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Peptidoglycan turnover and recycling in Gram-positive bacteria

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Abstract

Bacterial cells are protected by an exoskeleton, the stabilizing and shape-maintaining cell wall, consisting of the complex macromolecule peptidoglycan. In view of its function, it could be assumed that the cell wall is a static structure. In truth, however, it is steadily broken down by peptidoglycan-cleaving enzymes during cell growth. In this process, named cell wall turnover, in one generation up to half of the preexisting peptidoglycan of a bacterial cell is released from the wall. This would result in a massive loss of cell material, if turnover products were not be taken up and recovered. Indeed, in the Gram-negative model organism Escherichia coli, peptidoglycan recovery has been recognized as a complex pathway, named cell wall recycling. It involves about a dozen dedicated recycling enzymes that convey cell wall turnover products to peptidoglycan synthesis or energy pathways. Whether Gram-positive bacteria also recover their cell wall is currently questioned. Given the much larger portion of peptidoglycan in the cell wall of Gram-positive bacteria, however, recovery of the wall material would provide an even greater benefit in these organisms compared to Gram-negatives. Consistently, in many Gram-positives, orthologs of recycling enzymes were identified, indicating that the cell wall may also be recycled in these organisms. This mini-review provides a compilation of information about cell wall turnover and recycling in Gram-positive bacteria during cell growth and division, including recent findings relating to muropeptide recovery in Bacillus subtilis and Clostridium acetobutylicum from our group. Furthermore, the impact of cell wall turnover and recycling on biotechnological processes is discussed.

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References

  • Araki Y, Nakatani T, Hayashi H, Ito E (1971) Occurrence of non-N-substituted glucosamine residues in lysozyme-resistant peptidoglycan from Bacillus cereus cell walls. Biochem Biophys Res Commun 42:691–697

    CAS  PubMed  Google Scholar 

  • Araki Y, Nakatani T, Nakayama K, Ito E (1972) Occurrence of N-nonsubstituted glucosamine residues in peptidoglycan of lysozyme-resistant cell walls from Bacillus cereus. J Biol Chem 247:6312–6322

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Blackman SA, Smith TJ, Foster SJ (1998) The role of autolysins during vegetative growth of Bacillus subtilis 168. Microbiology 144:73–82

    CAS  PubMed  Google Scholar 

  • Blümel P, Uecker W, Giesbrecht P (1979) Zero order kinetics of cell wall turnover in Staphylococcus aureus. Arch Microbiol 121:103–110

    PubMed  Google Scholar 

  • Boothby D, Daneo-Moore L, Higgins ML, Coyette J, Shockman GD (1973) Turnover of bacterial cell wall peptidoglycans. J Biol Chem 248:2161–2169

    CAS  PubMed  Google Scholar 

  • Burman LG, Raichler J, Park JT (1983) Evidence for diffuse growth of the cylindrical portion of the Escherichia coli murein sacculus. J Bacteriol 155:983–988

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chaloupka J, Křečková P, Řihová L (1962a) The mucopeptide turnover in the cell walls of growing cultures of Bacillus megaterium KM. Experientia 18:362–363

    CAS  PubMed  Google Scholar 

  • Chaloupka J, Křečková P, Říhová L (1962b) Changes in the character of the cell wall in growth of Bacillus megaterium cultures. Folia Microbiol 7:269–274

    CAS  Google Scholar 

  • Chapot-Chartier MP (2010) Bacterial autolysins (Chapter 13). In: König H, Claus H, Varma A (eds) Prokaryotic cell wall compounds — structure and biochemistry. Springer, Heidelberg, pp 383–406

    Google Scholar 

  • Cheng Q, Park JT (2002) Substrate specificity of the AmpG permease required for recycling of cell wall anhydro-muropeptides. J Bacteriol 184:6434–6436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng Q, Li H, Merdek K, Park JT (2000) Molecular characterization of the β-N-acetylglucosaminidase of Escherichia coli and its role in cell wall recycling. J Bacteriol 182:4836–4840

    CAS  PubMed  PubMed Central  Google Scholar 

  • Croux C, Canard B, Goma G, Soucaille P (1992) Purification and characterization of an extracellular muramidase of Clostridium acetobutylicum ATCC 824 that acts on non-N-acetylated peptidoglycan. Appl Environ Microbiol 58:1075–1081

