Advertisement

Gram-Negative Bacteria: The cell Membranes

  • S N ChatterjeeEmail author
  • Keya Chaudhuri
Chapter
Part of the SpringerBriefs in Microbiology book series (BRIEFSMICROBIOL)

Abstract

This chapter presents a brief outline of our current knowledge of the structures of the bounding membranes (the inner and the outer membranes and the intermediate periplasmic layer) of a Gram-negative bacterial cell. Also the structure and chemical composition of the outer membrane vesicles (OMVs) originating from the surface of these bacteria including their proteomic profile, as obtained mainly by mass spectroscopic and related studies, have been presented in brief.

Keywords

Inner membrane Outer membrane Peptidoglycan OMVs Structure Chemical composition Mass spectrometry Protein profile 

References

  1. Allan ND, Beveridge TJ (2003) Gentamicin delivery to Burkholderia cepacia group IIIa strains via membrane vesicles from Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 47:2962–2965PubMedCrossRefGoogle Scholar
  2. Allan ND, Kooi C, Sokol PA, Beveridge TJ (2003) Putative virulence factors are released in association with membrane vesicles from Burkholderia cepacia. Can J Microbiol 49:613–624PubMedCrossRefGoogle Scholar
  3. Balsalobre C, Silvan JM, Berglund S, Mizunoe Y, Uhlin BE, Wai SN (2006) Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol Microbiol 59:99–112PubMedCrossRefGoogle Scholar
  4. Bauman SJ, Kuehn MJ (2006) Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect 8:2400–2408PubMedCrossRefGoogle Scholar
  5. Bergman MA, Cummings LA, Barrett SL, Smith KD, Lara JC, Aderem A, Cookson BT (2005) CD4+ T cells and toll-like receptors recognize Salmonella antigens expressed in bacterial surface organelles. Infect Immun 73:1350–1356PubMedCrossRefGoogle Scholar
  6. Berlanda Scorza F, Doro F, Rodriguez-Ortega MJ, Stella M, Liberatori S et al (2008) Proteomics characterization of outer membrane vesicles from the extraintestinal pathogenic Escherichia coli DeltatolR IHE3034 mutant. Mol Cell Proteomics 7:473–485PubMedGoogle Scholar
  7. Beveridge TJ (1999) Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733PubMedGoogle Scholar
  8. Bjerre A, Brusletto B, Rosenqvist E, Namork E, Kierulf P et al (2000) Cellular activating properties and morphology of membrane-bound and purified meningococcal lipopolysaccharide. J Endotoxin Res 6:437–445PubMedGoogle Scholar
  9. Boardman BK, Meehan BM, Fullner Satchell KJ (2007) Growth phase regulation of Vibrio cholerae RTX toxin export. J Bacteriol 189:1827–1835PubMedCrossRefGoogle Scholar
  10. Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O’Toole GA, Stanton BA (2009) Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5:e1000382PubMedCrossRefGoogle Scholar
  11. 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 585:1357–1362PubMedCrossRefGoogle Scholar
  12. Chatterjee SN, Das J (1966) Secretory activity of Vibrio cholerae as evidenced by electron microscopy. In: Uyeda (ed) Electron microscopy, Maruzen Co. Ltd, TokyoGoogle Scholar
  13. Chatterjee SN, Das J (1967) Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J Gen Microbiol 49:1–11PubMedCrossRefGoogle Scholar
  14. Chatterjee SN, Chaudhuri K (2003) Lipopolysaccharides of Vibrio cholerae. I. Physical and chemical characterization. Biochim Biophys Acta 1639:65–79PubMedCrossRefGoogle Scholar
  15. Chaudhuri K, Chatterjee SN (2009) Cholera toxins. Springer, HeidelbergCrossRefGoogle Scholar
  16. Chi B, Qi M, Kuramitsu HK (2003) Role of dentilisin in Treponema denticola epithelial cell layer penetration. Res Microbiol 154:637–643PubMedCrossRefGoogle Scholar
