Advertisement

Controlling Autolysis During Flagella Insertion in Gram-Negative Bacteria

  • Francesca A. Herlihey
  • Anthony J. ClarkeEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 925)

Abstract

The flagellum is an important macromolecular machine for many pathogenic bacteria. It is a hetero-oligomeric structure comprised of three major sub-structures: basal body, hook and thin helical filament. An important step during flagellum assembly is the localized and controlled degradation of the peptidoglycan sacculus to allow for the insertion of the rod as well as to facilitate anchoring for proper motor function. The peptidoglycan lysis events require specialized lytic enzymes, β-N-acetylglucosaminidases and lytic transglycosylases, which differ in flagellated proteobacteria. Due to their autolytic activity, these enzymes need to be controlled in order to prevent cellular lysis. This review summarizes are current understanding of the peptidoglycan lysis events required for flagellum assembly and motility with a main focus on Gram-negative bacteria.

Keywords

Flagella Peptidoglycan Lytic transglycosylases β-N-acetylglucosaminidases 

Abbreviations

PG

peptidoglycan

MurNAc

N-acetylmuramic acid

GlcNAc

N-acetylglucosamine

PBP

penicillin-binding proteins

LT

lytic transglycosylase

T3SS

type three secretion system

Mot

motor

OmpA

outer membrane protein A

PGB

peptidoglycan binding

Mlt

membrane-bound lytic transglycosylases

Slt

soluble lytic transglycosylases

GH

glycoside hydrolase

StFlgJ

Salmonella Typhimurium FlgJ

PDB

Protein Data Bank

SAC

substrate-assisted catalysis

RlpA

rare lipoprotein A

1,6-anhydroMurNAc

1,6-anhydromuramic acid

NAG thiazoline

N-acetylglucosamine thiazoline.

Notes

Acknowledgements

Research on the lytic transglycosylases and their control continues to be funded by an operating grant to AJC from the Natural Sciences and Engineering Research Council of Canada (NSERC; RGPN 03965–2016).

Conflict of Interest

The authors declare no conflict of interest.