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dahl U, Jaeger T, Nguyen BT, Sattler JM, Mayer C (2004) Identification of a phosphotransferase system of Escherichia coli required for growth on N-acetylmuramic acid. J Bacteriol 186:2385–2392

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Pedro M, Quintela J, Holtje J, Schwarz H (1997) Murein segregation in Escherichia coli. J Bacteriol 179:2823–2834

    PubMed  PubMed Central  Google Scholar 

  • Demchick P, Koch AL (1996) The permeability of the wall fabric of Escherichia coli and Bacillus subtilis. J Bacteriol 178:768–773

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle RJ, Chaloupka J, Vinter V (1988) Turnover of cell walls in microorganisms. Microbiol Rev 52:554–567

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dubrac S, Bisicchia P, Devine KM, Msadek T (2008) A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Mol Microbiol 70:1307–1322

    CAS  PubMed  Google Scholar 

  • Errington J (1993) Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev 57:1–33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fabret C, Hoch JA (1998) A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J Bacteriol 180:6375–6383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fabret C, Feher VA, Hoch JA (1999) Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J Bacteriol 181:1975–1983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Foster SJ, Popham DL (2002) Structure and synthesis of cell wall, spore cortex, teichoic acids, S-layers, and capsules. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, pp 21–41

    Google Scholar 

  • Goodell EW (1985) Recycling of murein by Escherichia coli. J Bacteriol 163:305–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goodell EW, Schwarz U (1985) Release of cell wall peptides into culture medium by exponentially growing Escherichia coli. J Bacteriol 162:391–397

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hancock IC, Cox CM (1991) Turnover of cell surface-bound capsular polysaccharide in Staphylococcus aureus. FEMS Microbiol Lett 77:25–30

    CAS  Google Scholar 

  • Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J, Schwarz H, De Pedro MA, Höltje J-V (2001) Involvement of N-acetylmuramyl-l-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol Microbiol 41:167–178

    CAS  PubMed  Google Scholar 

  • Herbold DR, Glaser L (1975) Bacillus subtilis N-acetylmuramic acid l-alanine amidase. J Biol Chem 250:1676–1682

    CAS  PubMed  Google Scholar 

  • Höltje J-V (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203

    PubMed  PubMed Central  Google Scholar 

  • Höltje J-V, Kopp U, Ursinus A, Wiedemann B (1994) The negative regulator of β-lactamase induction AmpD is a N-acetyl-anhydromuramyl-l-alanine amidase. FEMS Microbiol Lett 122:159–164

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobs C, Joris B, Jamin M, Klarsov K, van Beeumen J, Mengin-Lecreulx D, van Heijenoort J, Park JT, Normark S, Frère J-M (1995) AmpD, essential for both β-lactamase regulation and cell wall recycling, is a novel cytosolic N-acetylmuramyl-l-alanine amidase. Mol Microbiol 15:553–559

    CAS  PubMed  Google Scholar 

  • Jaeger T, Mayer C (2008a) N-acetylmuramic acid 6-phosphate lyases (MurNAc etherases): role in cell wall metabolism, distribution, structure, and mechanism. Cell Mol Life Sci 65:928–939

    CAS  PubMed  Google Scholar 

  • Jaeger T, Mayer C (2008b) The transcriptional factors MurR and catabolite activator protein regulate N-acetylmuramic acid catabolism in Escherichia coli. J Bacteriol 190:6598–6608

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jaeger T, Arsic M, Mayer C (2005) Scission of the lactyl ether bond of N-acetylmuramic acid by Escherichia coli “Etherase”. J Biol Chem 280:30100–30106

    CAS  PubMed  Google Scholar 

  • Koch AL, Doyle RJ (1985) Inside-to-outside growth and turnover of the wall of Gram-positive rods. J Theor Biol 117:137–157

    CAS  PubMed  Google Scholar 

  • Litzinger S, Mayer C (2010) The murein sacculus (Chapter 1). In: König H, Claus H, Varma A (eds) Prokaryotic cell wall compounds — structure and biochemistry. Springer, Berlin, pp 3–54

    Google Scholar 

  • Litzinger S, Duckworth A, Nitzsche K, Risinger C, Wittmann V, Mayer C (2010a) Muropeptide rescue in Bacillus subtilis involves sequential hydrolysis by β-N-acetylglucosaminidase and N-acetylmuramyl-l-alanine amidase. J Bacteriol 192:3132–3143