  17. Ciofu O, Beveridge TJ, Kadurugamuwa J, Walther-Rasmussen J, Hoiby N (2000) Chromosomal beta-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa. J Antimicrob Chemother 45:9–13PubMedCrossRefGoogle Scholar
  18. Cota-Gomez A, Vasil AI, Kadurugamuwa J, Beveridge TJ, Schweizer HP, Vasil ML (1997) PlcR1 and PlcR2 are putative calcium-binding proteins required for secretion of the hemolytic phospholipase C of Pseudomonas aeruginosa. Infect Immun 65:2904–2913PubMedGoogle Scholar
  19. Deatherage BL, Lara JC, Bergsbaken T, Rassoulian Barrett SL, Lara S, Cookson BT (2009) Biogenesis of bacterial membrane vesicles. Mol Microbiol 72:1395–1407PubMedCrossRefGoogle Scholar
  20. Dorward DW, Garon CF (1989) DNA-binding proteins in cells and membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171:4196–4201PubMedGoogle Scholar
  21. Dorward DW, Garon CF, Judd RC (1989) Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae. J Bacteriol 171:2499–2505PubMedGoogle Scholar
  22. Dorward DW, Schwan TG, Garon CF (1991) Immune capture and detection of Borrelia burgdorferi antigens in urine, blood, or tissues from infected ticks, mice, dogs, and humans. J Clin Microbiol 29:1162–1170PubMedGoogle Scholar
  23. Duncan L, Yoshioka M, Chandad F, Grenier D (2004) Loss of lipopolysaccharide receptor CD14 from the surface of human macrophage-like cells mediated by Porphyromonas gingivalis outer membrane vesicles. Microb Pathog 36:319–325PubMedCrossRefGoogle Scholar
  24. Dutta S, Iida K, Takade A, Meno Y, Nair GB, Yoshida S (2004) Release of Shiga toxin by membrane vesicles in Shigella dysenteriae serotype 1 strains and in vitro effects of antimicrobials on toxin production and release. Microbiol Immunol 48:965–969PubMedGoogle Scholar
  25. Ellis TN, Kuehn MJ (2010) Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev 74:81–94PubMedCrossRefGoogle Scholar
  26. Fernandez-Moreira E, Helbig JH, Swanson MS (2006) Membrane vesicles shed by Legionella pneumophila inhibit fusion of phagosomes with lysosomes. Infect Immun 74:3285–3295PubMedCrossRefGoogle Scholar
  27. Ferrari G, Garaguso I, Adu-Bobie J, Doro F, Taddei AR et al (2006) Outer membrane vesicles from group B Neisseria meningitidis delta gna33 mutant: proteomic and immunological comparison with detergent-derived outer membrane vesicles. Proteomics 6:1856–1866PubMedCrossRefGoogle Scholar
  28. Forsberg CW, Beveridge TJ, Hellstrom A (1981) Cellulase and xylanase release from Bacteroides succinogenes and its importance in the rumen environment. Appl Environ Microbiol 42:886–896PubMedGoogle Scholar
  29. Galka F, Wai SN, Kusch H, Engelmann S, Hecker M et al. (2008) Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76:1825–1836PubMedCrossRefGoogle Scholar
  30. Gamazo C, Moriyon I (1987) Release of outer membrane fragments by exponentially growing Brucella melitensis cells. Infect Immun 55:609–615PubMedGoogle Scholar
  31. Goulhen F, Hafezi A, Uitto VJ, Hinode D, Nakamura R, Grenier D, Mayrand D (1998) Subcellular localization and cytotoxic activity of the GroEL-like protein isolated from Actinobacillus actinomycetemcomitans. Infect Immun 66:5307–5313PubMedGoogle Scholar
  32. Grenier D, Mayrand D (1987) Functional characterization of extracellular vesicles produced by Bacteroides gingivalis. Infect Immun 55:111–117PubMedGoogle Scholar
  33. Grenier D (1992) Inactivation of human serum bactericidal activity by a trypsin like protease isolated from Porphyromonas gingivalis. Infect Immun 60:1854–1857PubMedGoogle Scholar
