Contour and persistence length of Corynebacterium diphtheria pili by atomic force microscopy

European Biophysics Journal

Volumn 41, Issue 6, 2012, Pages 561-570

  Rheinlaender, Johannes ^a   Gräbner, Anna ^a   Ott, Lisa ^a   Burkovski, Andreas ^a   Schäffer, Tilman E ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

AFM; Bacteria; Contour length; Persistence length; Stiffness

Indexed keywords

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIUM ADHERENCE; BIOLOGICAL MODEL; COMPUTER SIMULATION; CORYNEBACTERIUM DIPHTHERIAE; ELASTICITY; FIMBRIA; METHODOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

BACTERIAL ADHESION; COMPUTER SIMULATION; CORYNEBACTERIUM DIPHTHERIAE; ELASTICITY; FIMBRIAE, BACTERIAL; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL;

BACTERIA (MICROORGANISMS); CORYNEBACTERIUM DIPHTHERIAE;

EID: 84863608396     PISSN: 01757571     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00249-012-0818-4     Document Type: Article

References (48)

1. Abels JA, Moreno-Herrero F, van der Heijden T, Dekker C, Dekker NH (2005) Single-molecule measurements of the persistence length of double-stranded RNA. Biophys J 88(4):2737-2744. doi:10.1529/biophysj.104.052811 (Pubitemid 40976140)
2. Anselmetti D, Hansmeier N, Kalinowski J, Martini J, Merkle T, Palmisano R, Ros R, Schmied K, Sischka A, Toensing K (2007) Analysis of subcellular surface structure, function and dynamics. Anal Bioanal Chem 387(1):83-89. doi:10.1007/s00216-006-0789-3 (Pubitemid 44956254)
3. Arce FT, Carlson R, Monds J, Veeh R, Hu FZ, Stewart PS, Lal R, Ehrlich GD, Avci R (2009) Nanoscale structural and mechanical properties of nontypeable Haemophilus influenzae biofilms. J Bacteriol 191(8):2512-2520. doi:10.1128/jb.01596-08
4. Baumann CG, Smith SB, Bloomfield VA, Bustamante C (1997) Ionic effects on the elasticity of single DNA molecules. Proc Natl Acad Sci USA 94(12):6185-6190 (Pubitemid 27270659)
5. Bednar J, Furrer P, Katritch V, Stasiak A, Dubochet J, Stasiak A (1995) Determination of DNA persistence length by cryoelectron microscopy. Separation of the static and dynamic contributions to the apparent persistence length of DNA. J Mol Biol 254(4):579-594. doi:10.1006/jmbi.1995.0640 (Pubitemid 26001793)
6. Bertuccini L, Baldassarri L, von Hunolstein C (2004) Internalization of non-toxigenic Corynebacterium diphtheriae by cultured human respiratory epithelial cells. Microb Pathog 37(3):111-118. doi:10.1016/j.micpath.2004.06.002 (Pubitemid 39213981)
7. Bezanilla M, Manne S, Laney DE, Lyubchenko YL, Hansma HG (1995) Adsorption of DNA to mica, silylated mica, and minerals: characterization by atomic force microscopy. Langmuir 11(2):655-659. doi:10.1021/la00002a050
8. Colombo AV, Hirata R Jr, de Souza CM, Monteiro-Leal LH, Previato JO, Formiga LC, Andrade AF, Mattos-Guaraldi AL (2001) Corynebacterium diphtheriae surface proteins as adhesins to human erythrocytes. FEMS Microbiol Lett 197(2):235-239. doi: 10.1111/j.1574-6968.2001.tb10609.x (Pubitemid 32324187)
9. Dorst L, Smeulders AWM (1987) Length estimators for digitized contours. Comput Vis Graph Image Process 40(3):311-333
10. Dupres V, Alsteens D, Pauwels K, Dufrêne YF (2009) In vivo imaging of S-layer nanoarrays on Corynebacterium glutamicum. Langmuir 25(17):9653-9655. doi:10.1021/la902238q
11. Fälker S, Nelson AL, Morfeldt E, Jonas K, Hultenby K, Ries J, Melefors Ö., Normark S, Henriques-Normark B (2008) Sortasemediated assembly and surface topology of adhesive pneumococcal pili.Mol Microbiol 70(3):595-607. doi:10.1111/j.1365-2958.2008.06396.x
12. Gaspar AH, Ton-That H (2006) Assembly of distinct pilus structures on the surface of Corynebacterium diphtheriae. J Bacteriol 188(4):1526-1533. doi:10.1128/jb.188.4.1526-1533.2006 (Pubitemid 43228686)
