Abstract
Optical tweezers (OT) are a technique that, by focused laser light, can both manipulate micrometer sized objects and measure minute forces (in the pN range) in biological systems. The technique is therefore suitable for assessment of bacterial adhesion on an individual adhesin-receptor and single attachment organelle (pili) level. This chapter summarizes the use of OT for assessment of adhesion mechanisms of both non-piliated and piliated bacteria. The latter include the important helix-like pili expressed by uropathogenic Escherichia coli (UPEC), which have shown to have unique and intricate biomechanical properties. It is conjectured that the large flexibility of this type of pili allows for a redistribution of an external shear force among several pili, thereby extending the adhesion lifetime of bacteria. Systems with helix-like adhesion organelles may therefore act as dynamic biomechanical machineries, enhancing the ability of bacteria to withstand high shear forces originating from rinsing flows such as in the urinary tract. This implies that pili constitute an important virulence factor and a possible target for future anti-microbial drugs.
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References
An YH, Friedman RJ (2000) Handbook of bacterial adhesion principles, methods, and applications. Humana Press, Totowa, NJ
Andersson M, Axner O, Almqvist F, Uhlin BE, Fällman E (2008) Physical properties of biopolymers assessed by optical tweezers: analysis of folding and refolding of bacterial pili. ChemPhysChem 9:221–235
Andersson M, Fällman E, Uhlin BE, Axner O (2006) A sticky chain model of the elongation and unfolding of Escherichia coli P pili under stress. Biophys J 90:1521–1534
Andersson M, Uhlin BE, Fällman E (2007) The biomechanical properties of Escherichia coli pili for urinary tract attachment reflect the host environment. Biophys J 93:3008–3014
Ashkin A, Dziedzic JM (1987) Optical trapping and manipulation of viruses and bacteria. Science 235:1517–1520
Axner O, Björnham O, Castelain M, Koutris E, Schedin S, Fällman E, Andersson M (2009) Unraveling the secrets of bacterial adhesion organelles using single-molecule force spectroscopy. In: Rigler R (ed) Nobel symposium, vol 138, chapter 18. Springer, Berlin, pp 337–362
Båga M, Norgren M, Normark S (1987) Biogenesis of Escherichia coli Pap pili – PapH, a minor pilin subunit involved in cell anchoring and length modulation. Cell 49:241–251
Balsalobre C, Morschhauser J, Jass J, Hacker J, Uhlin BE (2003) Transcriptional analysis of the sfa determinant revealing multiple mRNA processing events in the biogenesis of S fimbriae in pathogenic Escherichia coli. J Bacteriol 185:620–629
Barocchi MA, Ries J, Zogaj X, Hemsley C, Albiger B, Kanth A, Dahlberg S, Fernebro J, Moschioni M, Masignani V, Hultenby K, Taddei AR, Beiter K, Wartha F, von Euler A, Covacci A, Holden DW, Normark S, Rappuoli R, Henriques-Normark B (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA 103:2857–2862
Bell MG (1978) Models for the specific adhesion of cells to cells. Science 200:618–627
Björnham O, Axner O (2009) Multipili attachment of bacteria with helixlike pili exposed to stress. J Chem Phys 130:18
Björnham O, Axner O (2010) Catch-bond behavior of bacteria binding by slip bonds. Biophys J 99:1331–1341
Björnham O, Axner O, Andersson M (2008) Modeling of the elongation and retraction of Escherichia coli P pili under strain by Monte Carlo simulations. Eur Biophys J 37:381–391
Björnham O, Bugaytsova J, Borén T, Schedin S (2009a) Dynamic force spectroscopy of the Helicobacter pylori BabA-Lewis b binding. Biophys Chem 143:102–105