  34. Guo L, Fatig RO 3rd, Orr GL, Schafer BW, Strickland JA et al (1999) Photorhabdus luminescens W-14 insecticidal activity consists of at least two similar but distinct proteins. Purification and characterization of toxin A and toxin B. J Biol Chem 274:9836–9842PubMedCrossRefGoogle Scholar
  35. Henry T, Pommier S, Journet L, Bernadac A, Gorvel JP, Lloubes R (2004) Improved methods for producing outer membrane vesicles in gram-negative bacteria. Res Microbiol 155:437–446PubMedCrossRefGoogle Scholar
  36. Hong GE, Kim DG, Park EM, Nam BH, Kim YO, Kong IS (2009) Identification of Vibrio anguillarum outer membrane vesicles related to immunostimulation in the Japanese flounder, Paralichthys olivaceus. Biosci Biotechnol Biochem 73:437–439PubMedCrossRefGoogle Scholar
  37. Horstman AL, Kuehn MJ (2000) Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J Biol Chem 275:12489–12496PubMedCrossRefGoogle Scholar
  38. Hozbor D, Rodriguez ME, Fernandez J, Lagares A, Guiso N, Yantorno O (1999) Release of outer membrane vesicles from Bordetella pertussis. Curr Microbiol 38:273–278PubMedCrossRefGoogle Scholar
  39. Hynes SO, Keenan JI, Ferris JA, Annuk H, Moran AP (2005) Lewis epitopes on outer membrane vesicles of relevance to Helicobacter pylori pathogenesis. Helicobacter 10:146–156PubMedCrossRefGoogle Scholar
  40. Kadurugamuwa JL, Beveridge TJ (1995) Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177:3998–4008PubMedGoogle Scholar
  41. Kadurugamuwa JL, Beveridge TJ (1998) Delivery of the non-membrane-permeative antibiotic gentamicin into mammalian cells by using Shigella flexneri membrane vesicles. Antimicrob Agents Chemother 42:1476–1483PubMedGoogle Scholar
  42. Kahnt J, Aguiluz K, Koch J, Treuner-Lange A, Konovalova A et al (2010) Profiling the outer membrane proteome during growth and development of the social bacterium Myxococcus xanthus by selective biotinylation and analyses of outer membrane vesicles. J Proteome Res 9:5197–5208PubMedCrossRefGoogle Scholar
  43. Kamaguchi A, Nakayama K, Ichiyama S, Nakamura R, Watanabe T et al. (2003) Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms. Curr Microbiol 47:485–491PubMedCrossRefGoogle Scholar
  44. Karched M, Ihalin R, Eneslatt K, Zhong D, Oscarsson J et al (2008) Vesicle-independent extracellular release of a proinflammatory outer membrane lipoprotein in free-soluble form. BMC Microbiol 8:18PubMedCrossRefGoogle Scholar
  45. Kato S, Kowashi Y, Demuth DR (2002) Outer membrane-like vesicles secreted by Actinobacillus actinomycetemcomitans are enriched in leukotoxin. Microb Pathog 32:1–13PubMedCrossRefGoogle Scholar
  46. Keenan J, Day T, Neal S, Cook B, Perez–Perez G, Allardyce R, Bagshaw P (2000) A role for the bacterial outer membrane in the pathogenesis of Helicobacter pylori infection. FEMS Microbiol Lett 182:259–264PubMedCrossRefGoogle Scholar
  47. Khandelwal P, Banerjee-Bhatnagar N (2003) Insecticidal activity associated with the outer membrane vesicles of Xenorhabdus nematophilus. Appl Environ Microbiol 69:2032–2037PubMedCrossRefGoogle Scholar
  48. Kobayashi H, Uematsu K, Hirayama H, Horikoshi K (2000) Novel toluene elimination system in a toluene-tolerant microorganism. J Bacteriol 182:6451–6455PubMedCrossRefGoogle Scholar
  49. Kolling GL, Matthews KR (1999) Export of virulence genes and Shiga toxin by membrane vesicles of Escherichia coli O157:H7. Appl Environ Microbiol 65:1843–1848PubMedGoogle Scholar