13. Gittes F, Mickey B, Nettleton J, Howard J (1993) Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol 120(4):923-934. doi:10.1083/jcb.120.4.923 (Pubitemid 23056298)
14. Guttilla IK, Gaspar AH, Swierczynski A, Swaminathan A, Dwivedi P, Das A, Ton-That H (2009) Acyl enzyme intermediates in sortase-catalyzed pilus morphogenesis in gram-positive bacteria. J Bacteriol 191(18):5603-5612. doi:10.1128/jb.00627-09
15. Hirata R Jr, Souza SMS, Rocha de Souza CM, Andrade AF, Monteiro-Leal LH, Formiga LCD, Mattos-Guaraldi AL (2004) Patterns of adherence to HEp-2 cells and actin polymerisation by toxigenic Corynebacterium diphtheriae strains. Microb Pathog 36(3):125-130. doi:10.1016/j.micpath.2003.10.002 (Pubitemid 38064321)
16. Hirata R Jr, Napoleao F, Monteiro-Leal LH, Andrade AFB, Nagao PE, Formiga LCD, Fonseca LS, Mattos-Guaraldi AL (2002) Intracellular viability of toxigenic Corynebacterium diphtheria strains in Hep-2 cells. FEMS Microbiol Lett 215(1):115-119. doi:10.1111/j.1574-6968.2002.tb11379.x (Pubitemid 35232592)
17. Hogan M, LeGrange J, Austin B (1983) Dependence of DNA helix flexibility on base composition. Nature 304(5928):752-754. doi: 10.1038/304752a0 (Pubitemid 13037728)
18. Huxley HE, Stewart A, Sosa H, Irving T (1994) X-ray diffraction measurements of the extensibility of actin and myosin filaments in contractingmuscle. Biophys J 67(6):2411-2421. doi:10.1016/s0006-3495(94)80728-3 (Pubitemid 24369665)
19. Jiao Y, Schäffer TE (2004) Accurate height and volume measurements on soft samples with the atomic force microscope. Langmuir 20(23):10038-10045. doi:10.1021/la048650u
20. Kang HJ, Paterson NG, Gaspar AH, Ton-That H, Baker EN (2009) The Corynebacterium diphtheriae shaft pilin SpaA is built of tandem Ig-like modules with stabilizing isopeptide and disulfide bonds. Proc Natl Acad Sci USA 106(40):16967-16971. doi: 10.1073/pnas.0906826106
21. Koch AL (1966) The logarithm in biology 1. Mechanisms generating the log-normal distribution exactly. J Theoret Biol 12(2):276-290. doi:10.1016/0022-5193(66)90119-6
22. Kojima H, Ishijima A, Yanagida T (1994) Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc Natl Acad Sci USA 91(26):12962-12966
23. Landau LD, Lifshits EM, Pitaevskiǐ LP (1980) Statistical physics. Course of theoretical physics, 3rd edn. Butterworth-Heinemann, Oxford
24. Landau LD, Lifshitz EM, Kosevich AM, Pitaevskiǐ LP (1986) Theory of elasticity. Course of theoretical physics, 3rd edn. Butterworth-Heinemann, Oxford
25. Leung KM, Wanger G, Guo Q, Gorby Y, Southam G, Lau WM, Yang J (2011) Bacterial nanowires: conductive as silicon, soft as polymer. Soft Matter 7(14):6617-6621. doi:10.1039/c1sm05611e
26. Limpert E, Stahel WA (2011) Problems with using the normal distribution-and ways to improve quality and efficiency of data analysis. PLoS ONE 6(7):e21403. doi:10.1371/journal.pone.0021403
27. Limpert E, Stahel WA, Abbt M (2001) Log-normal distributions across the sciences: keys and clues. Bioscience 51(5):341-352. doi:10.1641/0006-3568(2001) 051[0341:LNDATS]2.0.CO;2 (Pubitemid 32550418)
28. Mandlik A, Swierczynski A, Das A, Ton-That H (2007) Corynebacterium diphtheriae employs specific minor pilins to target human pharyngeal epithelial cells. Mol Microbiol 64(1):111-124. doi: 10.1111/j.1365-2958.2007.05630.x (Pubitemid 46435028)
29. Mandlik A, Das A, Ton-That H (2008) The molecular switch that activates the cell wall anchoring step of pilus assembly in grampositive bacteria. Proc Natl Acad Sci USA 105(37):14147-14152. doi:10.1073/pnas.0806350105
30. Mantelli S, Muller P, Harlepp S, Maaloum M (2011) Conformational analysis and estimation of the persistence length of DNA using atomic force microscopy in solution. Soft Matter 7(7):3412-3416. doi:10.1039/c0sm01160f
