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PMID: 1723487 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Surface layers of bacteria.

Microbiological reviews ·Vol. 55 ·No. 4 ·1991-12-00 ·Pages 684-705

Beveridge TJ, Graham LL

Abstract

Since bacteria are so small, microscopy has traditionally been used to study them as individual cells. To this end, electron microscopy has been a most powerful tool for studying bacterial surfaces; the viewing of macromolecular arrangements of some surfaces is now possible. This review compares older conventional electron-microscopic methods with new cryotechniques currently available and the results each has produced. Emphasis is not placed on the methodology but, rather, on the importance of the results in terms of our perception of the makeup and function of bacterial surfaces and their interaction with the surrounding environment.

MeSH Terms
Bacteria/ultrastructure Cell Membrane/ultrastructure Cell Wall/ultrastructure Cryopreservation Freeze Fracturing Gentian Violet Microscopy, Electron Phenazines Staining and Labeling
Chemicals
Gram's stain Phenazines Gentian Violet
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Beveridge T J
Department of Microbiology, College of Biological Science, University of Guelph, Ontario, Canada.
Graham L L
References (112)
112 references, click to expand
  1. ELECTRON MICROSCOPY AFTER RAPID FREEZING ON A METAL SURFACE AND SUBSTITUTION FIXATION.
    Anat Rec. 1964 Jul;149:381-5 PMID: 14208983
  2. Diagenesis of metals chemically complexed to bacteria: laboratory formation of metal phosphates, sulfides, and organic condensates in artificial sediments.
    Appl Environ Microbiol. 1983 Mar;45(3):1094-108 PMID: 16346230
  3. Metal Interactions with Microbial Biofilms in Acidic and Neutral pH Environments.
    Appl Environ Microbiol. 1989 May;55(5):1249-57 PMID: 16347914
  4. Metal-Binding Characteristics of the Gamma-Glutamyl Capsular Polymer of Bacillus licheniformis ATCC 9945.
    Appl Environ Microbiol. 1990 Dec;56(12):3671-7 PMID: 16348371
  5. Shape and fine structure of nucleoids observed on sections of ultrarapidly frozen and cryosubstituted bacteria.
    J Bacteriol. 1985 Jun;162(3):960-71 PMID: 3922958
  6. Effect of chemical fixatives on accurate preservation of Escherichia coli and Bacillus subtilis structure in cells prepared by freeze-substitution.
    J Bacteriol. 1990 Apr;172(4):2150-9 PMID: 2108132
  7. The tunneling microscope: a new look at the atomic world.
    Science. 1986 Apr 4;232(4746):48-53 PMID: 17773997
  8. The role of electron microscopy in the elucidation of bacterial structure and function.
    Annu Rev Microbiol. 1979;33:459-79 PMID: 227322
  9. Hyphal tip cell ultrastructure of the fungus Fusarium: improved preservation by freeze-substitution.
    J Ultrastruct Res. 1979 Mar;66(3):224-34 PMID: 374749
  10. Polysaccharide capsule of Escherichia coli: microscope study of its size, structure, and sites of synthesis.
    J Bacteriol. 1977 May;130(2):911-36 PMID: 400798
  11. Phototrophic prokaryotes: the cyanobacteria.
    Annu Rev Microbiol. 1977;31:225-74 PMID: 410354
  12. Structure of the surface layer protein of the outer membrane of Spirillum serpens.
    J Ultrastruct Res. 1979 Mar;66(3):235-42 PMID: 439191
  13. Asymmetrical distribution and artifactual reorientation of lipopolysaccharide in the outer membrane bilayer of Salmonella typhimurium.