References

  1. Aika T, Yoshimura H, Namba K (1990) Monolayer crystallization of flagellar L-P rings by sequential addition and depletion of lipid. Science 252:1544–1546Google Scholar
  2. Artola-Recolons C, Carrasco-López C, Llarrull LI, Kumarasiri M, Lastochkin E, Martínez de Ilarduya I, Meindl K, Usón I, Mobashery S, Hermoso JA (2011) High-resolution crystal structure of an outer membrane-anchored endolytic peptidoglycan lytic transglycosylases (MltE) from Escherichia coli. Biochemistry 50(13):2384–2386CrossRefPubMedGoogle Scholar
  3. Artola-Recolons C, Lee M, Bernardo-García N, Blázquez B, Hesek D, Bartual SG, Mahasenan KV, Lastochkin E, Pi H, Boggess B, Meindl K, Usón I, Fischer JF, Mobashery S, Hermoso JA (2014) Structure and cell wall cleavage by modular lytic transglycosylases MltC of Escherichia coli. ACS Chem Biol 9:2058–2066CrossRefPubMedPubMedCentralGoogle Scholar
  4. Asai Y, Kojima S, Kato H, Nishioka N, Kawagishi I, Homma M (1997) Putative channel components for the fast-rotating sodium-driven flagellar motor of a marine bacterium. J Bacteriol 176(16):5104–5110CrossRefGoogle Scholar
  5. Bai XH, Chen HJ, Jiang YL, Wen Z, Huang Y, Cheng W, Li Q, Qi L, Zhang JR, Chen Y, Zhou CZ (2014) Structure of pneumococcal peptidoglycan hydrolase LytB reveals insights into the bacterial cell wall remodeling and pathogenesis. J Biol Chem 289:23403–23416CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blackburn NT, Clarke AJ (2001) Identification of four families of peptidoglycan lytic transglycosylases. J Mol Evol 52:78–84CrossRefPubMedGoogle Scholar
  7. Bublitz M, Polle L, Holland C, Heinz DW, Nimtz M, Schubert W (2009) Structural basis for autoinhibition and activation of Auto, a virulence- associated peptidoglycan hydrolase of Listeria monocytogenes. Mol Microbiol 71:1509–1522CrossRefPubMedGoogle Scholar
  8. Burkinshaw BJ, Deng W, Lameignѐre E, Wasney GA, Zhu H, Worrall LJ, Finlay BB, Strynadka NC (2015) Structural analysis of a specialized type III secretion system peptidoglycan-cleaving enzyme. J Biol Chem 290:10406–10417CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chen R, Guttenplan SB, Blair KM, Kearns DB (2009) Role of the σD-dependent autolysins in Bacillus subtilis population heterogeneity. J Bacteriol 191(18):5775–5784CrossRefPubMedGoogle Scholar
  10. Clarke CA, Scheurwater EM, Clarke AJ (2010) The vertebrate lysozyme inhibitor Ivy functions to inhibit the activity of lytic transglycosylases. J Biol Chem 285:14843–14847CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cohen EJ, Hughes KT (2014) Rod-to-hook transition for extracellular flagellum assembly is catalyzed by the L-ring dependent rod scaffold removal. J Bacteriol 196:2387–2395CrossRefPubMedPubMedCentralGoogle Scholar
  12. Davies GJ, Wilson KS, Henrissat B (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J 321:557–559CrossRefPubMedPubMedCentralGoogle Scholar
  13. de la Mora J, Ballado T, González-Pedrajo B, Camerena L, Dreyfus G (2007) The flagellar muramidase from the photosynthetic bacterium Rhodobacter sphaeroides. J Bacteriol 189:7998–8004CrossRefPubMedPubMedCentralGoogle Scholar
  14. de la Mora J, Osorio-Valeriano M, González-Pedrajo B, Ballado T, Camarena L, Dreyfus G (2012) The C terminus of the flagellar muramidase SltF modulates the interaction with FlgJ in Rhodobacter sphaeroides. J Bacteriol 194:4513–4520CrossRefPubMedPubMedCentralGoogle Scholar
  15. De Mot R, Vanderleyden J (1994) The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both Gram-positive and Gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan. Mol Microbiol 12(2):333–334CrossRefPubMedGoogle Scholar
  16. Demchick P, Koch AL (1996) The permeability of the wall fabric of Escherichia coli and Bacillus substilis. J Bacteriol 178(3):768–773CrossRefPubMedPubMedCentralGoogle Scholar
  17. Drouillard S, Armand S, Davies GJ, Vorgias CE, Henrissat B (1997) Serratia marcescens chitobiase is a retaining glycosidase utilizing substrate acetamido group participation. Biochem J 328:945–949CrossRefPubMedPubMedCentralGoogle Scholar
