1932

Abstract

Most bacteria are protected from environmental offenses by a cell wall consisting of strong yet elastic peptidoglycan. The cell wall is essential for preserving bacterial morphology and viability, and thus the enzymes involved in the production and turnover of peptidoglycan have become preferred targets for many of our most successful antibiotics. In the past decades, , the gram-negative pathogen causing the diarrheal disease cholera, has become a major model for understanding cell wall genetics, biochemistry, and physiology. More than 100 articles have shed light on novel cell wall genetic determinants, regulatory links, and adaptive mechanisms. Here we provide the first comprehensive review of ’s cell wall biology and genetics. Special emphasis is placed on the similarities and differences with , the paradigm for understanding cell wall metabolism and chemical structure in gram-negative bacteria.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-040621-122027
2021-10-08
2024-10-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/75/1/annurev-micro-040621-122027.html?itemId=/content/journals/10.1146/annurev-micro-040621-122027&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    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
    [Google Scholar]
  2. 2. 
    Altindis E, Dong T, Catalano C, Mekalanos J. 2015. Secretome analysis of Vibrio cholerae type VI secretion system reveals a new effector-immunity pair. mBio 6:e00075
    [Google Scholar]
  3. 3. 
    Alvarez L, Aliashkevich A, de Pedro MA, Cava F. 2018. Bacterial secretion of d-arginine controls environmental microbial biodiversity. ISME J 12:438–50
    [Google Scholar]
  4. 4. 
    Antonoplis A, Zang X, Wegner T, Wender PA, Cegelski L. 2019. Vancomycin–arginine conjugate inhibits growth of carbapenem-resistant E. coli and targets cell-wall synthesis. ACS Chem. Biol. 14:2065–70
    [Google Scholar]
  5. 5. 
    Asmar AT, Collet JF. 2018. Lpp, the Braun lipoprotein, turns 50—major achievements and remaining issues. FEMS Microbiol. Lett. 365:fny199
    [Google Scholar]
  6. 6. 
    Baker RM, Singleton FL, Hood MA. 1983. Effects of nutrient deprivation on Vibrio cholerae. Appl. Environ. Microbiol. 46:930–40
    [Google Scholar]
  7. 7. 
    Banzhaf M, Yau HC, Verheul J, Lodge A, Kritikos G et al. 2020. Outer membrane lipoprotein NlpI scaffolds peptidoglycan hydrolases within multi-enzyme complexes in Escherichia coli. EMBO J 39:e102246
    [Google Scholar]
  8. 8. 
    Bartlett TM, Bratton BP, Duvshani A, Miguel A, Sheng Y et al. 2017. A periplasmic polymer curves Vibrio cholerae and promotes pathogenesis. Cell 168:172–85.e15Identifies CrvA, the first curvature determinant in Vibrio cholerae, which controls asymmetrical peptidoglycan insertion.
    [Google Scholar]
  9. 9. 
    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. 197:603–14
    [Google Scholar]
  10. 10. 
    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. 280:38096–101
    [Google Scholar]
  11. 11. 
    Bielig H, Dongre M, Zurek B, Wai SN, Kufer TA. 2011. A role for quorum sensing in regulating innate immune responses mediated by Vibrio cholerae outer membrane vesicles (OMVs). Gut Microbes 2:274–79
    [Google Scholar]
  12. 12. 
    Blasco B, Pisabarro AG, de Pedro MA. 1988. Peptidoglycan biosynthesis in stationary-phase cells of Escherichia coli. J. Bacteriol. 170:5224–28
    [Google Scholar]
  13. 13. 
    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. 281:26985–93
    [Google Scholar]
  14. 14. 
    Brenzinger S, van der Aart LT, van Wezel GP, Lacroix JM, Glatter T, Briegel A. 2019. Structural and proteomic changes in viable but non-culturable Vibrio cholerae. Front. Microbiol. 10:793
    [Google Scholar]
  15. 15. 
    Brooks TM, Unterweger D, Bachmann V, Kostiuk B, Pukatzki S. 2013. Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J. Biol. Chem. 288:7618–25
    [Google Scholar]
  16. 16. 
    Burrows W. 1957. Studies on immunity to asiatic cholera. IX. Electrophoretic fractions of cell wall and intracellular substance of Vibrio cholerae and their occurrence in successive isolates during the course of the disease. J. Infect. Dis. 101:73–84
    [Google Scholar]
  17. 17. 
    Bush K. 2018. Past and present perspectives on β-lactamases. Antimicrob. Agents Chemother. 62:10e01076-18
    [Google Scholar]
  18. 18. 
