Microbial Surfaces Investigated Using Atomic Force Microscopy

Methods in Microbiology

Volumn 34, Issue , 2004, Pages 163-197

  Dufrêne, Yves F ^a   Müller, Daniel J ^b  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 34548230431     PISSN: 05809517     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0580-9517(04)34006-7     Document Type: Review

References (120)

1. N.I. Abu-Lail T.A. Camesano Elasticity of Pseudomonas putida KT2442 surface polymers probed with single-molecule force microscopy Langmuir 18 2002 4071 4081
2. N.I. Abu-Lail T.A. Camesano Polysaccharide properties probed with atomic force microscopy J. Microsc.-Oxf 212 2003 217 238
3. F. Ahimou F.A. Denis A. Touhami Y.F. Dufrêne Probing microbial cell surface charges by atomic force microscopy Langmuir 18 2002 9937 9941
4. F. Ahimou A. Touhami Y.F. Dufrêne Real-time imaging of the surface topography of living yeast cells by atomic force microscopy Yeast 20 2003 25 30
5. U. Alexiev T. Marti M.P. Heyn H.G. Khorana P. Scherrer Surface charge of bacteriorhodopsin detected with covalently bound pH indicators at selected extracellular and cytoplasmic sites Biochemistry 33 1994 298 306
6. M. Amrein D.J. Müller Sample preparation techniques in scanning probe microscopy Nanobiology 4 1999 229 256
7. T. Ando N. Kodera E. Takai D. Maruyama K. Saito A. Toda A high-speed atomic force microscope for studying biological macromolecules Proc. Natl Acad. Sci. USA 98 2001 12468 12472
8. W. Baumeister M. Barth R. Hegerl R. Guckenberger M. Hahn W.O. Saxton Three-dimensional structure of the regular surface layer (HPI layer) of Deinococcus radiodurans J. Mol. Biol 187 1986 241 253
9. W. Baumeister I. Wildhaber H. Engelhardt Bacterial surface proteins: some structural, functional and evolutionary aspects Biophys. Chem 29 1988 39 49
10. I.B. Beech The potential use of atomic force microscopy for studying corrosion of metals in the presence of bacterial biofilms – an overview Int. Biodet. Biodeg 37 1996 141 149
11. M. Benoit D. Gabriel G. Gerisch H.E. Gaub Discrete interactions in cell adhesion measured by single-molecule force spectroscopy Nat. Cell. Biol 2 2000 313 317
12. T.J. Beveridge Structures of gram-negative cell walls and their derived membrane vesicles J. Bacteriol 181 1999 4725 4733
13. T.J. Beveridge L.L. Graham Surface layers of bacteria Microbiol. Rev 55 1991 684 705
14. G. Binnig C.F. Quate C. Gerber Atomic force microscope Phys. Rev. Lett 56 1986 930 933
15. W.R. Bowen R.W. Lovitt C.J. Wright Atomic force microscopy study of the adhesion of Saccharomyces cerevisiae J. Coll. Interf. Sci 237 2001 54 61
16. H.-J. Butt Electrostatic interaction in atomic force microscopy Biophys. J 60 1991 777 785
17. H.-J. Butt M. Jaschke W. Ducker Measuring surface forces in aqueous electrolyte solution with the atomic force microscope Bioelectrochem. Bioenerg 38 1995 191 201
18. H. Clausen-Schaumann M. Seitz R. Krautbauer H.E. Gaub Force spectroscopy with single bio-molecules Curr. Opin. Chem. Biol 4 2000 524 530
19. S.A. Crawford M.J. Higgins P. Mulvaney R. Wetherbee Nanostructure of the diatom frustule as revealed by atomic force and scanning electron microscopy J. Phycol 37 2001 543 554
20. D. Czajkowsky M. Allen V. Elings Z. Shao Direct visualization of surface charge in aqueous solution Ultramicroscopy 74 1998 1 5