31. Miller E, Garcia T, Hultgren S, Oberhauser AF (2006) The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophys J 91(10):3848-3856. doi: 10.1529/biophysj.106.088989 (Pubitemid 44788327)
32. Nagashima H, Asakura S (1980) Dark-field light microscopic study of the flexibility of F-actin complexes. J Mol Biol 136(2):169-182 (Pubitemid 10136650)
33. Ott L, Höller M, Rheinlaender J, Schäffer TE, Hensel M, Burkovski A (2010) Strain-specific differences in pili formation and the interaction of Corynebacterium diphtheriae with host cells. BMC Microbiol 10:257. doi:10.1186/1471-2180-10-257
34. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435(7045):1098-1101. doi:10.1038/nature03661 (Pubitemid 40910516)
35. Rivetti C, Codeluppi S (2000) Accurate length determination of DNA molecules visualized by atomic force microscopy: evidence for a partial B- to A-form transition on mica. Ultramicroscopy 87(1-2):55-66. doi:10.1016/s0304- 3991(00)00064-4 (Pubitemid 32220175)
36. Rivetti C, Guthold M, Bustamante C (1996) Scanning force microscopy of DNA deposited onto mica: Equilibration versus kinetic trapping studied by statistical polymer chain analysis. J Mol Biol 264(5):919-932. doi:10.1006/jmbi.1996.0687 (Pubitemid 27019483)
37. Rogers EA, Das A, Ton-That H (2011) Adhesion by pathogenic corynebacteria. In: Linke D, Goldman A (eds) Bacterial adhesion, vol 715. Advances in experimental medicine and biology. Springer, the Netherlands, pp 91-103. doi:10.1007/978-94-007-0940-9-6
38. Silverman PM, Clarke MB (2010) New insights into F-pilus structure, dynamics, and function. Integr Biol 2(1):25-31. doi:10.1039/b917761b
39. Skerker JM, Berg HC (2001) Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci USA 98(12): 6901-6904. doi:10.1073/pnas. 121171698 (Pubitemid 32538314)
40. Swierczynski A, Ton-That H (2006) Type III pilus of corynebacteria: pilus length is determined by the level of its major pilin subunit. J Bacteriol 188(17):6318-6325. doi:10.1128/jb.00606-06 (Pubitemid 44448574)
41. Taylor WH, Hagerman PJ (1990) Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure: II. NaCl-dependence of DNA flexibility and helical repeat. J Mol Biol 212(2):363-376. doi:10.1016/0022-2836(90)90131-5 (Pubitemid 20130734)
42. Touhami A, Jericho MH, Boyd JM, Beveridge TJ (2006) Nanoscale characterization and determination of adhesion forces of Pseudomonas aeruginosa pili by using atomic force microscopy. J Bacteriol 188(2):370-377. doi:10.1128/jb.188.2.370-377.2006 (Pubitemid 43100524)
43. Trachtenberg S, Hammel I (1992) The rigidity of bacterial flagellar filaments and its relation to filament polymorphism. J Struct Biol 109(1):18-27. doi:10.1016/1047-8477(92)90063-g (Pubitemid 23080839)
44. Wang MD, Yin H, Landick R, Gelles J, Block SM (1997) Stretching DNA with optical tweezers. Biophys J 72(3):1335-1346. doi: 10.1016/s0006-3495(97)78780-0 (Pubitemid 27113656)
45. Wang YA, Yu X, Overman S, Tsuboi M, Thomas GJ Jr, Egelman EH (2006) The structure of a filamentous bacteriophage. J Mol Biol 361(2):209-215. doi:10.1016/j.jmb.2006.06.027 (Pubitemid 44092782)
46. Wright CJ, Shah MK, Powell LC, Armstrong I (2010) Application of AFM from microbial cell to biofilm. Scanning 32(3):134-149. doi:10.1002/sca.20193
47. Yanagawa R, Honda E (1976) Presence of pili in species of human and animal parasites and pathogens of the genus corynebacterium. Infect Immun 13(4):1293-1295
48. Yanagida T, Nakase M, Nishiyama K, Oosawa F (1984) Direct observation of motion of single F-actin filaments in the presence of myosin. Nature 307(5946):58-60. doi:10.1038/307058a0 (Pubitemid 14132930)