    Cameron DE, Urbach JM, Mekalanos JJ 2008. A defined transposon mutant library and its use in identifying motility genes in Vibrio cholerae. PNAS 105:8736–41
    [Google Scholar]
  19. 19. 
    Castanheira S, Cestero JJ, Rico-Perez G, Garcia P, Cava F et al. 2017. A specialized peptidoglycan synthase promotes Salmonella cell division inside host cells. mBio 8:6e01685-17
    [Google Scholar]
  20. 20. 
    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 30:3442–53Characterizes different processes mediating the incorporation of noncanonical d-amino acids into the peptidoglycan.
    [Google Scholar]
  21. 21. 
    Ceccarelli D, Alam M, Huq A, Colwell RR. 2016. Reduced susceptibility to extended-spectrum β-lactams in Vibrio cholerae isolated in Bangladesh. Front. Public Health 4:231
    [Google Scholar]
  22. 22. 
    Chaiyanan S, Chaiyanan S, Grim C, Maugel T, Huq A, Colwell RR. 2007. Ultrastructure of coccoid viable but non-culturable Vibrio cholerae. Environ. Microbiol. 9:393–402
    [Google Scholar]
  23. 23. 
    Chao MC, Pritchard JR, Zhang YJ, Rubin EJ, Livny J et al. 2013. High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model–based analyses of transposon-insertion sequencing data. Nucleic Acids Res 41:9033–48
    [Google Scholar]
  24. 24. 
    Chatterjee D, Chaudhuri K. 2011. Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett 585:1357–62
    [Google Scholar]
  25. 25. 
    Chatterjee SN, Das J. 1967. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J. Gen. Microbiol. 49:1–11
    [Google Scholar]
  26. 26. 
    Chodisetti PK, Reddy M 2019. Peptidoglycan hydrolase of an unusual cross-link cleavage specificity contributes to bacterial cell wall synthesis. PNAS 116:7825–30
    [Google Scholar]
  27. 27. 
    Conner JG, Teschler JK, Jones CJ, Yildiz FH. 2016. Staying alive: Vibrio cholerae’s cycle of environmental survival, transmission, and dissemination. Microbiol. Spectr. 4:; https://doi.org/10.1128/microbiolspec.VMBF-0015-2015
    [Crossref] [Google Scholar]
  28. 28. 
    Das B, Verma J, Kumar P, Ghosh A, Ramamurthy T. 2020. Antibiotic resistance in Vibrio cholerae: understanding the ecology of resistance genes and mechanisms. Vaccine 38:Suppl. 1A83–92
    [Google Scholar]
  29. 29. 
    Das J, Chatterjee SN. 1966. Electron microscopic studies on some ultra-structural aspects of Vibrio cholerae. Indian J. Med. Res. 54:330–38
    [Google Scholar]
  30. 30. 
    Das M, Chopra AK, Wood T, Peterson JW. 1998. Cloning, sequencing and expression of the flagellin core protein and other genes encoding structural proteins of the Vibrio cholerae flagellum. FEMS Microbiol. Lett. 165:239–46
    [Google Scholar]
  31. 31. 
    Derouaux A, Wolf B, Fraipont C, Breukink E, Nguyen-Disteche 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. 190:1831–34
    [Google Scholar]
  32. 32. 
    Desmarais SM, Tropini C, Miguel A, Cava F, Monds RD et al. 2015. High-throughput, highly sensitive analyses of bacterial morphogenesis using ultra performance liquid chromatography. J. Biol. Chem. 290:31090–100
    [Google Scholar]
  33. 33. 
    Dik DA, Fisher JF, Mobashery S. 2018. Cell-wall recycling of the gram-negative bacteria and the nexus to antibiotic resistance. Chem. Rev. 118:5952–84
    [Google Scholar]
  34. 34. 
    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. 295:3347–61
    [Google Scholar]
  35. 35. 
    Dorr T, Alvarez L, Delgado F, Davis BM, Cava F, Waldor MK. 2016. A cell wall damage response mediated by a sensor kinase/response regulator pair enables β-lactam tolerance. PNAS 113:404–9Identifies VxrAB, a two-component system that promotes peptidoglycan synthesis in response to cell-wall damage.
    [Google Scholar]
  36. 36. 
    Dorr 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. 89:949–62Studies Vibrio cholerae’s Shy d,d-endopeptidases and their substrate specificity.
    [Google Scholar]
  37. 37. 
    Dorr T, Davis BM, Waldor MK 2015. Endopeptidase-mediated β lactam tolerance. PLOS Pathog 11:e1004850Describes Vibrio cholerae's survival mechanism against β-lactams via peptidoglycan hydrolase–mediated sphere formation.