21. D.M. Czajkowsky S. Sheng Z. Shao Staphylococcal alpha-hemolysin can form hexamers in phospholipid bilayers J. Mol. Biol 276 1998 325 330
22. D.M. Czajkowsky H. Iwamoto T.L. Cover Z. Shao The vacuolating toxin from Helicobacter pylori forms hexameric pores in lipid bilayers at low pH Proc. Natl Acad. Sci. USA 96 1999 2001 2006
23. P.B. Dengis P.G. Rouxhet Surface properties of top- and bottom-fermenting yeast Yeast 13 1997 931 943
24. M.J. Doktycz C.J. Sullivan P.R. Hoyt D.A. Pelletier S. Wu D.P. Allison AFM imaging of bacteria in liquid media immobilized on gelatin coated mica surfaces Ultramicroscopy 97 2003 209 216
25. R.J. Doyle M. Rosenberg Microbial Cell Surface Hydrophobicity 1990 American Society for Microbiology Washington, DC
26. B. Drake C.B. Prater A.L. Weisenhorn S.A.C. Gould T.R. Albrecht C.F. Quate D.S. Cannell H.G. Hansma P.K. Hansma Imaging crystals, polymers, and processes in water with the atomic force microscope Science 243 1989 1586 1588
27. Y.F. Dufrêne Direct characterization of the physicochemical properties of fungal spores using functionalized AFM probes Biophys. J 78 2000 3286 3291
28. Y.F. Dufrêne Atomic force microscopy, a powerful tool in microbiology J. Bacteriol 184 2002 5205 5213
29. Y.F. Dufrêne Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology Curr. Opin. Microbiol 6 2003 317 323
30. Y.F. Dufrêne C.J.P. Boonaert P.A. Gerin M. Asther P.G. Rouxhet Direct probing of the surface ultrastructure and molecular interactions of dormant and germinating spores of Phanerochaete chrysosporium J. Bacteriol 181 1999 5350 5354
31. A. Engel D.J. Müller Observing single biomolecules at work with the atomic force microscope Nat. Struct. Biol 7 2000 715 718
32. D. Fotiadis D.J. Müller G. Tsiotis L. Hasler P. Tittmann T. Mini P. Jenö H. Gross A. Engel Surface analysis of the photosystem I complex by electron and atomic force microscopy J. Mol. Biol 283 1998 83 94
33. D. Fotiadis L. Hasler D.J. Müller H. Stahlberg J. Kistler A. Engel Surface tongue-and-groove contours on lens MIP facilitate cell-to-cell adherence J. Mol. Biol 300 2000 779 789
34. 2+-binding domain at the C terminus of AQP1 J. Mol. Biol 318 2002 1381 1394
35. D. Fotiadis Y. Liang S. Filipek D.A. Saperstein A. Engel K. Palczewski Atomic-force microscopy: rhodopsin dimers in native disc membranes Nature 421 2003 127 128
36. D. Fotiadis P. Qian A. Philippsen P.A. Bullough A. Engel C.N. Hunter Structural analysis of the reaction center light-harvesting complex I photosynthetic core complex of Rhodospirillum rubrum using atomic force microscopy J. Biol. Chem 279 2004 2063 2068
37. M. Gad A. Ikai Method for immobilizing microbial cells on gel surface for dynamic AFM studies Biophys. J 69 1995 2226 2233
38. E.S. Gyorvary O. Stein D. Pum U.B. Sleytr Self-assembly and recrystallization of bacterial S-layer proteins at silicon supports imaged in real time by atomic force microscopy J. Microsc 212 2003 300 306
39. H.G. Hansma Surface biology of DNA by atomic force microscopy Annu. Rev. Phys. Chem 52 2001 71 92
40. W.F. Heinz J.H. Hoh Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope Tibtech 17 1999 143 150
41. W.F. Heinz J.H. Hoh Relative surface charge density mapping with the atomic force microscope Biophys. J 76 1999 528 538