Björnham O, Fällman E, Axner O, Ohlsson J, Nilsson U, Borén T, Schedin S (2005) Measurements of the binding force between the Helicobacter pylori adhesin BabA and the Lewis b blood group antigen using optical tweezers. J Biomed Opt 10:044024
Björnham O, Nilsson H, Andersson M, Schedin S (2009b) Physical properties of the specific PapG–galabiose binding in E. coli P pili-mediated adhesion. Eur Biophys J 38:245–254
Björnham O, Schedin S (2009) Methods and estimations of uncertainties in single-molecule dynamic force spectroscopy. Eur Biophys J 38:911–922
Bullitt E, Makowski L (1995) Structural polymorphism of bacterial adhesion pili. Nature 373:164–167
Bustamante C, Marko JF, Siggia ED, Smith S (1994) Entropic elasticity of lambda-phage DNA. Science 265:1599–1600
Capitanio M, Romano G, Ballerini R, Giuntini M, Pavone FS, Dunlap D, Finzi L (2002) Calibration of optical tweezers with differential interference contrast signals. Rev Sci Instrum 73:1687–1696
Castelain M, Ehlers S, Klinth J, Lindberg S, Andersson M, Uhlin BE, Axner O (2011) Fast uncoiling kinetics of F1C pili expressed by uropathogenic Escherichia coli are revealed on a single pilus level using force-measuring optical tweezers. Eur Biophys J 40(3):305–316
Castelain M, Koutris E, Andersson M, Wiklund K, Björnham O, Schedin S, Axner O (2009a) Characterization of the biomechanical properties of T4 pili expressed by Streptococcus pneumoniae – a comparison between helix-like and open coil-like pili. ChemPhysChem 10:1533–1540
Castelain M, Sjöstrom AE, Fällman E, Uhlin BE, Andersson M (2009b) Unfolding and refolding properties of S pili on extraintestinal pathogenic Escherichia coli. Eur Biophys J 39:1105–1115
de Breij A, Gaddy J, van der Meer J, Koning R, Koster A, van den Broek P, Actis L, Nibbering P, Dijkshoorn L (2009) CsuA/BABCDE-dependent pili are not involved in the adherence of Acinetobacter baumannii ATCC19606T to human airway epithelial cells and their inflammatory response. Res Microbiol 160:213–218
Ericsson M, Hanstorp D, Hagberg P, Enger J, Nyström T (2000) Sorting out bacterial viability with optical tweezers. J Bacteriol 182:5551–5555
Evans E (2001) Probing the relation between force – lifetime – and chemistry in single molecular bonds. Annu Rev Biophys Biomol Struct 30:105–128
Grover SC, Skirtach AG, Gauthier RC, Grover CP (2001) Automated single-cell sorting system based on optical trapping. J Biomed Opt 6:14–22
Hahn E, Wild P, Hermanns U, Sebbel P, Glockshuber R, Haner M, Taschner N, Burkhard P, Aebi U, Müller SA (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 pili. J Mol Biol 323:845–857
Haruff HM, Munakata-Marr J, Marr DWM (2003) Directed bacterial surface attachment via optical trapping. Colloids Surf B27:189–195
Hilleringmann M, Ringler P, Muller SA, De Angelis G, Rappuoli R, Ferlenghi I, Engel A (2009) Molecular architecture of Streptococcus pneumoniae TIGR4 pili. EMBO J 28:3921–3930
Horner F, Woerdemann M, Muller S, Maier B, Denz C (2010) Full 3D translational and rotational optical control of multiple rod-shaped bacteria. J Biophotonics 3:468–475
Jacob-Dubuisson F, Heuser J, Dodson K, Normark S, Hultgren S (1993) Initiation of assembly and association of the structural elements of a bacterial pilus depend on 2 specialized tip proteins. EMBO J 12:837–847
Jass J, Schedin S, Fällman E, Ohlsson J, Nilsson UJ, Uhlin BE, Axner O (2004) Physical properties of Escherichia coli P pili measured by optical tweezers. Biophys J 87:4271–4283