    [Google Scholar]
  38. 38. 
    Dorr T, Delgado F, Umans BD, Gerding MA, Davis BM, Waldor MK. 2016. A transposon screen identifies genetic determinants of Vibrio cholerae resistance to high-molecular-weight antibiotics. Antimicrob. Agents Chemother. 60:4757–63
    [Google Scholar]
  39. 39. 
    Dorr 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:e1004433Characterizes CsiV, a novel penicillin-binding protein activator essential for growth in the presence of noncanonical d-amino acids.
    [Google Scholar]
  40. 40. 
    Dorr T, Moll A, Chao MC, Cava F, Lam H et al. 2014. Differential requirement for PBP1a and PBP1b in in vivo and in vitro fitness of Vibrio cholerae. Infect. Immun. 82:2115–24
    [Google Scholar]
  41. 41. 
    Echazarreta MA, Klose KE. 2019. Vibrio flagellar synthesis. Front. Cell Infect. Microbiol. 9:131
    [Google Scholar]
  42. 42. 
    Emami K, Guyet A, Kawai Y, Devi J, Wu LJ et al. 2017. RodA as the missing glycosyltransferase in Bacillus subtilis and antibiotic discovery for the peptidoglycan polymerase pathway. Nat. Microbiol. 2:16253
    [Google Scholar]
  43. 43. 
    Espaillat A, Carrasco-Lopez C, Bernardo-Garcia N, Pietrosemoli N, Otero LH et al. 2014. Structural basis for the broad specificity of a new family of amino-acid racemases. Acta Crystallogr. D Biol. Crystallogr. 70:79–90
    [Google Scholar]
  44. 44. 
    Fallingborg J, Christensen LA, Ingeman-Nielsen M, Jacobsen BA, Abildgaard K, Rasmussen HH. 1989. pH-profile and regional transit times of the normal gut measured by a radiotelemetry device. Aliment. Pharmacol. Ther. 3:605–13
    [Google Scholar]
  45. 45. 
    Faruque SM, Biswas K, Udden SM, Ahmad QS, Sack DA et al. 2006. Transmissibility of cholera: in vivo–formed biofilms and their relationship to infectivity and persistence in the environment. PNAS 103:6350–55
    [Google Scholar]
  46. 46. 
    Fernandez NL, Hsueh BY, Nhu NTQ, Franklin JL, Dufour YS, Waters CM 2020. Vibrio cholerae adapts to sessile and motile lifestyles by cyclic di-GMP regulation of cell shape. PNAS 117:29046–54
    [Google Scholar]
  47. 47. 
    Fleurie A, Zoued A, Alvarez L, Hines KM, Cava F et al. 2019. A Vibrio cholerae BolA-like protein is required for proper cell shape and cell envelope integrity. mBio 10:4e00790-19
    [Google Scholar]
  48. 48. 
    Fu X, Liang W, Du P, Yan M, Kan B 2014. Transcript changes in Vibrio cholerae in response to salt stress. Gut Pathog 6:47
    [Google Scholar]
  49. 49. 
    Galli E, Paly E, Barre FX. 2017. Late assembly of the Vibrio cholerae cell division machinery postpones septation to the last 10% of the cell cycle. Sci. Rep. 7:44505
    [Google Scholar]
  50. 50. 
    Galli E, Poidevin M, Le Bars R, Desfontaines JM, Muresan L et al. 2016. Cell division licensing in the multi-chromosomal Vibrio cholerae bacterium. Nat. Microbiol. 1:16094Studies Vibrio cholerae's divisome positioning and assembly during the cell cycle.
    [Google Scholar]
  51. 51. 
    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. 3:1243–54
    [Google Scholar]
  52. 52. 
    Ghosh AS, Chowdhury C, Nelson DE. 2008. Physiological functions of d-alanine carboxypeptidases in Escherichia coli. Trends Microbiol 16:309–17
    [Google Scholar]
  53. 53. 
    Ghosh AS, Young KD. 2003. Sequences near the active site in chimeric penicillin binding proteins 5 and 6 affect uniform morphology of Escherichia coli. J. Bacteriol. 185:2178–86
    [Google Scholar]
  54. 54. 
    Ghuysen JM. 1968. Use of bacteriolytic enzymes in determination of wall structure and their role in cell metabolism. Bacteriol. Rev. 32:425–64
    [Google Scholar]
  55. 55. 