  50. Kouokam JC, Wai SN, Fallman M, Dobrindt U, Hacker J, Uhlin BE (2006) Active cytotoxic necrotizing factor 1 associated with outer membrane vesicles from uropathogenic Escherichia coli. Infect Immun 74:2022–2030PubMedCrossRefGoogle Scholar
  51. Kuehn MJ, Kesty NC (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19:2645–2655PubMedCrossRefGoogle Scholar
  52. Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163–184PubMedCrossRefGoogle Scholar
  53. Kwon SO, Gho YS, Lee JC, Kim SI (2009) Proteome analysis of outer membrane vesicles from a clinical Acinetobacter baumannii isolate. FEMS Microbiol Lett 297:150–156PubMedCrossRefGoogle Scholar
  54. Lee EY, Bang JY, Park GW, Choi DS, Kang JS et al (2007) Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 7:3143–3153PubMedCrossRefGoogle Scholar
  55. Lee EY, Choi DS, Kim KP, Gho YS (2008) Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom Rev 27:535–555PubMedCrossRefGoogle Scholar
  56. Li Z, Clarke AJ, Beveridge TJ (1998) Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J Bacteriol 180:5478–5483PubMedGoogle Scholar
  57. Lindmark B, Rompikuntal PK, Vaitkevicius K, Song T, Mizunoe Y et al (2009) Outer membrane vesicle-mediated release of cytolethal distending toxin (CDT) from Campylobacter jejuni. BMC Microbiol 9:220PubMedCrossRefGoogle Scholar
  58. MacEachran DP, Ye S, Bomberger JM, Hogan DA, Swiatecka-Urban A, Stanton BA, O’Toole GA (2007) The Pseudomonas aeruginosa secreted protein PA2934 decreases apical membrane expression of the cystic fibrosis transmembrane conductance regulator. Infect Immun 75:3902–3912PubMedCrossRefGoogle Scholar
  59. Mashburn-Warren LM, Whiteley M (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846PubMedCrossRefGoogle Scholar
  60. Mashburn LM, Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437:422–425PubMedCrossRefGoogle Scholar
  61. Masignani V, Balducci E, Di Marcello F, Savino S, Serruto D et al (2003) NarE: a novel ADP-ribosyltransferase from Neisseria meningitidis. Mol Microbiol 50:1055–1067PubMedCrossRefGoogle Scholar
  62. McBroom AJ, Kuehn MJ (2005) Outer membrane vesicles In: III RC (ed) EcoSal—Escherichia coli and Salmonella : cellular and molecular biology. American Society for Microbiology Press, WashingtonGoogle Scholar
  63. Molloy MP, Herbert BR, Slade MB, Rabilloud T, Nouwens AS, Williams KL, Gooley AA (2000) Proteomic analysis of the Escherichia coli outer membrane. Eur J Biochem 267:2871–2881PubMedCrossRefGoogle Scholar
  64. Negrete-Abascal E, Garcia RM, Reyes ME, Godinez D, de la Garza M (2000) Membrane vesicles released by Actinobacillus pleuropneumoniae contain proteases and Apx toxins. FEMS Microbiol Lett 191:109–113PubMedCrossRefGoogle Scholar
  65. Nevot M, Deroncele V, Messner P, Guinea J, Mercade E (2006) Characterization of outer membrane vesicles released by the psychrotolerant bacterium Pseudoalteromonas antarctica NF3. Environ Microbiol 8:1523–1533PubMedCrossRefGoogle Scholar
  66. Park GW, Kwon KH, Kim JY, Lee JH, Yun SH et al (2006) Human plasma proteome analysis by reversed sequence database search and molecular weight correlation based on a bacterial proteome analysis. Proteomics 6:1121–1132PubMedCrossRefGoogle Scholar
  67. Patrick S, McKenna JP, O’Hagan S, Dermott E (1996) A comparison of the haemagglutinating and enzymic activities of Bacteroides fragilis whole cells and outer membrane vesicles. Microb Pathog 20:191–202PubMedCrossRefGoogle Scholar
  68. Post DM, Zhang D, Eastvold JS, Teghanemt A, Gibson BW, Weiss JP (2005) Biochemical and functional characterization of membrane blebs purified from Neisseria meningitidis serogroup B. J Biol Chem 280:38383–38394PubMedCrossRefGoogle Scholar