Jones CH, Pinkner JS, Roth R, Heuser J, Nicholes AV, Abraham SN, Hultgren SJ (1995) FimH adhesin of type-1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc Natl Acad Sci USA 92:2081–2085
Källenius G, Svenson SB, Hultberg H, Möllby R, Helin I, Cedergren B, Winberg J (1981) Occurrence of P-fimbriated Escherichia coli in urinary tract infections. Lancet 2:1369–1372
Knight SD, Choudhury D, Hultgren S, Pinkner J, Stojanoff V, Thompson A (2002) Structure of the S pilus periplasmic chaperone SfaE at 2.2 Ångstrom resolution. Acta Crystallogr D Biol Crystallogr 58:1016–1022
Le Trong I, Aprikian P, Kidd BA, Forero-Shelton M, Tchesnokova V, Rajagopal P, Rodriguez V, Interlandi G, Klevit R, Vogel V, Stenkamp RE, Sokurenko EV, Thomas WE (2010) Structural basis for mechanical force regulation of the adhesin FimH via finger trap-like beta sheet twisting. Cell 141:645–655
Liang MN, Smith SP, Metallo SJ, Choi IS, Prentiss M, Whitesides GM (2000) Measuring the forces involved in polyvalent adhesion of uropathogenic Escherichia coli to mannose-presenting surfaces. Proc Natl Acad Sci USA 97:13092–13096
Maier B (2005) Using laser tweezers to measure twitching motility in Neisseria. Curr Opin Microbiol 8:344–349
Neuman KC, Block SM (2004) Optical trapping. Rev Sci Instrum 75:2787–2809
Proft T, Baker EN (2009) Pili in Gram-negative and Gram-positive bacteria – structure, assembly and their role in disease. Cell Mol Life Sci 66:613–635
Rad R, Gerhard M, Lang R, Schoniger M, Rosch T, Schepp W, Becker I, Wagner H, Prinz C (2002) The Helicobacter pylori blood group antigen-binding adhesin facilitates bacterial colonization and augments a nonspecific immune response. J Immunol 168:3033–3041
Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9:117–128
Sauer FG, Barnhart M, Choudhury D, Knights SD, Waksman G, Hultgren SJ (2000) Chaperone-assisted pilus assembly and bacterial attachment. Curr Opin Struct Biol 10:548–556
Sauer FG, Remaut H, Hultgren SJ, Waksman G (2004) Fiber assembly by the chaperone-usher pathway. Biochim Biophys Acta-Mol Cell Res 1694:259–267
Simpson KH, Bowden MG, Hook M, Anvari B (2002) Measurement of adhesive forces between S-epidermidis and fibronectin-coated surfaces using optical tweezers. Lasers Surg Med 31:45–52
Simpson KH, Bowden G, Hook M, Anvari B (2003) Measurement of adhesive forces between individual Staphylococcus aureus MSCRAMMs and protein-coated surfaces by use of optical tweezers. J Bacteriol 185:2031–2035
Simpson KH, Bowden MG, Peacock SJ, Arya M, Höök M, Anvari B (2004) Adherence of Staphylococcus aureus fibronectin binding protein A mutants: an investigation using optical tweezers. Biomol Eng 21:105–111
Sherlock O, Schembri MA, Reisner A, Klemm P (2004) Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation. J Bacteriol 186:8058–8065
Thomas WE, Nilsson LM, Forero M, Sokurenko EV, Vogel V (2004) Shear-dependent “stick-and-roll” adhesion of type 1 fimbriated Escherichia coli. Mol Microbiol 53:1545–1557
Wang S, Arellano-Santoyo H, Combs PA, Shaevitz JW (2010) Measuring the bending stiffness of bacterial cells using an optical trap. J Vis Exp 38. doi:10.3791/2012
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Axner, O. et al. (2011). Assessing Bacterial Adhesion on an Individual Adhesin and Single Pili Level Using Optical Tweezers. In: Linke, D., Goldman, A. (eds) Bacterial Adhesion. Advances in Experimental Medicine and Biology, vol 715. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0940-9_19
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DOI: https://doi.org/10.1007/978-94-007-0940-9_19
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