    Gladkikh AS, Feranchuk SI, Ponomareva AS, Bochalgin NO, Mironova LV. 2020. Antibiotic resistance in Vibrio cholerae El Tor strains isolated during cholera complications in Siberia and the Far East of Russia. Infect. Genet. Evol. 78:104096
    [Google Scholar]
  56. 56. 
    Godessart P, Lannoy A, Dieu M, Van der Verren SE, Soumillion P et al. 2020. β-Barrels covalently link peptidoglycan and the outer membrane in the α-proteobacterium Brucella abortus. Nat. Microbiol. 6:27–33
    [Google Scholar]
  57. 57. 
    Goffin C, Ghuysen JM. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079–93
    [Google Scholar]
  58. 58. 
    Gray AN, Egan AJ, Van't Veer IL, Verheul J, Colavin A et al. 2015. Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division. eLife 4:e07118
    [Google Scholar]
  59. 59. 
    Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J et al. 2001. Involvement of N-acetylmuramyl-l-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol. 41:167–78
    [Google Scholar]
  60. 60. 
    Heidrich C, Ursinus A, Berger J, Schwarz H, Holtje JV. 2002. Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J. Bacteriol. 184:6093–99
    [Google Scholar]
  61. 61. 
    Herlihey FA, Clarke AJ. 2017. Controlling autolysis during flagella insertion in gram-negative bacteria. Adv. Exp. Med. Biol. 925:41–56
    [Google Scholar]
  62. 62. 
    Herlihey FA, Moynihan PJ, Clarke AJ. 2014. The essential protein for bacterial flagella formation FlgJ functions as a β-N-acetylglucosaminidase. J. Biol. Chem. 289:31029–42
    [Google Scholar]
  63. 63. 
    Hernandez SB, Cava F. 2016. Environmental roles of microbial amino acid racemases. Environ. Microbiol. 18:1673–85
    [Google Scholar]
  64. 64. 
    Hernandez SB, Cava F, Pucciarelli MG, Garcia–Del Portillo F, de Pedro MA, Casadesus J 2015. Bile-induced peptidoglycan remodelling in Salmonella enterica. Environ. Microbiol. 17:1081–89
    [Google Scholar]
  65. 65. 
    Hernandez SB, Dorr T, Waldor MK, Cava F 2020. Modulation of peptidoglycan synthesis by recycled cell wall tetrapeptides. Cell Rep 31:107578Analyzes in depth the noncanonical d-amino acid–modified muropeptide recycling pathway and the control of peptidoglycan synthesis and cross-linking.
    [Google Scholar]
  66. 66. 
    Hirano T, Minamino T, Macnab RM. 2001. The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase. J. Mol. Biol. 312:359–69
    [Google Scholar]
  67. 67. 
    Holtje JV. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181–203
    [Google Scholar]
  68. 68. 
    Horcajo P, de Pedro MA, Cava F. 2012. Peptidoglycan plasticity in bacteria: stress-induced peptidoglycan editing by noncanonical d-amino acids. Microb. Drug Resist. 18:306–13
    [Google Scholar]
  69. 69. 
    Hugonnet JE, Mengin-Lecreulx D, Monton A, den Blaauwen T, Carbonnelle E et al. 2016. Factors essential for l,d-transpeptidase-mediated peptidoglycan cross-linking and β-lactam resistance in Escherichia coli. eLife 5:e19469
    [Google Scholar]
  70. 70. 
    Huq A, West PA, Small EB, Huq MI, Colwell RR. 1984. Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar 01 associated with live copepods in laboratory microcosms. Appl. Environ. Microbiol. 48:420–24
    [Google Scholar]
  71. 71. 
    Irazoki O, Hernandez SB, Cava F. 2019. Peptidoglycan muropeptides: release, perception, and functions as signaling molecules. Front. Microbiol. 10:500
    [Google Scholar]
  72. 72. 
    Jaishankar J, Srivastava P. 2017. Molecular basis of stationary phase survival and applications. Front. Microbiol. 8:2000
    [Google Scholar]
  73. 73. 
    Johnson JW, Fisher JF, Mobashery S. 2013. Bacterial cell-wall recycling. Ann. N. Y. Acad. Sci. 1277:54–75
    [Google Scholar]
  74. 74. 
    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. 93:113–28
    [Google Scholar]
  75. 75. 
    Kanjilal S, Citorik R, LaRocque RC, Ramoni MF, Calderwood SB. 2010. A systems biology approach to modeling Vibrio cholerae gene expression under virulence-inducing conditions. J. Bacteriol. 192:4300–10
    [Google Scholar]
  76. 76. 
    Keeler RF, Ritchie AE, Bryner JH, Elmore J 1966. The preparation and characterization of cell walls and the preparation of flagella of Vibrio fetus. J. Gen. Microbiol. 43:439–54
    [Google Scholar]
  77. 77. 