    Eur J Biochem. 1975 Feb 21;51(2):343-52 PMID: 807474
  14. Uptake and retention of metals by cell walls of Bacillus subtilis.
    J Bacteriol. 1976 Sep;127(3):1502-18 PMID: 821933
  15. Electron microscopy of frozen hydrated biological specimens.
    J Ultrastruct Res. 1976 Jun;55(3):448-56 PMID: 933264
  16. Mechanism of gram variability in select bacteria.
    J Bacteriol. 1990 Mar;172(3):1609-20 PMID: 1689718
  17. Morphological evidence for penetration of anti-O antibody through the capsule of Klebsiella pneumoniae.
    Infect Immun. 1990 May;58(5):1421-8 PMID: 1691148
  18. Characterization of adhesion zones in E. coli cells.
    FEMS Microbiol Lett. 1990 Jan 15;55(1-2):39-43 PMID: 1691728
  19. Antigenic differences among Campylobacter fetus S-layer proteins.
    J Bacteriol. 1990 Sep;172(9):5035-43 PMID: 1697574
  20. Structure of PhoE porin in projection at 3.5 A resolution.
    J Struct Biol. 1990 Mar;103(1):57-63 PMID: 1697759
  21. Ultrastructure, inferred porosity, and gram-staining character of Methanospirillum hungatei filament termini describe a unique cell permeability for this archaeobacterium.
    J Bacteriol. 1991 Jan;173(1):130-40 PMID: 1702777
  22. Periplasmic space and the concept of the periplasm.
    Trends Biochem Sci. 1991 Sep;16(9):328-9 PMID: 1949152
  23. Ultrastructural study of surface components of Streptococcus suis.
    J Bacteriol. 1990 Jun;172(6):2833-8 PMID: 1971617
  24. Direct proof of a "more-than-single-layered" peptidoglycan architecture of Escherichia coli W7: a neutron small-angle scattering study.
    J Bacteriol. 1991 Jan;173(2):751-6 PMID: 1987162
  25. Freeze-substitution of gram-negative eubacteria: general cell morphology and envelope profiles.
    J Bacteriol. 1991 Mar;173(5):1623-33 PMID: 1999383
  26. Evaluation of freeze-substitution and conventional embedding protocols for routine electron microscopic processing of eubacteria.
    J Bacteriol. 1990 Apr;172(4):2141-9 PMID: 2108131
  27. Crystalline order to high resolution in the sheath of Methanospirillum hungatei: a cross-beta structure.
    J Mol Biol. 1985 Jun 5;183(3):509-15 PMID: 3927007
  28. Asymmetric distribution of charge on the cell wall of Bacillus subtilis.
    J Bacteriol. 1985 Sep;163(3):1167-71 PMID: 3928597
  29. The fine structure of Bacillus subtilis revealed by the rapid-freezing and substitution-fixation method.
    J Electron Microsc (Tokyo). 1985;34(1):13-7 PMID: 3932576
  30. Inside-to-outside growth and turnover of the wall of gram-positive rods.
    J Theor Biol. 1985 Nov 7;117(1):137-57 PMID: 3935878
  31. Discontinuity of charge on cell wall poles of Bacillus subtilis.
    Can J Microbiol. 1985 Sep;31(9):875-7 PMID: 3936611
  32. The isolation of surface array proteins from bacteria.
    Can J Biochem Cell Biol. 1984 Nov;62(11):1181-9 PMID: 6525568
  33. Sites of metal deposition in the cell wall of Bacillus subtilis.
    J Bacteriol. 1980 Feb;141(2):876-87 PMID: 6767692
  34. Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall.
    J Bacteriol. 1980 Jul;143(1):471-80 PMID: 6772632
  35. High-resolution topography of the S-layer sheath of the archaebacterium Methanospirillum hungatei provided by scanning tunneling microscopy.
    J Bacteriol. 1990 Nov;172(11):6589-95 PMID: 2121719
  36. Remobilization of toxic heavy metals adsorbed to bacterial wall-clay composites.
    Appl Environ Microbiol. 1990 Oct;56(10):3191-203 PMID: 2126702
  37. Characterization of the surface layer glycoprotein of Clostridium symbiosum HB25.
    J Bacteriol. 1990 May;172(5):2576-83 PMID: 2332405
  38. Surface-active novel glycolipid and linked 3-hydroxy fatty acids produced by Serratia rubidaea.
    J Bacteriol. 1990 Jun;172(6):3015-22 PMID: 2345132
  39. Localization of enterobacterial common antigen immunoreactivity in the ribosomal cytoplasm of Escherichia coli cells cryosubstituted and embedded at low temperature.