  18. González-Pedrajo B, de la Mora J, Ballado T, Camerena L, Dreyfus G (2002) Characterization of the flgG operon of Rhodobacter sphaeroides WS8 and its role in flagellum biosynthesis. Biochim Biophys Acta 1579:55–63CrossRefPubMedGoogle Scholar
  19. Gumbart JC, Beeby M, Jensen GJ, Roux B (2014) Escherichia coli peptidoglycan structure and mechanics as predicted by atomic-scale stimulations. PLoS Comput Biol 10(2):e1003475. doi: 10.1371/journal.pcbi.1003475 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Hashimoto W, Ochiai A, Momma K, Itoh T, Mikami B, Maruyama Y, Murata K (2009) Crystal structure of the glycosidase family 73 peptidoglycan hydrolase FlgJ. Biochem Biophys Res Commun 381(1):16–21CrossRefPubMedGoogle Scholar
  21. 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(45):31029–31042CrossRefPubMedPubMedCentralGoogle Scholar
  22. Herlihey FA, Osorio-Valeriano M, Dreyfus G, Clarke AJ (2016) Modulation of the lytic activity of the dedicated autolysin for flagella formation SltF by flagella rod proteins FlgB and FlgF. J Bacteriol. doi: 10.1128/JB.00203-16 Google Scholar
  23. 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 312:359–369CrossRefPubMedGoogle Scholar
  24. Hizukuri Y, Morton JF, Yakushi T, Kojima S, Homma M (2009) The peptidoglycan-binding (PGB) domain of the Escherichia coli Pal protein can also function as the PGB domain in E. coli flagellar motor protein MotB. J Biochem 146:219–229CrossRefPubMedGoogle Scholar
  25. Holtje J-V (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203PubMedPubMedCentralGoogle Scholar
  26. Hӧltje JV, Mirelman D, Sharon N, Schwarz U (1975) Novel type of murein transglycosylases in Escherichia coli. J Bacteriol 124:1067–1076Google Scholar
  27. Homma M, Komeda Y, Iino T, Macnab RM (1987) The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export. J Bacteriol 169:1493–1498CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hӧpper C, Carle A, Sivanesan D, Hoeppner S, Baron C (2005) The putative lytic transglycosylases VirB from Brucella suis interacts with the type IV secretion system core components VirB8, VirB9 and VirB11. Microbiology 151:3469–3482CrossRefGoogle Scholar
  29. Hoskin ER, Vogt C, Bakker EP, Manson MD (2006) The Escherichia coli MotAB proton channel unplugged. J Mol Biol 364:921–937CrossRefGoogle Scholar
  30. Inagaki N, Iguchi A, Yokoyama T, Yokoi KJ, Ono Y, Yamakawa A, Taketo A, Kodaira K (2009) Molecular properties of the glucosaminidase AcmA from Lactococcus lactis MG1363: mutational and biochemical analyses. Gene 447(2):61–71CrossRefPubMedGoogle Scholar
  31. Jorgenson MA, Chen Y, Yahashiri A, Popham DL, Weiss DS (2014) The bacterial septal ring protein RlpA is a lytic transglycosylases that contributes to rod shape and daughter cell separation in Pseudomonas aeruginosa. Mol Microbiol 93(1):113–128CrossRefPubMedPubMedCentralGoogle Scholar
  32. Knapp S, Vocadlo DJ, Gao Z, Kirk B, Lou J, Withers SG (1996) NAG-thiazoline, An N-Acetyl-β-hexosaminidase inhibitor that implicates acetamido participation. J Am Chem Soc 118:6804–6805CrossRefGoogle Scholar
  33. Kojima S, Blair DF (2001) Conformational change in the stator of the bacterial flagellar motor. Biochemistry 40:13041–13050CrossRefPubMedGoogle Scholar
  34. Kojima S, Imada K, Sakuma M, Sudo Y, Kojima C, Minamino T, Homma M, Namba K (2008a) Stator assembly and activation mechanism of the flagellar motor by the periplasmic region of MotB. Mol Microbiol 73:710–718CrossRefGoogle Scholar
  35. Kojima S, Shinohara A, Terashima H, Yakushi T, Sakuma M, Homma M, Namba K, Imada K (2008b) Insights into the stator assembly of the Vibrio flagellar motor from the crystal structure of MotY. Proc Natl Acad Sci U S A 105(22):7696–7701CrossRefPubMedPubMedCentralGoogle Scholar
  36. Koushik P, Erhardt M, Hirano T, Blair DF, Hughes KT (2008) Energy source of flagellar type III secretion. Nature 451:489–492CrossRefGoogle Scholar