    Khutoryanskiy VV. 2015. Supramolecular materials: longer and safer gastric residence. Nat. Mater. 14:963–64
    [Google Scholar]
  78. 78. 
    Kim JS, Chowdhury N, Yamasaki R, Wood TK. 2018. Viable but non-culturable and persistence describe the same bacterial stress state. Environ. Microbiol. 20:2038–48
    [Google Scholar]
  79. 79. 
    Kim YK, McCarter LL. 2000. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 182:3693–704
    [Google Scholar]
  80. 80. 
    Knaysi G. 1930. The cell structure and cell division of Bacillus subtilis. J. Bacteriol. 19:113–15
    [Google Scholar]
  81. 81. 
    Knaysi G. 1941. Observations on the cell division of some yeasts and bacteria. J. Bacteriol. 41:141–53
    [Google Scholar]
  82. 82. 
    Koch AL. 2003. Bacterial wall as target for attack. Past Present Future Res 16:673–87
    [Google Scholar]
  83. 83. 
    Kondo K, Takade A, Amako K. 1994. Morphology of the viable but nonculturable Vibrio cholerae as determined by the freeze fixation technique. FEMS Microbiol. Lett. 123:179–84
    [Google Scholar]
  84. 84. 
    Krebs SJ, Taylor RK. 2011. Nutrient-dependent, rapid transition of Vibrio cholerae to coccoid morphology and expression of the toxin co-regulated pilus in this form. Microbiology 157:2942–53
    [Google Scholar]
  85. 85. 
    Kumar A, Sarkar SK, Ghosh D, Ghosh AS. 2012. Deletion of penicillin-binding protein 1b impairs biofilm formation and motility in Escherichia coli. Res. Microbiol. 163:254–57
    [Google Scholar]
  86. 86. 
    Lam H, Oh DC, Cava F, Takacs CN, Clardy J et al. 2009. d-Amino acids govern stationary phase cell wall remodeling in bacteria. Science 325:1552–55The first study describing the production and release of noncanonical d-amino acids and their role in peptidoglycan synthesis modulation.
    [Google Scholar]
  87. 87. 
    Lavollay M, Arthur M, Fourgeaud M, Dubost L, Marie A et al. 2008. The peptidoglycan of stationary-phase Mycobacterium tuberculosis predominantly contains cross-links generated by l,d-transpeptidation. J. Bacteriol. 190:4360–66
    [Google Scholar]
  88. 88. 
    Le NH, Peters K, Espaillat A, Sheldon JR, Gray J et al. 2020. Peptidoglycan editing provides immunity to Acinetobacter baumannii during bacterial warfare. Sci. Adv. 6:eabb5614
    [Google Scholar]
  89. 89. 
    Lee TK, Huang KC. 2013. The role of hydrolases in bacterial cell-wall growth. Curr. Opin. Microbiol. 16:760–66
    [Google Scholar]
  90. 90. 
    Lin HV, Massam-Wu T, Lin CP, Wang YA, Shen YC et al. 2017. The Vibrio cholerae var regulon encodes a metallo-β-lactamase and an antibiotic efflux pump, which are regulated by VarR, a LysR-type transcription factor. PLOS ONE 12:e0184255
    [Google Scholar]
  91. 91. 
    Lovering AL, Safadi SS, Strynadka NC. 2012. Structural perspective of peptidoglycan biosynthesis and assembly. Annu. Rev. Biochem. 81:451–78
    [Google Scholar]
  92. 92. 
    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. 133:10748–51
    [Google Scholar]
  93. 93. 
    Magnet S, Arbeloa A, Mainardi JL, Hugonnet JE, Fourgeaud M et al. 2007. Specificity of l,d-transpeptidases from gram-positive bacteria producing different peptidoglycan chemotypes. J. Biol. Chem. 282:13151–59
    [Google Scholar]
  94. 94. 
    Magnet S, Bellais S, Dubost L, Fourgeaud M, Mainardi JL et al. 2007. Identification of the l,d-transpeptidases responsible for attachment of the Braun lipoprotein to Escherichia coli peptidoglycan. J. Bacteriol. 189:3927–31
    [Google Scholar]
  95. 95. 
    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. 190:4782–85
    [Google Scholar]
  96. 96. 
    Mainardi JL, Fourgeaud M, Hugonnet JE, Dubost L, Brouard JP et al. 2005. A novel peptidoglycan cross-linking enzyme for a β-lactam-resistant transpeptidation pathway. J. Biol. Chem. 280:38146–52
    [Google Scholar]
  97. 97. 