    J Bacteriol. 1990 Feb;172(2):1106-13 PMID: 2404937
  40. Gentamicin interaction with Pseudomonas aeruginosa cell envelope.
    Antimicrob Agents Chemother. 1986 Jun;29(6):1079-87 PMID: 2425732
  41. Molecular sieving through S layers of Bacillus stearothermophilus strains.
    J Bacteriol. 1987 Sep;169(9):4092-8 PMID: 2442137
  42. Multilayered distribution of peptidoglycan in the periplasmic space of Escherichia coli.
    J Gen Microbiol. 1989 May;135(5):1243-54 PMID: 2482861
  43. Cell wall mechanical properties as measured with bacterial thread made from Bacillus subtilis.
    J Bacteriol. 1989 Feb;171(2):1055-62 PMID: 2492505
  44. Analysis of a common-antigen lipopolysaccharide from Pseudomonas aeruginosa.
    J Bacteriol. 1989 Apr;171(4):2244-8 PMID: 2495275
  45. Stable expression of lipooligosaccharide antigens during attachment, internalization, and intracellular processing of Neisseria gonorrhoeae in infected epithelial cells.
    Infect Immun. 1989 Nov;57(11):3395-402 PMID: 2509361
  46. Physicochemical interaction of Escherichia coli cell envelopes and Bacillus subtilis cell walls with two clays and ability of the composite to immobilize heavy metals from solution.
    Appl Environ Microbiol. 1989 Nov;55(11):2976-84 PMID: 2516433
  47. Characterization of a dynamic S layer on Bacillus thuringiensis.
    J Bacteriol. 1989 Dec;171(12):6656-67 PMID: 2592346
  48. Ultrastructure and biochemistry of Methanococcus voltae.
    Crit Rev Microbiol. 1989;17(1):53-87 PMID: 2669831
  49. The structure of crystalline bacterial surface layers.
    Prog Biophys Mol Biol. 1988;51(2):131-63 PMID: 3076242
  50. Ultrastructure of the cell envelope of the archaebacteria Thermoproteus tenax and Thermoproteus neutrophilus.
    J Bacteriol. 1986 Jun;166(3):1046-54 PMID: 3086286
  51. Physicochemical roles of soluble metal cations in the outer membrane of Escherichia coli K-12.
    Can J Microbiol. 1986 Jul;32(7):594-601 PMID: 3091229
  52. The functions of autolysins in the growth and division of Bacillus subtilis.
    Crit Rev Microbiol. 1987;15(2):169-222 PMID: 3123142
  53. Amikacin disrupts the cell envelope of Pseudomonas aeruginosa ATCC 9027.
    Can J Microbiol. 1988 Jan;34(1):12-8 PMID: 3132316
  54. The superficial protein arrays on bacteria.
    Microbiol Sci. 1986 Dec;3(12):357-61 PMID: 3153568
  55. Crystalline surface layers in procaryotes.
    J Bacteriol. 1988 Jul;170(7):2891-7 PMID: 3290191
  56. The efficiency of immunolabel on Lowicryl sections compared to theoretical predictions.
    J Histochem Cytochem. 1987 Sep;35(9):959-69 PMID: 3302020
  57. Three-dimensional structure of the frozen-hydrated flagellar filament. The left-handed filament of Salmonella typhimurium.
    J Mol Biol. 1987 Jun 5;195(3):581-601 PMID: 3309339
  58. Surface properties from the S-layer of Clostridium thermosaccharolyticum D120-70 and Clostridium thermohydrosulfuricum L111-69.
    Arch Microbiol. 1988;149(6):527-33 PMID: 3389971
  59. Structural and biochemical analyses of a surface array protein of Campylobacter fetus.
    J Bacteriol. 1988 Sep;170(9):4165-73 PMID: 3410826
  60. Site specificity of metallic ion binding in Escherichia coli K-12 lipopolysaccharide.
    Can J Microbiol. 1986 Jan;32(1):52-5 PMID: 3516350
  61. Electron probe analysis, X-ray mapping, and electron energy-loss spectroscopy of calcium, magnesium, and monovalent ions in log-phase and in dividing Escherichia coli B cells.
    J Bacteriol. 1986 Sep;167(3):935-9 PMID: 3528130
  62. Immunocytochemical localization of enterobacterial common antigen in Escherichia coli and Yersinia enterocolitica cells.
    J Bacteriol. 1986 Oct;168(1):348-56 PMID: 3531175
  63. Structure of the Staphylococcus aureus cell wall determined by the freeze-substitution method.
    J Bacteriol. 1987 Jun;169(6):2482-7 PMID: 3584061
  64. Charge distribution on the S layer of Bacillus stearothermophilus NRS 1536/3c and importance of charged groups for morphogenesis and function.