  37. Kubori T, Shimamoto N, Shigeru Y, Namba K, Aizawa S-I (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J Mol Biol 226:433–446CrossRefPubMedGoogle Scholar
  38. Lee M, Hesek D, Llarrull LI, Lastochkin E, Pi H, Boggess B, Mobashery S (2013) Reactions of all E. coli lytic transglycosylases with bacterial cell wall. J Am Chem Soc 135(9):3311–3314CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lee M, Domínguez-Gil T, Hesek D, Mahasenan KV, Lastochkin E, Hermoso JA, Mobashery S (2016) Turnover of bacterial cell wall by SltB3, a multidomain lytic transglycosylases of Pseudomonas aeruginosa. ACS Chem Biol. doi: 10.1021/acschembio.6b00194 Google Scholar
  40. Legaree BA, Clarke AJ (2008) Interaction of penicillin-binding protein 2 with soluble lytic transglycosylases B1 in Pseudomonas aeruginosa. J Bacteriol 190(20):6922–6926CrossRefPubMedPubMedCentralGoogle Scholar
  41. Leung AKW, Duewel HS, Honek JF, Berghuis AM (2001) Crystal structure of the lytic transglycosylases from bacteriophage lambda in complex with hexa-N-acetylchitohexaose. Biochemistry 40:5665–5673CrossRefPubMedGoogle Scholar
  42. Lipski A, Hervé M, Lombard V, Nurizzo D, Mengin-Lecreulx D, Bourne Y, Vincent F (2015) Structural and biochemical characterization of the β-N-acetylglucosaminidase from Thermotoga maritima: toward rationalization of mechanistic knowledge in the GH73 family. Glycobiology 25(3):319–330CrossRefPubMedGoogle Scholar
  43. Lombard V, Golaconda Ramulu H, Drula E, Countinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495CrossRefPubMedGoogle Scholar
  44. Macdonald JM, Tarling CA, Taylor EJ, Dennis RJ, Myers DS, Knapp S, Davies GJ, Withers SG (2010) Chitinase inhibition by chitobiose and chitotriose thiazolines. Angew Chem Int Ed Engl 49(14):2599–2602CrossRefPubMedGoogle Scholar
  45. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 577:77–100CrossRefGoogle Scholar
  46. Maruyama Y, Ochiai A, Itoh T, Mikami B, Hashimoto W, Murata K (2010) Mutational studies of the peptidoglycan hydrolase FlgJ of Sphingomonas sp. strain A1. J Basic Microbiol 50(4):311–317CrossRefPubMedGoogle Scholar
  47. McCarter JD, Withers SG (1994) Mechanisms of enzymatic glycoside hydrolysis. Curr Opin Struct Biol 4:885–892CrossRefPubMedGoogle Scholar
  48. Minamino T, Imada K (2015) The bacterial flagellar motor and its structural diversity. Trends Microbiol 23(5):267–274CrossRefPubMedGoogle Scholar
  49. Minamino T, Macnab RM (1999) Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181:1388–1394PubMedPubMedCentralGoogle Scholar
  50. Minaminoa T, Namba K (2008) Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 451:485–488CrossRefGoogle Scholar
  51. Moynihan PJ, Clarke AJ (2011) O-Acetylated peptidoglycan: controlling the activity of bacterial autolysins and lytic enzymes of innate immune systems. Int J Biochem Cell Biol 43:1655–1659CrossRefPubMedGoogle Scholar
  52. 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 181:1555–1561PubMedPubMedCentralGoogle Scholar
  53. Nambu T, Inagaki Y, Kutsukake K (2006) Plasticity of the domain structure in FlgJ, a bacterial protein involved in flagellar rod formation. Genes Genet Syst 81:381–389CrossRefPubMedGoogle Scholar
  54. Nikolaidis I, Izore T, Job V, Thielens N, Breukink E, Dessen A (2012) Calcium-dependent complex formation between PBP2 and lytic transglycosylases SltB1. Microb Drug Resist 18:298–305CrossRefPubMedGoogle Scholar
  55. Osorio-Valeriano M, de la Mora J, Camarena L, Dreyfus G (2016) Biochemical characterization of the flagellar rod components of Rhodobacter sphaeroides: properties and interactions. J Bacteriol 198(3):544–552CrossRefPubMedCentralGoogle Scholar
  56. Park JS, Lee WC, Yeo KJ, Ryu K-S, Kumarasiri M, Hesek D, Lee M, Mobashery S, Song JH, Kim SI, Lee JC, Cheong C, Jeon YH, Kim H-Y (2012) Mechanism of anchoring of OmpA protein to the cell wall peptidoglycan of the gram-negative bacterial outer membrane. FASEB J 26(1):219–228CrossRefPubMedPubMedCentralGoogle Scholar
  57. Parsons LM, Lin F, Orban J (2006) Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45:2122–2128CrossRefPubMedGoogle Scholar