  69. Rosen G, Naor R, Rahamim E, Yishai R, Sela MN (1995) Proteases of Treponema denticola outer sheath and extracellular vesicles. Infect Immun 63:3973–3979PubMedGoogle Scholar
  70. Schlichting E, Lyberg T, Solberg O, Andersen BM (1993) Endotoxin liberation from Neisseria meningitidis correlates to their ability to induce procoagulant and fibrinolytic factors in human monocytes. Scand J Infect Dis 25:585–594PubMedCrossRefGoogle Scholar
  71. Shoberg RJ, Thomas DD (1993) Specific adherence of Borrelia burgdorferi extracellular vesicles to human endothelial cells in culture. Infect Immun 61:3892–3900PubMedGoogle Scholar
  72. Sidhu VK, Vorholter FJ, Niehaus K, Watt SA (2008) Analysis of outer membrane vesicle associated proteins isolated from the plant pathogenic bacterium Xanthomonas campestris pv. campestris. BMC Microbiol 8:87PubMedCrossRefGoogle Scholar
  73. Tan TT, Morgelin M, Forsgren A, Riesbeck K (2007) Hemophilus influenzae survival during complement-mediated attacks is promoted by Moraxella catarrhalis outer membrane vesicles. J Infect Dis 195:1661–1670PubMedCrossRefGoogle Scholar
  74. Vipond C, Suker J, Jones C, Tang C, Feavers IM, Wheeler JX (2006) Proteomic analysis of a meningococcal outer membrane vesicle vaccine prepared from the group B strain NZ98/254. Proteomics 6:3400–3413PubMedCrossRefGoogle Scholar
  75. Wai SN, Lindmark B, Soderblom T, Takade A, Westermark M et al (2003) Vesicle-mediated export and assembly of pore-forming oligomers of the enterobacterial ClyA cytotoxin. Cell 115:25–35PubMedCrossRefGoogle Scholar
  76. Wei C, Yang J, Zhu J, Zhang X, Leng W et al (2006) Comprehensive proteomic analysis of Shigella flexneri 2a membrane proteins. J Proteome Res 5:1860–1865PubMedCrossRefGoogle Scholar
  77. Wu CC, Yates JR 3rd (2003) The application of mass spectrometry to membrane proteomics. Nat Biotechnol 21:262–267PubMedCrossRefGoogle Scholar
  78. Xia XX, Han MJ, Lee SY, Yoo JS (2008) Comparison of the extracellular proteomes of Escherichia coli B and K-12 strains during high cell density cultivation. Proteomics 8:2089–2103PubMedCrossRefGoogle Scholar
  79. Xu C, Lin X, Ren H, Zhang Y, Wang S, Peng X (2006) Analysis of outer membrane proteome of Escherichia coli related to resistance to ampicillin and tetracycline. Proteomics 6:462–473PubMedCrossRefGoogle Scholar
  80. Yaron S, Kolling GL, Simon L, Matthews KR (2000) Vesicle-mediated transfer of virulence genes from Escherichia coli O157:H7 to other enteric bacteria. Appl Environ Microbiol 66:4414–4420PubMedCrossRefGoogle Scholar
  81. Yokoyama K, Horii T, Yamashino T, Hashikawa S, Barua S et al (2000) Production of shiga toxin by Escherichia coli measured with reference to the membrane vesicle-associated toxins. FEMS Microbiol Lett 192:139–144PubMedCrossRefGoogle Scholar
  82. Yoon H, Ansong C, Adkins JN, Heffron F (2011) Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages. Infect Immun 79:2182–2192PubMedCrossRefGoogle Scholar
  83. Zhu W, Thomas CE, Chen CJ, Van Dam CN, Johnston RE, Davis NL, Sparling PF (2005) Comparison of immune responses to gonococcal PorB delivered as outer membrane vesicles, recombinant protein, or Venezuelan equine encephalitis virus replicon particles. Infect Immun 73:7558–7568PubMedCrossRefGoogle Scholar

Copyright information

© The Author(s) 2012

Authors and Affiliations

  1. 1.BiophysicsFormerly of Saha Institute of Nuclear PhysicsKolkataIndia
  2. 2.Molecular and Human Genetics DivisionIndian Institute of Chemical BiologyKolkataIndia

Personalised recommendations