42. M.J. Higgins S.A. Crawford P. Mulvaney R. Wetherbee The topography of soft, adhesive diatom “trails” as observed by atomic force microscopy Biofouling 16 2000 133 139
43. P. Hinterdorfer Molecular recognition studies using the atomic force microscope Meth. Cell Biol 68 2002 115 139
44. A.D.L. Humphris M.J. Miles Developments in dynamic force microscopy and spectroscopy Meth. Cell Biol 68 2002 337 355
45. A.D.L. Humphris J.K. Hobbs M.J. Miles Ultrahigh-speed scanning near-field optical microscopy capable of over 100 frames per second Appl. Phys. Lett 83 2003 6 8
46. J. Israelachvili Intermolecular & Surface Forces 2nd edn. 1991 Academic Press London
47. H. Janovjak M. Kessler H. Gaub D. Oesterhelt D.J. Müller Unfolding pathways of native bacteriorhodopsin depend on temperature EMBO J 22 2003 5220 5229
48. A. Janshoff M. Neitzert Y. Oberdörfer H. Fuchs Force spectroscopy of molecular systems-single molecule spectroscopy of polymers and biomolecules Angew. Chem. Int. Ed 39 2000 3213 3237
49. S. Karrasch R. Hegerl J. Hoh W. Baumeister A. Engel Atomic force microscopy produces faithful high-resolution images of protein surfaces in an aqueous environment Proc. Natl Acad. Sci. USA 91 1994 836 838
50. S. Kasas A. Ikai A method for anchoring round shaped cells for atomic force microscope imaging Biophys. J 68 1995 1678 1680
51. P.E. Klebba S.M. Newton Mechanisms of solute transport through outer membrane porins: burning down the house Curr. Opin. Microbiol 1 1998 238 247
52. Y. Koch K.H. Rademacher Chemical and enzymatic changes in the cell walls of Candida albicans and Saccharomyces cerevisiae by scanning electron microscopy Can. J. Microbiol 26 1980 965 970
53. W. Kühlbrandt Two-dimensional crystallization of membrane proteins Q. Rev. Biophys 25 1992 1 49
54. Y.G. Kuznetsov A.J. Malkin A. McPherson Atomic force microscopy studies of living cells: visualization of motility, division, aggregation, transformation, and apoptosis J. Struct. Biol 120 1997 180 191
55. S.K. Lower M.F. Hochella T.J. Beveridge Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and α-FeOOH Science 292 2001 1360 1363
56. A.J. Malkin M. Plomp A. McPherson Application of atomic force microscopy to studies of surface processes in virus crystallization and structural biology Acta Crystallogr. Sect. D – Biol. Crystallogr 58 2002 1617 1621
57. A.J. Malkin A. McPherson P.D. Gershon Structure of intracellular mature vaccinia virus visualized by in situ atomic force microscopy J. Virol 77 2003 6332 6340
58. P.E. Marszalek A.F. Oberhauser Y.P. Pang J.M. Fernandez Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring Nature 396 1998 661 664
59. P.A. Maurice M.A. Vierkorn L.E. Hersman J.E. Fulghum A. Ferryman Enhancement of kaolinite dissolution by an aerobic Pseudomonas mendocina bacterium Geomicrobiol. J 18 2001 21 35
60. D. Moll C. Huber B. Schlegel D. Pum U.B. Sleytr M. Sara S-layer-streptavidin fusion proteins as template for nanopatterned molecular arrays Proc. Natl Acad. Sci. USA 99 2002 14646 14651
61. C. Möller M. Allen V. Elings A. Engel D.J. Müller Tapping mode atomic force microscopy produces faithful high-resolution images of protein surfaces Biophys. J 77 1999 1050 1058