    J Bacteriol. 1987 Jun;169(6):2804-9 PMID: 3584071
  65. Nephelometric determination of turgor pressure in growing gram-negative bacteria.
    J Bacteriol. 1987 Aug;169(8):3654-63 PMID: 3611024
  66. Difference Fourier analysis of "surface features" of bacteriorhodopsin using glucose-embedded and frozen-hydrated purple membrane.
    Ultramicroscopy. 1987;23(1):17-28 PMID: 3660490
  67. Manganese oxidation by Leptothrix discophora.
    J Bacteriol. 1987 Feb;169(2):489-94 PMID: 3804969
  68. Characterization of extracellular Mn2+-oxidizing activity and isolation of an Mn2+-oxidizing protein from Leptothrix discophora SS-1.
    J Bacteriol. 1987 Mar;169(3):1279-85 PMID: 3818545
  69. Electron microscopy of frozen-hydrated biological material.
    Nature. 1986 Feb 20-26;319(6055):631-6 PMID: 3951536
  70. Two patterns in the Aeromonas salmonicida A-layer may reflect a structural transformation that alters permeability.
    J Bacteriol. 1986 Apr;166(1):120-7 PMID: 3957865
  71. Unusual stability of the Methanospirillum hungatei sheath.
    J Bacteriol. 1985 May;162(2):728-37 PMID: 3988711
  72. A simple freeze-substitution method for electron microscopy.
    J Ultrastruct Res. 1966 Aug;15(5):469-79 PMID: 5330121
  73. Alterations in outer membrane permeability.
    Annu Rev Microbiol. 1984;38:237-64 PMID: 6093683
  74. Ultrastructure, chemistry, and function of the bacterial wall.
    Int Rev Cytol. 1981;72:229-317 PMID: 6166584
  75. Electron microscopy: its development and application to microbiology.
    Can J Microbiol. 1982 Jan;28(1):1-53 PMID: 6175387
  76. Chemical mechanism of the Gram stain and synthesis of a new electron-opaque marker for electron microscopy which replaces the iodine mordant of the stain.
    J Bacteriol. 1983 Nov;156(2):837-45 PMID: 6195147
  77. Cellular responses of Bacillus subtilis and Escherichia coli to the Gram stain.
    J Bacteriol. 1983 Nov;156(2):846-58 PMID: 6195148
  78. Projected structure of unstained, frozen-hydrated T-layer of Bacillus brevis.
    EMBO J. 1984 Jan;3(1):101-5 PMID: 6200319
  79. Periplasmic gel: new concept resulting from the reinvestigation of bacterial cell envelope ultrastructure by new methods.