    Mainardi JL, 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
    [Google Scholar]
  98. 98. 
    Martin NR, Blackman E, Bratton BP, Bartlett TM, Gitai Z. 2020. The evolution of bacterial shape complexity by a curvature-inducing module. bioRxiv 2020.02.20.954503. https://doi.org/10.1101/2020.02.20.954503
    [Crossref]
  99. 99. 
    McDonough MA, Anderson JW, Silvaggi NR, Pratt RF, Knox JR, Kelly JA. 2002. Structures of two kinetic intermediates reveal species specificity of penicillin-binding proteins. J. Mol. Biol. 322:111–22
    [Google Scholar]
  100. 100. 
    Meisel U, Holtje JV, Vollmer W. 2003. Overproduction of inactive variants of the murein synthase PBP1B causes lysis in Escherichia coli. J. Bacteriol. 185:5342–48
    [Google Scholar]
  101. 101. 
    Moll A, Dorr T, Alvarez L, Chao MC, Davis BM et al. 2014. Cell separation in Vibrio cholerae is mediated by a single amidase whose action is modulated by two nonredundant activators. J. Bacteriol. 196:3937–48
    [Google Scholar]
  102. 102. 
    Moll A, Dorr T, Alvarez L, Davis BM, Cava F, Waldor MK. 2015. A d,d-carboxypeptidase is required for Vibrio cholerae halotolerance. Environ. Microbiol. 17:527–40
    [Google Scholar]
  103. 103. 
    More N, Martorana AM, Biboy J, Otten C, Winkle M et al. 2019. Peptidoglycan remodeling enables Escherichia coli to survive severe outer membrane assembly defect. mBio 10:e02729-18
    [Google Scholar]
  104. 104. 
    Morita D, Takahashi E, Morita M, Ohnishi M, Mizuno T et al. 2020. Genomic characterization of antibiotic resistance–encoding genes in clinical isolates of Vibrio cholerae non-O1/non-O139 strains from Kolkata, India: generation of novel types of genomic islands containing plural antibiotic resistance genes. Microbiol. Immunol. 64:435–44
    [Google Scholar]
  105. 105. 
    Murphy SG, Alvarez L, Adams MC, Liu S, Chappie JS et al. 2019. Endopeptidase regulation as a novel function of the Zur-dependent zinc starvation response. mBio 10:1e02620-18
    [Google Scholar]
  106. 106. 
    Nambu T, Minamino T, Macnab RM, Kutsukake K. 1999. Peptidoglycan-hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J. Bacteriol. 181:1555–61
    [Google Scholar]
  107. 107. 
    Navarro Llorens JM, Tormo A, Martinez-Garcia E. 2010. Stationary phase in gram-negative bacteria. FEMS Microbiol. Rev. 34:476–95
    [Google Scholar]
  108. 108. 
    Nelson DE, Young KD. 2000. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J. Bacteriol. 182:1714–21
    [Google Scholar]
  109. 109. 
    Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S et al. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:1110–20
    [Google Scholar]
  110. 110. 
    Park JT, Uehara T. 2008. How bacteria consume their own exoskeletons (turnover and recycling of cell wall peptidoglycan). Microbiol. Mol. Biol. Rev. 72:211–27
    [Google Scholar]
  111. 111. 
    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
    [Google Scholar]
  112. 112. 
    Peters K, Kannan S, Rao VA, Biboy J, Vollmer D et al. 2016. The redundancy of peptidoglycan carboxypeptidases ensures robust cell shape maintenance in Escherichia coli. mBio 7:3e00819-16
    [Google Scholar]
  113. 113. 
    Ragunathan A, Malathi K, Anbarasu A. 2018. MurB as a target in an alternative approach to tackle the Vibrio cholerae resistance using molecular docking and simulation study. J. Cell Biochem. 119:1726–32
    [Google Scholar]
  114. 114. 
    Rahbar M, Saboorian R, Van de Velde S, Farzami MR, Mardani M. 2019. Activity of temocillin and comparators against clinical isolates of Vibrio cholerae from Iran. Eur. J. Clin. Microbiol. Infect. Dis. 38:615–16
    [Google Scholar]
  115. 115. 
    Roier S, Zingl FG, Cakar F, Durakovic S, Kohl P et al. 2016. A novel mechanism for the biogenesis of outer membrane vesicles in gram-negative bacteria. Nat. Commun. 7:10515
    [Google Scholar]
  116. 116. 