62. C. Möller G. Büldt N. Dencher A. Engel D.J. Müller Reversible loss of crystallinity on photobleaching purple membrane in presence of hydroxylamine J. Mol. Biol 301 2000 869 879
63. J.X. Mou J. Yang Z.F. Shao Atomic force microscopy of cholera toxin B-oligomers bound to bilayers of biologically relevant lipids J. Mol. Biol 248 1995 507 512
64. N. Mozes P.S. Handley H.J. Busscher P.G. Rouxhet Microbial Cell Surface Analysis: Structural and Physicochemical Methods 1991 VCH Publishers New York
65. D.J. Müller A. Engel The height of biomolecules measured with the atomic force microscope depends on electrostatic interactions Biophys. J 73 1997 1633 1644
66. D.J. Müller A. Engel Voltage and pH-induced channel closure of porin OmpF visualized by atomic force microscopy J. Mol. Biol 285 1999 1347 1351
67. D.J. Müller G. Büldt A. Engel Force-induced conformational change of bacteriorhodopsin J. Mol. Biol 249 1995 239 243
68. D.J. Müller W. Baumeister A. Engel Conformational change of the hexagonally packed intermediate layer of Deinococcus radiodurans imaged by atomic force microscopy J. Bacteriol 178 1996 3025 3030
69. D.J. Müller M. Amrein A. Engel Adsorption of biological molecules to a solid support for scanning probe microscopy J. Struct. Biol 119 1997 172 188
70. D.J. Müller D. Fotiadis A. Engel Mapping flexible protein domains at subnanometer resolution with the AFM FEBS Lett 430 1998 105 111
71. D.J. Müller W. Baumeister A. Engel Controlled unzipping of a bacterial surface layer with atomic force microscopy Proc. Natl Acad. Sci. USA 96 1999 13170 13174
72. D.J. Müller D. Fotiadis S. Scheuring S.A. Müller A. Engel Electrostatically balanced subnanometer imaging of biological specimens by atomic force microscopy Biophys. J 76 1999 1101 1111
73. D.J. Müller G.M. Hand A. Engel G. Sosinsky Conformational changes in surface structures of isolated Connexin26 gap junctions EMBO J 21 2002 3598 3607
74. D.J. Müller M. Kessler F. Oesterhelt C. Moeller D. Oesterhelt H. Gaub Stability of bacteriorhodopsin alpha-helices and loops analyzed by single-molecule force spectroscopy Biophys. J 83 2002 3578 3588
75. 2 imaged with atomic force microscopy Pflugers Arch 439 2000 251 255
76. D. Oesterhelt W. Stoeckenius Isolation of the cell membrane of Halobacterium halobium and its fraction into red and purple Membrane Meth. Enzymol 31 1974 667 678
77. F. Oesterhelt D. Oesterhelt M. Pfeiffer A. Engel H.E. Gaub D.J. Müller Unfolding pathways of individual bacteriorhodopsins Science 288 2000 143 146
78. R.S. Pembrey K.C. Marshall R.P. Schneider Cell surface analysis techniques: what do cell preparation protocols do to cell surface properties? Appl. Environ. Microbiol 65 1999 2877 2894
79. N. Persike M. Pfeiffer R. Guckenberger M. Radmacher M. Fritz Direct observation of different surface structures on high-resolution images of native halorhodopsin J. Mol. Biol 310 2001 773 780
80. J. Peters M. Peters F. Lottspeich W. Schäfer W. Baumeister Nucleotide sequence of the gene encoding the Deinococcus radiodurans surface protein, derived amino acid sequence, and complementary protein chemical studies J. Bacteriol 169 1987 5216 5223
81. K. Pethe M. Aumercier E. Fort C. Gatot C. Locht F.D. Menozzi Characterization of the heparin-binding site of the mycobacterial heparin-binding hemagglutinin adhesin J. Biol. Chem 275 2000 14273 14280
