprenyl-pyrophosphate phosphatase implicated in undecaprenyl phosphate recycling. Microbiology 153:2518–2529
Templin MF, Edwards DH, Höltje JV (1992) A murein hydrolase is the specific target of bulgecin in Escherichia coli. J Biol Chem 267:20039–20043
Thunnissen AM, Dijkstra AJ, Kalk KH, Rozeboom HJ, Engel H, Keck W, Dijkstra BW (1994) Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography. Nature 367:750–753
Thunnissen AM, Rozeboom HJ, Kalk KH, Dijkstra BW (1995) Structure of the 70-kDa soluble lytic transglycosylase complexed with bulgecin A. Implications for the enzymatic mechanism. Biochemistry 34:12729–12737
Tomioka S, Matsuhashi M (1978) Purification of penicillin-insensitive dd-endopeptidase, a new cell wall peptidoglycan-hydrolyzing enzyme in Escherichia coli, and its inhibition by deoxyribonucleic acids. Biochem Biophys Res Commun 84:978–984
Touze T, Blanot D, Mengin-Lecreulx D (2008) Substrate specificity and membrane topology of Escherichia coli PgpB, an undecaprenyl pyrophosphate phosphatase. J Biol Chem 283:16573–16583
Tsang MJ, Bernhardt TG (2015) A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division. Mol Microbiol 95:925–944
Tsang MJ, Yakhnina AA, Bernhardt TG (2017) NlpD links cell wall remodeling and outer membrane invagination during cytokinesis in Escherichia coli. PLoS Genet 13:e1006888
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
Tuson HH, Auer GK, Renner LD, Hasebe M, Tropini C, Salick M, Crone WC, Gopinathan A, Huang KC, Weibel DB (2012) Measuring the stiffness of bacterial cells from growth rates in hydrogels of tunable elasticity. Mol Microbiol 84:874–891
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
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
Uehara T, Dinh T, Bernhardt TG (2009) LytM-domain factors are required for daughter cell separation and rapid ampicillin-induced lysis in Escherichia coli. J Bacteriol 191:5094–5107
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
Uehara T, Parzych KR, Dinh T, Bernhardt TG (2010) Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J 29:1412–1422
Ursell TS, Nguyen J, Monds RD, Colavin A, Billings G, Ouzounov N, Gitai Z, Shaevitz JW, Huang KC (2014) Rod-like bacterial shape is maintained by feedback between cell curvature and cytoskeletal localization. Proc Natl Acad Sci USA 111:E1025–E1034
Ursinus A, van den Ent F, Brechtel S, de Pedro M, Höltje JV, Lowe J, Vollmer W (2004) Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli. J Bacteriol 186:6728–6737
van Asselt EJ, Thunnissen AM, Dijkstra BW (1999) High resolution crystal structures of the Escherichia coli lytic transglycosylase Slt70 and its complex with a peptidoglycan fragment. J Mol Biol 291:877–898
van den Bogaart G, Hermans N, Krasnikov V, Poolman B (2007) Protein mobility and diffusive barriers in Escherichia coli: consequences of osmotic stress. Mol Microbiol 64:858–871
van den Ent F, Izore T, Bharat TA, Johnson CM, Lowe J (2014) Bacterial actin MreB forms antiparallel double filaments. Elife 3:e02634
van Heijenoort J (2011) Peptidoglycan hydrolases of Escherichia coli. Microbiol Mol Biol Rev 75:636–663
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
Varma A, de Pedro MA, Young KD (2007) FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli. J Bacteriol 189:5692–5704
Varma A, Young KD (2004) FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J Bacteriol 186:6768–6774
Vega D, Ayala JA (2006) The dd-carboxypeptidase activity encoded by pbp4B is not essential for the cell growth of Escherichia coli. Arch Microbiol 185:23–27
Vinella D, Joseleau-Petit D, Thevenet D, Bouloc P, D’Ari R (1993) Penicillin-binding protein 2 inactivation in Escherichia coli results in cell division inhibition, which is relieved by FtsZ overexpression. J Bacteriol 175:6704–6710
Vollmer W (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32:287–306
Vollmer W, Bertsche U (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1778:1714–1734
Vollmer W, Blanot D, de Pedro MA (2008a) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32:149–167