    CAS  PubMed  PubMed Central  Google Scholar 

  • Litzinger S, Fischer S, Polzer P, Diederichs K, Welte W, Mayer C (2010b) Structural and kinetic analysis of Bacillus subtilis N-acetylglucosaminidase reveals a unique Asp–His dyad mechanism. J Biol Chem 285:35675–35684

    CAS  PubMed  PubMed Central  Google Scholar 

  • Matias VRF, 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

    CAS  PubMed  Google Scholar 

  • Matias VRF, Beveridge TJ (2006) Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J Bacteriol 188:1011–1021

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mauck J, Glaser L (1970) Turnover of the cell wall of Bacillus subtilis W-23 during logarithmic growth. Biochem Biophys Res Commun 39:699–706

    CAS  PubMed  Google Scholar 

  • Mauck J, Chan L, Glaser L (1971) Turnover of the cell wall of Gram-positive bacteria. J Biol Chem 246:1820–1827

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Mengin-Lecreulx D, van Heijenoort J, Park J (1996) Identification of the mpl gene encoding UDP-N-acetylmuramate: l-alanyl-gamma-d-glutamyl-meso-diaminopimelate ligase in Escherichia coli and its role in recycling of cell wall peptidoglycan. J Bacteriol 178:5347–5352

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mesnage S, Chau F, Dubost L, Arthur M (2008) Role of N-acetylglucosaminidase and N-acteylmuramidase activities in Enterococcus faecalis peptidoglycan metabolism. J Biol Chem 283:19845–19853

    CAS  PubMed  Google Scholar 

  • Meyer P, Gutierrez J, Pogliano K, Dworkin J (2011) Cell wall synthesis is necessary for membrane dynamics during sporulation of Bacillus subtilis. Mol Microbiol 76:956–970

    Google Scholar 

  • Morlot C, Uehara T, Marquis KA, Bernhardt TG, Rudner DZ (2011) A highly coordinated cell wall degradation machine governs spore morphogenesis in Bacillus subtilis. Genes Dev 24:411–422

    Google Scholar 

  • Park JT (1993) Turnover and recycling of the murein sacculus in oligopeptide permease-negative strains of Escherichia coli: indirect evidence for an alternative permease system and for a monolayered sacculus. J Bacteriol 175:7–11

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park JT, Raychaudhuri D, Li H, Normark S, Mengin-Lecreulx D (1998) MppA, a periplasmic binding protein essential for import of the bacterial cell wall peptide l-Alanyl-gamma-d-Glutamyl-meso-diaminopimelate. J Bacteriol 180:1215–1223

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pasztor L, Ziebandt AK, Nega M, Schlag M, Haase S, Franz-Wachtel M, Madlung J, Nordheim A, Heinrichs DE, Götz F (2010) Staphylococcal major autolysin (Atl) is involved in excretion of cytoplasmic proteins. J Biol Chem 285:36794–36803

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plumbridge J (2009) An alternative route for recycling of N-acetylglucosamine from peptidoglycan involves the N-acetylglucosamine phosphotransferase system in Escherichia coli. J Bacteriol 191:5641–5647

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pooley HM (1976a) Layered distribution, according to age, within the cell wall of Bacillus subtilis. J Bacteriol 125:1139–1147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pooley HM (1976b) Turnover and spreading of old wall during surface growth of Bacillus subtilis. J Bacteriol 125:1127–1138

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Psylinakis E, Boneca IG, Mavromatis K, Deli A, Hayhurst E, Foster SJ, Varum KM, Bouriotis V (2005) Peptidoglycan N-acetylglucosamine deacetylases from Bacillus cereus, highly conserved proteins in Bacillus anthracis. J Biol Chem 280:30856–30863

    CAS  PubMed  Google Scholar 

  • Reith J, Mayer C (2011) Characterisation of a glucosamine/β-glucosaminide N-acetyltransferase of Clostridium acetobutylicum. J Bacteriol, in press

  • Reith J, Berking A, Mayer C (2011) Characterisation of an N-acetylmuramic acid/N-acetylglucosamine kinase of Clostridium acetobutylicum. J Bacteriol, in press

  • Reizer J, Saier MH Jr, Deutscher J, Grenier F, Thompson J, Hengstenberg W (1988) The phosphoenolpyruvate: sugar phosphotransferase system in Gram-positive bacteria: properties, mechanism, and regulation. Crit Rev Microbiol 15:297–338