82. A. Philippsen W. Im A. Engel T. Schirmer B. Roux D.J. Müller Imaging the electrostatic potential of transmembrane channels: atomic probe microscopy on OmpF porin Biophys. J 82 2002 1667 1676
83. C.A.J. Putman K. van der Werft B.G. de Grooth N.F. van Hulst J. Greve P.K. Hansma A new imaging mode in the atomic force microscope based on the error signal SPIE 1639 1992 198 204
84. M. Radmacher Measuring the elastic properties of living cells by the atomic force microscope Meth. Cell Biol 68 2002 67 90
85. M. Rief F. Oesterhelt B. Heymann H.E. Gaub Single molecule force spectroscopy on polysaccharides by atomic force microscopy Science 275 1997 1295 1297
86. C. Rotsch K. Jacobson M. Radmacher Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy Proc. Natl Acad. Sci. USA 96 1999 921 926
87. P. Schaer-Zammaretti J. Ubbink Imaging of lactic acid bacteria with AFM-elasticity and adhesion maps and their relationship to biological and structural data Ultramicroscopy 97 2003 199 208
88. T.E. Schäffer J.P. Cleveland F. Ohnesorge D.A. Walters P.K. Hansma Studies of vibrating atomic force microscope cantilevers in liquid J. Appl. Phys 80 1996 3622 3627
89. S. Scheuring P. Ringler M. Borgina H. Stahlberg D.J. Müller P. Agre A. Engel High resolution topographs of the Escherichia coli waterchannel aquaporin Z EMBO J 18 1999 4981 4987
90. S. Scheuring F. Reiss-Husson A. Engel J.L. Rigaud J.L. Ranck High-resolution AFM topographs of Rubrivivax gelatinosus light-harvesting complex LH2 EMBO J 20 2001 3029 3035
91. S. Scheuring D.J. Müller H. Stahlberg H.A. Engel A. Engel Sampling the conformational space of membrane protein surfaces with the AFM Eur. Biophys. J 31 2002 172 178
92. S. Scheuring H. Stahlberg M. Chami C. Houssin J.L. Rigaud A. Engel Charting and unzipping the surface layer of Corynebacterium glutamicum with the atomic force microscope Mol. Microbiol 44 2002 675 684
93. S. Scheuring J. Seguin S. Marco D. Levy C. Breyton B. Robert J.L. Rigaud AFM characterization of tilt and intrinsic flexibility of Rhodobacter sphaeroides light harvesting complex 2 (LH2) J. Mol. Biol 325 2003 569 580
94. H. Schindler J.P. Rosenbusch Matrix protein from Escherichia coli outer membranes forms voltage-controlled channels in lipid bilayers Proc. Natl Acad. Sci. USA 75 1978 3751 3755
95. T. Schirmer General and specific porins from bacterial outer membranes J. Struct. Biol 121 1998 101 109
96. U.D. Schwarz H. Haefke P. Reimann H.J. Guntherodt Tip artefacts in scanning force microscopy J. Microsc 173 1994 183 197
97. H. Seelert A. Poetsch N.A. Dencher A. Engel H. Stahlberg D.J. Müller Proton powered turbine of a plant motor Nature 405 2000 418 419
98. N. Sharon H. Lis Lectins as cell recognition molecules Science 246 1989 227 234
99. L.S. Shlyakhtenko A.A. Gall A. Filonov Z. Cerovac A. Lushnikov Y.L. Lyubchenko Silatrane-based surface chemistry for immobilization of DNA, protein-DNA complexes and other biological materials Ultramicroscopy 97 2003 279 287
100. U.B. Sleytr Basic and applied S-layer research: an overview FEMS Microbiol. Rev 20 1997 5 12
101. U.B. Sleytr T.J. Beveridge Bacterial S-layers Trends Microbiol 7 1999 253 260
102. U.B. Sleytr M. Sára Ultrafiltration membranes with uniform pores from crystalline bacterial cell envelope layers Appl. Microbiol. Biotechnol 25 1986 83 90