Vollmer W, Joris B, Charlier P, Foster S (2008b) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32:259–286
Vollmer W, Tomasz A (2000) The pgdA gene encodes for a peptidoglycan N-acetylglucosamine deacetylase in Streptococcus pneumoniae. J Biol Chem 275:20496–20501
von Rechenberg M, Ursinus A, Höltje JV (1996) Affinity chromatography as a means to study multienzyme complexes involved in murein synthesis. Microb Drug Resist 2:155–157
Weadge JT, Clarke AJ (2006) Identification and characterization of O-acetylpeptidoglycan esterase: a novel enzyme discovered in Neisseria gonorrhoeae. Biochemistry 45:839–851
Weadge JT, Pfeffer JM, Clarke AJ (2005) Identification of a new family of enzymes with potential O-acetylpeptidoglycan esterase activity in both Gram-positive and Gram-negative bacteria. BMC Microbiol 5:49
Wettmann L, Kruse K (2018) The Min-protein oscillations in Escherichia coli: an example of self-organized cellular protein waves. Philos Trans R Soc Lond B Biol Sci 373
Whatmore AM, Reed RH (1990) Determination of turgor pressure in Bacillus subtilis: a possible role for K+ in turgor regulation. J Gen Microbiol 136:2521–2526
Wheeler R, Turner RD, Bailey RG, Salamaga B, Mesnage S, Mohamad SA, 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
Williams AH, Wheeler R, Rateau L, Malosse C, Chamot-Rooke J, Haouz A, Taha MK, Boneca IG (2018) A step-by-step in crystallo guide to bond cleavage and 1,6-anhydro-sugar product synthesis by a peptidoglycan-degrading lytic transglycosylase. J Biol Chem 293:6000–6010
Workman SD, Worrall LJ, Strynadka NCJ (2018) Crystal structure of an intramembranal phosphatase central to bacterial cell-wall peptidoglycan biosynthesis and lipid recycling. Nat Commun 9:1159
Xiao J, Goley ED (2016) Redefining the roles of the FtsZ-ring in bacterial cytokinesis. Curr Opin Microbiol 34:90–96
Yadav AK, Espaillat A, Cava F (2018) Bacterial strategies to preserve cell wall integrity against environmental threats. Front Microbiol 9:2064
Yahashiri A, Jorgenson MA, Weiss DS (2015) Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides. Proc Natl Acad Sci USA 112:11347–11352
Yakhnina AA, McManus HR, Bernhardt TG (2015) The cell wall amidase AmiB is essential for Pseudomonas aeruginosa cell division, drug resistance and viability. Mol Microbiol 97:957–973
Yanagihara Y, Kamisango K, Yasuda S, Kobayashi S, Mifuchi I, Azuma I, Yamamura Y, Johnson RC (1984) Chemical compositions of cell walls and polysaccharide fractions of spirochetes. Microbiol Immunol 28:535–544
Yang DC, Peters NT, Parzych KR, Uehara T, Markovski M, Bernhardt TG (2011) An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring. Proc Natl Acad Sci USA 108:E1052–E1060
Yang DC, Tan K, Joachimiak A, Bernhardt TG (2012) A conformational switch controls cell wall-remodelling enzymes required for bacterial cell division. Mol Microbiol 85:768–781
Yang X, Lyu Z, Miguel A, McQuillen R, Huang KC, Xiao J (2017) GTPase activity-coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis. Science 355:744–747
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
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
Yuan Y, Barrett D, Zhang Y, Kahne D, Sliz P, Walker S (2007) Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis. Proc Natl Acad Sci USA 104:5348–5353
Zapun A, Philippe J, Abrahams KA, Signor L, Roper DI, Breukink E, Vernet T (2013) In vitro reconstitution of peptidoglycan assembly from the Gram-positive pathogen Streptococcus pneumoniae. ACS Chem Biol 8:2688–2696
Zheng S, Sham LT, 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
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The authors thank Professor Waldemar Vollmer at Newcastle University for critical reading this manuscript.
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Pazos, M., Peters, K. (2019). Peptidoglycan. In: Kuhn, A. (eds) Bacterial Cell Walls and Membranes . Subcellular Biochemistry, vol 92. Springer, Cham. https://doi.org/10.1007/978-3-030-18768-2_5
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