    Salton MR, Horne RW. 1951. Studies of the bacterial cell wall. I. Electron microscopical observations on heated bacteria. Biochim. Biophys. Acta 7:19–42
    [Google Scholar]
  117. 117. 
    Salton MR, Horne RW. 1951. Studies of the bacterial cell wall. II. Methods of preparation and some properties of cell walls. Biochim. Biophys. Acta 7:177–97
    [Google Scholar]
  118. 118. 
    Sandoz KM, Moore RA, Beare PA, Patel AV, Smith RE et al. 2020. β-Barrel proteins tether the outer membrane in many gram-negative bacteria. Nat. Microbiol. 6:19–26; https://doi.org/10.1038/s41564-020-00798-4
    [Crossref] [Google Scholar]
  119. 119. 
    Santin YG, Cascales E. 2017. Domestication of a housekeeping transglycosylase for assembly of a Type VI secretion system. EMBO Rep 18:138–49
    [Google Scholar]
  120. 120. 
    Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. 2008. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol. Rev. 32:234–58
    [Google Scholar]
  121. 121. 
    Schaefer K, Owens TW, Page JE, Santiago M, Kahne D, Walker S. 2020. Structure and reconstitution of a hydrolase complex that may release peptidoglycan from the membrane after polymerization. Nat. Microbiol. 6:34–43; https://doi.org/10.1038/s41564-020-00808-5
    [Crossref] [Google Scholar]
  122. 122. 
    Scheffers DJ, Tol MB. 2015. LipidII: just another brick in the wall?. PLOS Pathog 11:e1005213
    [Google Scholar]
  123. 123. 
    Scheurwater E, Reid CW, Clarke AJ. 2008. Lytic transglycosylases: bacterial space-making autolysins. Int. J. Biochem. Cell Biol. 40:586–91
    [Google Scholar]
  124. 124. 
    Schild S, Tamayo R, Nelson EJ, Qadri F, Calderwood SB, Camilli A. 2007. Genes induced late in infection increase fitness of Vibrio cholerae after release into the environment. Cell Host Microbe 2:264–77
    [Google Scholar]
  125. 125. 
    Schleifer KH, Kandler O. 1972. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol. Rev. 36:407–77
    [Google Scholar]
  126. 126. 
    Schwechheimer C, Rodriguez DL, Kuehn MJ 2015. NlpI-mediated modulation of outer membrane vesicle production through peptidoglycan dynamics in Escherichia coli. Microbiologyopen 4:375–89
    [Google Scholar]
  127. 127. 
    Sengupta TK, Chatterjee AN, Das J. 1990. Penicillin binding proteins of Vibrio cholerae. Biochem. Biophys. Res. Commun. 171:1175–81
    [Google Scholar]
  128. 128. 
    Sengupta TK, Chaudhuri K, Majumdar S, Lohia A, Chatterjee AN, Das J. 1992. Interaction of Vibrio cholerae cells with β-lactam antibiotics: emergence of resistant cells at a high frequency. Antimicrob. Agents Chemother. 36:788–95
    [Google Scholar]
  129. 129. 
    Senoh M, Ghosh-Banerjee J, Ramamurthy T, Hamabata T, Kurakawa T et al. 2010. Conversion of viable but nonculturable Vibrio cholerae to the culturable state by co-culture with eukaryotic cells. Microbiol. Immunol. 54:502–7
    [Google Scholar]
  130. 130. 
    Sham LT, Butler EK, Lebar MD, Kahne D, Bernhardt TG, Ruiz N. 2014. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345:220–22
    [Google Scholar]
  131. 131. 
    Shin JH, Sulpizio AG, Kelley A, Alvarez L, Murphy SG et al. 2020. Structural basis of peptidoglycan endopeptidase regulation. PNAS 117:11692–702
    [Google Scholar]
  132. 132. 
    Signoretto C, Lleo M, Canepari P. 2002. Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Curr. Microbiol. 44:125–31
    [Google Scholar]
  133. 133. 
    Stenstrom TA, Conway P, Kjelleberg S 1989. Inhibition by antibiotics of the bacterial response to long-term starvation of Salmonella typhimurium and the colon microbiota of mice. J. Appl. Bacteriol. 67:53–59
    [Google Scholar]
  134. 134. 
    Stubbs KA, Balcewich M, Mark BL, Vocadlo DJ. 2007. Small molecule inhibitors of a glycoside hydrolase attenuate inducible AmpC-mediated β-lactam resistance. J. Biol. Chem. 282:21382–91
    [Google Scholar]
  135. 135. 
    Sur P, Chatteejee SN. 1972. Chemical composition of isolated cell walls of Vibrio cholerae. Bull. Calcutta Sch. Trop. Med. 20:23–24
    [Google Scholar]
  136. 136. 