103. U.B. Sleytr H. Bayley M. Sara A. Breitwieser S. Kupcu C. Mader S. Weigert F.M. Unger P. Messner B. Jahn-Schmid B. Schuster D. Pum K. Douglas N.A. Clark J.T. Moore T.A. Winningham S. Levy I. Frithsen J. Pankovc P. Beale H.P. Gillis D.A. Choutov K.P. Martin Applications of S-layers FEMS Microbiol. Rev 20 1997 151 175
104. B.F. Sloat J.R. Pringle A mutant of yeast defective in cellular morphogenesis Science 200 1978 1171 1173
105. H. Stahlberg D. Fotiadis S. Scheuring H. Remigy T. Braun K. Mitsuoka Y. Fujiyoshi A. Engel Two-dimensional crystals: a powerful approach to assess structure, function and dynamics of membrane proteins FEBS Lett 504 2001 166 172
106. H. Stahlberg D.J. Müller K. Suda D. Fotiadis A. Engel U. Matthey T. Meier P. Dimroth Bacterial ATP synthase has an undecameric rotor EMBO Rep 21 2001 1 5
107. D. Stoffler K.N. Goldie B. Feja U. Aebi Calcium-mediated structural changes of native nuclear pore complexes monitored by time-lapse atomic force microscopy J. Mol. Biol 287 1999 741 752
108. A. Touhami B. Nysten Y.F. Dufrêne Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy Langmuir 19 2003 4539 4543
109. A. Touhami B. Hoffmann A. Vasella F.A. Denis Y.F. Dufrêne Aggregation of yeast cells: direct measurement of discrete lectin-carbohydrate interactions Microbiol. SGM 149 2003 2873 2878
110. B.C. van der Aa Y.F. Dufrêne In situ characterization of bacterial extracellular polymeric substances by AFM Colloids Surf. B: Biointerf 23 2002 173 182
111. B.C. van der Aa R.M. Michel M. Asther M.T. Zamora P.G. Rouxhet Y.F. Dufrêne Stretching cell surface macromolecules by atomic force microscopy Langmuir 17 2001 3116 3119
112. B.C. van der Aa M. Asther Y.F. Dufrêne Surface properties of Aspergillus oryzae spores investigated by atomic force microscopy Colloids Surf. B: Biointerf 24 2002 277 284
113. M.B. Viani L.I. Pietrasanta J.B. Thompson A. Chand I.C. Gebeshuber J.H. Kindt M. Richter H.G. Hansma P.K. Hansma Probing protein–protein interactions in real time Nat. Struct. Biol 7 2000 644 647
114. P. Wagner Immobilization strategies for biological scanning probe microscopy FEBS Lett 430 1998 112 115
115. H. Wang D.E. Clapham Conformational changes of the in situ nuclear pore complex Biophys. J 77 1999 241 247
116. W. Xu P.J. Mulhern B.L. Blackford M.H. Jericho M. Firtel T.J. Beveridge Modeling and measuring the elastic properties of an archaeal surface, the sheath of Methanospirillum hungatei , and the implication for methane production J. Bacteriol 178 1996 3106 3112
117. J. Yang J.X. Mou Z.F. Shao Structure and stability of pertussis toxin studied by in situ atomic force microscopy FEBS Lett 338 1994 89 92
118. X. Yao M. Jericho D. Pink T. Beveridge Thickness and elasticity of Gram-negative murein sacculi measured by atomic force microscopy J. Bacteriol 181 1999 6865 6875
119. X. Yao J. Walter S. Burke S. Stewart M.H. Jericho D. Pink R. Hunter T.J. Beveridge Atomic force microscopy and theoretical considerations of surface properties and turgor pressures of bacteria Colloids Surf. B: Biointerf 23 2002 213 230
120. J. Zlatanova S.M. Lindsay S.H. Leuba Single molecule force spectroscopy in biology using the atomic force microscope Prog. Biophys. Mol. Biol 74 2000 37 61