    CAS  PubMed  Google Scholar 

  • Rogers HJ (1967) The structure and biosynthesis of the components of the cell walls of Gram-positive bacteria. Folia Microbiol 12:191–200

    CAS  Google Scholar 

  • Shah IM, Laaberki MH, Popham DL, Dworkin J (2008) A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135:486–496

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shockman GD, Höltje JV (1994) Microbial peptidoglycan (murein) hydrolases. In: Ghuysen JM, Hackenbeck R (eds) Bacterial cell wall. Elsevier, Amsterdam, pp 131–166

    Google Scholar 

  • Smith TJ, Blackman SA, Foster SJ (2000) Autolysins of Bacillus subtilis: multiple enzymes with multiple functions. Microbiology 146:249–262

    CAS  PubMed  Google Scholar 

  • Templin MF, Ursinus A, Holtje J-V (1999) A defect in cell wall recycling triggers autolysis during the stationary growth phase of Escherichia coli. EMBO J 18:4108–4117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Traub S, von Aulock S, Hartung T, Hermann C (2006) MDP and other muropeptides—direct and synergistic effects on the immune system. J Endotoxin Res 12:69–85

    CAS  PubMed  Google Scholar 

  • Uehara T, Park JT (2004) The N-acetyl-d-glucosamine kinase of Escherichia coli and its role in murein recycling. J Bacteriol 186:7273–7279

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uehara T, Park JT (2008) Growth of Escherichia coli: significance of peptidoglycan degradation during elongation and septation. J Bacteriol 190:3914–3922

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uehara T, Suefuji K, Valbuena N, Meehan B, Donegan M, Park JT (2005) Recycling of the anhydro-N-acetylmuramic acid derived from cell wall murein involves a two-step conversion to N-acetylglucosamine-phosphate. J Bacteriol 187:3643–3649

    CAS  PubMed  PubMed Central  Google Scholar 

  • Uehara T, Suefuji K, Jaeger T, Mayer C, Park JT (2006) MurQ etherase is required by Escherichia coli in order to metabolize anhydro-N-acetylmuramic acid obtained either from the environment or from its own cell wall. J Bacteriol 188:1660–1662

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vollmer W (2008) Structural variation in the glycan strands of bacterial peptidoglycan. FEMS Microbiol Rev 32:287–306

    CAS  PubMed  Google Scholar 

  • Vollmer W, Blanot D, De Pedro MA (2008) Peptidoglycan structure and architecture. FEMS Microbiol Rev 32:149–167

    CAS  PubMed  Google Scholar 

  • Vötsch W, Templin MF (2000) Characterization of a β-N-acetylglucosaminidase of Escherichia coli and elucidation of its role in muropeptide recycling and β-lactamase induction. J Biol Chem 275:39032–39038

    PubMed  Google Scholar 

  • Weidenmaier C, Peschel A (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6:276–287

    CAS  PubMed  Google Scholar 

  • White RJ (1968) Control of amino sugar metabolism in Escherichia coli and isolation of mutants unable to degrade amino sugars. Biochem J 106:847–858

    CAS  PubMed  PubMed Central  Google Scholar 

  • White RJ, Pasternak CA (1967) The purification and properties of N-acetylglucosamine 6-phosphate deacetylase from Escherichia coli. Biochem J 105:121–125

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wong W, Young FE, Chatterjee AN (1974) Regulation of bacterial cell walls: turnover of cell wall in Staphylococcus aureus. J Bacteriol 120:837–843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto H, Hashimoto M, Higashitsuji Y, Harada H, Hariyama N, Takahashi L, Iwashita T, Ooiwa S, Sekiguchi J (2008) Post-translational control of vegetative cell separation enzymes through a direct interaction with specific inhibitor IseA in Bacillus subtilis. Mol Microbiol 70:168–182

    CAS  PubMed  Google Scholar 

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  1. Fachbereich Biologie, Molekulare Mikrobiologie, University of Konstanz, 78457, Konstanz, Germany

    Jan Reith & Christoph Mayer

  2. Interfakultäres Institut für Mikrobiologie und Infektionsmedizin Tübingen IMIT, Mikrobiologie/Biotechnologie, Eberhard Karls Universität Tübingen, 72076, Tübingen, Germany

    Christoph Mayer

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Reith, J., Mayer, C. Peptidoglycan turnover and recycling in Gram-positive bacteria. Appl Microbiol Biotechnol 92, 1–11 (2011). https://doi.org/10.1007/s00253-011-3486-x

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