    Taguchi A, Welsh MA, Marmont LS, Lee W, Sjodt M et al. 2019. FtsW is a peptidoglycan polymerase that is functional only in complex with its cognate penicillin-binding protein. Nat. Microbiol. 4:587–94
    [Google Scholar]
  137. 137. 
    Templin MF, Ursinus A, Holtje JV. 1999. A defect in cell wall recycling triggers autolysis during the stationary growth phase of Escherichia coli. EMBO J 18:4108–17
    [Google Scholar]
  138. 138. 
    Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J et al. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097–109
    [Google Scholar]
  139. 139. 
    Uehara T, Parzych KR, Dinh T, Bernhardt TG. 2010. Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J 29:1412–22
    [Google Scholar]
  140. 140. 
    Urakawa H, Rivera I 2006. Aquatic environment. The Biology of Vibrios F Thompson, B Austin, J Swings 175–89 Washington, DC: ASM Press
    [Google Scholar]
  141. 141. 
    van Heijenoort J. 2001. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11:25R–36R
    [Google Scholar]
  142. 142. 
    Verma J, Bag S, Saha B, Kumar P, Ghosh TS et al. 2019. Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. PNAS 116:6226–31
    [Google Scholar]
  143. 143. 
    Vollmer W, Blanot D, de Pedro MA. 2008. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32:149–67
    [Google Scholar]
  144. 144. 
    Wang R, Liu H, Zhao X, Li J, Wan K 2018. IncA/C plasmids conferring high azithromycin resistance in Vibrio cholerae. Int. J. Antimicrob. Agents 51:140–44
    [Google Scholar]
  145. 145. 
    Weaver AI, Jimenez-Ruiz V, Tallavajhala SR, Ransegnola BP, Wong KQ, Dorr T 2019. Lytic transglycosylases RlpA and MltC assist in Vibrio cholerae daughter cell separation. Mol. Microbiol. 112:1100–15Analyzes Vibrio cholerae's lytic transglycosylases and the role of RlpA and MltC in division.
    [Google Scholar]
  146. 146. 
    Weaver AI, Murphy SG, Umans BD, Tallavajhala S, Onyekwere I et al. 2018. Genetic determinants of penicillin tolerance in Vibrio cholerae. Antimicrob. Agents Chemother. 62:10e01326-18
    [Google Scholar]
  147. 147. 
    Weichart D, Kjelleberg S. 1996. Stress resistance and recovery potential of culturable and viable but nonculturable cells of Vibrio vulnificus. Microbiology 142:Part 4845–53
    [Google Scholar]
  148. 148. 
    Weidel W, Pelzer H. 1964. Bagshaped macromolecules—a new outlook on bacterial cell walls. Adv. Enzymol. Relat. Subj. Biochem. 26:193–232
    [Google Scholar]
  149. 149. 
    Xu HS, Roberts N, Singleton FL, Attwell RW, Grimes DJ, Colwell RR. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8:313–23
    [Google Scholar]
  150. 150. 
    Yadav AK, Espaillat A, Cava F. 2018. Bacterial strategies to preserve cell wall integrity against environmental threats. Front. Microbiol. 9:2064
    [Google Scholar]
  151. 151. 
    Yakhnina AA, Bernhardt TG 2020. The Tol-Pal system is required for peptidoglycan-cleaving enzymes to complete bacterial cell division. PNAS 117:6777–83
    [Google Scholar]
  152. 152. 
    Yamamoto T, Nair GB, Takeda Y. 1995. Emergence of tetracycline resistance due to a multiple drug resistance plasmid in Vibrio cholerae O139. FEMS Immunol. Med. Microbiol. 11:131–36
    [Google Scholar]
  153. 153. 
    Yu YJ, Wang XH, Fan GC. 2018. Versatile effects of bacterium-released membrane vesicles on mammalian cells and infectious/inflammatory diseases. Acta Pharmacol. Sin. 39:514–33
    [Google Scholar]
  154. 154. 
    Zeng X, Lin J. 2013. β-Lactamase induction and cell wall metabolism in gram-negative bacteria. Front. Microbiol. 4:128
    [Google Scholar]
  155. 155. 
    Zhao H, Patel V, Helmann JD, Dorr T. 2017. Don't let sleeping dogmas lie: new views of peptidoglycan synthesis and its regulation. Mol. Microbiol. 106:847–60
    [Google Scholar]
/content/journals/10.1146/annurev-micro-040621-122027
Loading
/content/journals/10.1146/annurev-micro-040621-122027
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error