  58. Pfeffer JM, Moynihan PJ, Clarke CA, Clarke AJ (2012) Control of lytic transglycosylase activity within bacterial cell walls. In: Reid, Twine, Read (eds) Bacterial glycomics. Caister Academic Press, Norfolk, pp 55–68Google Scholar
  59. Powell AJ, Liu ZJ, Nicholas RA, Davies C (2006) Crystal structure of the lytic transglycosylases MltA from N. gonorrhoeae and E. coli: insights into interdomain movements and substrate binding. J Mol Biol 359:122–136CrossRefPubMedGoogle Scholar
  60. Reboul CF, Andrews DA, Nahar MF, Buckle AM, Roujeinikova A (2011) Crystallographic and molecular dynamics analysis of loop motions unmasking the peptidoglycan-binding site in stator protein MotB of flagellar motor. PLoS One 6(4):e18981. doi: 10.1371/journal.pone.0018981 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Reid CW, Blackburn NT, Legaree BA, Auzanneau F-I, Clarke AJ (2004) Inhibition of membrane-bound lytic transglycosylase B by NAG-thiazoline. FEBS Lett 574:73–79CrossRefPubMedGoogle Scholar
  62. Reid CW, Legaree BA, Clarke AJ (2007) Role of Ser216 in the mechanism of action of membrane-bound lytic transglycosylases B: further evidence for substrate-assisted catalysis. FEBS Lett 581:4988–4992CrossRefPubMedGoogle Scholar
  63. Rico-Lastres P, Díez-Martínez R, Iglesias-Bexiga M, Bustamante N, Aldridge C, Hesek D, Lee M, Mobashery S, Gray J, Vollmer W, Garcia P, Menéndez M (2015) Substrate recognition and catalysis by LytB, a pneumococcal peptidoglycan hydrolase involved in virulence. Sci Rep 5:16198CrossRefPubMedPubMedCentralGoogle Scholar
  64. Romeis T, Hӧltje JV (1994) Specific interaction of penicillin-binding proteins 3 and 7/8 with soluble lytic transglycosylases in Escherichia coli. J Biol Chem 269(34):21603–21607PubMedGoogle Scholar
  65. Roujeinikova A (2008) Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: implications for peptidoglycan recognition. Proc Natl Acad Sci U S A 105:10348–10353CrossRefPubMedPubMedCentralGoogle Scholar
  66. Roure S, Bonis M, Chaput C, Ecobichon C, Mattox A, Barriѐre C, Geldmacher N, Guadagnini S, Schmitt C, Prѐvost MC, Labigne A, Backert S, Ferrero RL, Boneca IG (2012) Peptidoglycan maturation enzymes affect flagellar functionality in bacteria. Mol Micrbiol 86:845–856CrossRefGoogle Scholar
  67. Scheurwater EM, Clarke AJ (2008) The C-terminal domain of Escherichia coli YhfD functions as a lytic transglycosylases. J Biol Chem 283(13):8363–8373CrossRefPubMedPubMedCentralGoogle Scholar
  68. Scheurwater E, Reid CW, Clarke AJ (2008) Lytic transglycosylases: bacterial space-making autolyins. Int J Biochem Cell Biol 40:586–591CrossRefPubMedGoogle Scholar
  69. Strating H, Vandenende C, Clarke AJ (2012) Changes in peptidoglycan structure and metabolism during differentiation of Proteus mirabilis into swarmer cells. Can J Microbiol 58:1183–1194CrossRefPubMedGoogle Scholar
  70. Sudiarta IP, Fukushima T, Sekiguchi J (2010) Bacillus subtilis CwlQ (previously YjbJ) is a bifunctional enzyme exhibiting muramidase and soluble-lytic transglycosylases activities. Biochem Biophys Rec Commun 398:606–612CrossRefGoogle Scholar
  71. Suzuki H, Yonekura K, Murata K, Hirai T, Oosawa K, Namba K (1998) A structural feature in the central channel of the bacterial flagellar FliE ring complex is implicated in type III protein export. J Struct Biol 124:104–114CrossRefPubMedGoogle Scholar
  72. Terashima H, Fukuoka H, Yakushi T, Kojima S, Homma M (2006) The Vibrio motor proteins, MotX and MotY, are associated with the basal body of Na+-driven flagella and required for stator formation. Mol Microbiol 62(4):1170–1180CrossRefPubMedGoogle Scholar
  73. Terashima H, Koike M, Kojima S, Homma M (2010) The flagellar basal body-associated protein FlgT is essential for a novel ring structure in the sodium-driven Vibrio motor. J Bacteriol 192(21):5609–5615CrossRefPubMedPubMedCentralGoogle Scholar