    J Bacteriol. 1984 Oct;160(1):143-52 PMID: 6207168
  80. Cryo-electron microscopy of viruses.
    Nature. 1984 Mar 1-7;308(5954):32-6 PMID: 6322001
  81. Structure of the envelope of Escherichia coli observed by the rapid-freezing and substitution fixation method.
    Microbiol Immunol. 1983;27(1):95-9 PMID: 6346024
  82. Beggiatoa, Thiothrix, and Thioploca.
    Annu Rev Microbiol. 1983;37:341-67 PMID: 6357055
  83. The surface stress theory of microbial morphogenesis.
    Adv Microb Physiol. 1983;24:301-66 PMID: 6364728
  84. Biology of iron- and manganese-depositing bacteria.
    Annu Rev Microbiol. 1984;38:515-50 PMID: 6388499
  85. Electron microscopy of frozen-hydrated bacteria.
    J Bacteriol. 1983 Jul;155(1):381-90 PMID: 6408064
  86. Crystalline surface layers on bacteria.
    Annu Rev Microbiol. 1983;37:311-39 PMID: 6416145
  87. Metal binding by the peptidoglycan sacculus of Escherichia coli K-12.
    Can J Microbiol. 1984 Feb;30(2):204-11 PMID: 6424920
  88. Evidence for the presence of a capsule in Vibrio vulnificus.
    J Gen Microbiol. 1984 Oct;130(10):2741-3 PMID: 6512503
  89. Role of cellular design in bacterial metal accumulation and mineralization.
    Annu Rev Microbiol. 1989;43:147-71 PMID: 2679352
  90. Influence of fixatives and embedding media on immunolabelling of freeze-substituted cells.
    Scanning Microsc Suppl. 1989;3:57-63; discussion 63-4 PMID: 2694274
  91. Putative role of a 70 kDa outer-surface protein in promoting cell-surface hydrophobicity of Serratia marcescens RZ.
    J Gen Microbiol. 1989 Aug;135(8):2277-81 PMID: 2699331
  92. Improved preservation of bacterial capsule for electron microscopy.
    J Electron Microsc Tech. 1989 Feb;11(2):167-9 PMID: 2709135
  93. Immunoglobulin binding by the regular surface array of Aeromonas salmonicida.
    J Biol Chem. 1988 Jul 5;263(19):9298-303 PMID: 2967820
  94. Increased cell surface hydrophobicity of a Serratia marcescens NS 38 mutant lacking wetting activity.
    J Bacteriol. 1988 Sep;170(9):4361-4 PMID: 3045093
  95. Fine structures of the capsules of Klebsiella pneumoniae and Escherichia coli K1.
    J Bacteriol. 1988 Oct;170(10):4960-2 PMID: 3049556
  96. The bacterial surface: general considerations towards design and function.
    Can J Microbiol. 1988 Apr;34(4):363-72 PMID: 3052749
  97. Growth and form in microorganisms: morphogenesis of Escherichia coli.
    Can J Microbiol. 1988 Apr;34(4):381-9 PMID: 3052750
  98. Bacterial extracellular polysaccharides.
    Can J Microbiol. 1988 Apr;34(4):415-20 PMID: 3052752
  99. Computer image processing of electron micrographs of biological structures with helical symmetry.
    J Electron Microsc Tech. 1988 Aug;9(4):325-58 PMID: 3058895
  100. Low temperature embedding with Lowicryl resins: two new formulations and some applications.
    J Microsc. 1985 Oct;140(Pt 1):55-63 PMID: 3912508
  101. Distribution of calcium and other elements in cryosectioned Bacillus cereus T spores, determined by high-resolution scanning electron probe x-ray microanalysis.
    J Bacteriol. 1980 Jul;143(1):481-91 PMID: 6772633
  102. Intracellular structures of Mycoplasma pneumoniae revealed after membrane removal.
    J Bacteriol. 1980 Oct;144(1):390-9 PMID: 6774963
  103. Asymmetric localization of lipopolysaccharides on the outer membrane of Salmonella typhimurium.
    J Bacteriol. 1980 Mar;141(3):1463-5 PMID: 6988417
  104. The bacterial glycocalyx in nature and disease.
    Annu Rev Microbiol. 1981;35:299-324 PMID: 7027902
  105. Specimen preparation for electron microscopy using low temperature embedding resins.
    J Microsc. 1982 Apr;126(Pt 1):77-85 PMID: 7040669
  106. Reconstruction of imperfectly ordered zinc-induced tubulin sheets using cross-correlation and real space averaging.
    Ultramicroscopy. 1981;6(1):7-17 PMID: 7233611
  107. Scanning electron probe x-ray microanalysis of elemental distributions in freeze-dried cryosections of Bacillus coagulans spores.
    J Bacteriol. 1981 Aug;147(2):670-4 PMID: 7263617
  108. Loss of virulence during culture of Aeromonas salmonicida at high temperature.
    J Bacteriol. 1981 Oct;148(1):333-40 PMID: 7287625
  109. Electron microscopy of ultra-thin sections of bacteria I. Cellular division in Bacillus cereus.
    J Bacteriol. 1953 Sep;66(3):362-73 PMID: 13096487
  110. Methods and principles of fixation by freeze-substitution.
    J Biophys Biochem Cytol. 1958 Sep 25;4(5):593-600 PMID: 13587555
  111. The net hydration of T-4 bacteriophage deoxyribonuecleic acid and the effect of hydration on buoyant behavior in a density gradient at equilibrium in the ultracentrifuge.
    Proc Natl Acad Sci U S A. 1961 Jul 15;47:1005-14 PMID: 13712606
  112. The relationship between the nature of the cell wall and the Gram stain.
    J Gen Microbiol. 1963 Feb;30:223-35 PMID: 13991188
Article Info
Journal
Microbiological reviews
Abbr.
Microbiol Rev
ISSN
0146-0749
Published
1991-12-00
Pages
684-705
Language
English
Region
United States
NLM ID
7806086
PMCID
PMC372843
Subset
IM
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