  74. Terwisscha van Scheltinga AC, Armand S, Kalk KH, Isogai A, Henrissat B, Dijkstra BW (1995) Stereochemistry of chitin hydrolysis by a plant chitinase/lysozyme and x-ray structure of a complex with allosamidin: evidence for substrate assisted catalysis. Biochemistry 34:15619–15623CrossRefPubMedGoogle Scholar
  75. Tews I, Perrakis A, Oppenheim A, Dauter Z, Wilson KS, Vorgias CE (1996) Bacterial chitobiase structure provides insight into catalytic mechanism and the basis of Tay-Sachs disease. Nat Struct Biol 3:638–648CrossRefPubMedGoogle Scholar
  76. Thunnissen A-MWH, Isaacs NW, Dijkstra BW (1995) The catalytic domain of a bacterial lytic transglycosylases defines a novel class of lysozymes. Proteins 22:245–258CrossRefPubMedGoogle Scholar
  77. van Asselt EJ, Dijkstra AJ, Kalk KH, Takacs B, Keck W, Dijkstra BW (1999a) Crystal structure of Escherichia coli lytic transglycosylases Slt35 reveals a lysozyme-like catalytic domain with an EF-hand. Structure 7:1167–1180CrossRefPubMedGoogle Scholar
  78. van Asselt EJ, Thunnissen A-MWH, Dijkstra BW (1999b) High resolution crystal structures of the Escherichia coli lytic transglycosylases Slt70 and its complex with a peptidoglycan fragment. J Mol Biol 291:877–898CrossRefPubMedGoogle Scholar
  79. van Asselt EJ, Kalk KH, Dijkstra BW (2000) Crystallographic studies of the interactions of Escherichia coli lytic transglycosylases Slt35 with peptidoglycan. Biochemistry 39:1924–1934CrossRefPubMedGoogle Scholar
  80. van Straaten KE, Dijkstra BW, Vollmer W, Thunnissen A-MWH (2005) Crystal structure of MltA from Escherichia coli reveals a unique lytic transglycosylases fold. J Mol Biol 353:1068–1082CrossRefGoogle Scholar
  81. Vázquez-Laslop N, Hyunwoo L, Hu R, Neyfakh AA (2001) Molecular sieve mechanism of selective release of cytoplasmic proteins by osmotically shocked Escherichia coli. J Bacteriol 183(8):2399–2404CrossRefPubMedPubMedCentralGoogle Scholar
  82. Viollier PH, Shapiro L (2003) A lytic transglycosylases homologue, PleA, is required for the assembly of pili and the flagellum at the Caulobacter crescentus cell pole. Mol Microbiol 49:331–345CrossRefPubMedGoogle Scholar
  83. Vollmer W, Bertsche U (2008) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli. Biochim Biophys Acta 1178:1714–1734CrossRefGoogle Scholar
  84. Vollmer W, Joris B, Charlier P, Foster S (2008) Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol Rev 32:259–286CrossRefPubMedGoogle Scholar
  85. Weadge JT, Clarke AJ (2005) Identification and characterization of O-acetylpeptidoglycan esterase: a novel enzyme discovered in Neisseria gonorrhoeae. Biochemistry 45:839–851CrossRefGoogle Scholar
  86. Yokoi KJ, Sugahara K, Iguchi A, Nishitani G, Ikeda M, Shimada T, Inagaki N, Yamakawa A, Taketo A, Kodaira K (2008) Molecular properties of the putative autolysin Atl(WM) encoded by Staphylococcus warneri M: mutational and biochemical analyses of the amidase and glucosaminidase domains. Gene 416(1–2):66–76CrossRefPubMedGoogle Scholar
  87. Yunck R, Hongbaek C, Bernhardt TG (2016) Identification of MltG as a potential terminase for peptidoglycan polyermization in bacteria. Mol Microbiol 99(4):700–718CrossRefPubMedGoogle Scholar
  88. Zabola P, Bailey-Elkin BA, Derksen M, Mark BL (2016) Structural and biochemical insights into the peptidoglycan hydrolase domain of FlgJ from Salmonell typhimurium. PLoS One 11(2):e0149204CrossRefGoogle Scholar
  89. Zhao X, Zhang K, Boquoi T, Hu B, Motaleb MA, Miller KA, James ME, Charon NW, Manson MD, Norris SJ, Li C, Liu J (2013) Cryoelectron tomography reveals the sequential assembly of bacterial flagellum in Borrelia burgdorferi. Proc Natl Acad Sci U S A 110(35):14390–14395CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zhu S, Takao M, Li N, Sakuma M, Nishino Y, Homma M, Kojima S, Imada K (2014) Conformational change in the periplasmic region of the flagellar stator coupled with the assembly around the rotor. Proc Natl Acad Sci U S A 111(37):13523–13528CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Molecular and Cellular BiologyUniversity of GuelphGuelphCanada

Personalised recommendations