journal article·2021

On the strong connection between nanoscale adhesion of Yad fimbriae and macroscale attachment of Yad-decorated bacteria to glycosylated, hydrophobic and hydrophilic surfaces

Grégory Francius, Florian Petit, Eloïse Clément, Yankel Chekli, Jean-Marc Ghigo, Christophe Beloin, Jérôme F. L. Duval

Nanoscale· Volume 13· Issue 2
Publisher page

Abstract

Yad fimbriae are currently viewed as versatile bacterial adhesins able to significantly mediate host or plant-pathogen recognition and contribute to the persistence of Escherichia coli in both the environment and within hosts. To date, however, the underlying adhesion process of Yad fimbriae on surfaces defined by controlled coating chemistries has not been evaluated on the relevant molecular scale. In this work, the interaction forces operational between Yad fimbriae expressed by genetically modified E. coli and self-assembled monolayers (SAM) differing in terms of charge, hydrophobicity or the nature of decorating sugar units are quantified by Single Molecule Force Spectroscopy (SMFS) on the nanoscale. It is found that the adhesion of Yad fimbriae onto probes functionalized with xylose is as strong as that measured with probes decorated with anti-Yad antibodies (ca. 80 to 300 pN). In contrast, the interactions of Yad with galactose, lactose, mannose, -OH, -NH2, -COOH and -CH3 terminated SAMs are clearly non-specific. Interpretation of SMFS measurements on the basis of worm-like-chain modeling for polypeptide nanomechanics further leads to the estimates of the maximal extension of Yad fimbriae upon stretching, of their persistence length and of their polydispersity. Finally, we show for the first time a strong correlation between the adhesion properties of Yad-decorated bacteria determined from conventional macroscopic counting methods and the molecular adhesion capacity of Yad fimbriae. This demonstration advocates the effort that should be made to understand on the nanoscale level the interactions between fimbriae and their cognate ligands. The results could further help the design of potential anti-adhesive molecules or surfaces to better fight against the virulence of bacterial pathogens.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Micro and Nano Robotics · Proteins in Food Systems · Force Microscopy Techniques and Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Université de Lorraine

LCPME

UMR 7564

Villers-lès-Nancy

France

Genetics of Biofilms Laboratory

Institut Pasteur

UMR CNRS2001

Paris

LIEC

UMR 7360

Vandœuvre-lès-Nancy

Funding

Ministère de l'Education Nationale, de l'Enseignement Supérieur et de la Recherche · Fondation pour la Recherche Médicale · Agence Nationale de la Recherche

References (76)

Show source-provided references
1. Costa · Lett. Appl. Microbiol. · 2019 · 68 · 26910.1111/lam.13127 ↗
2. Galié · Front. Microbiol. · 2018 · 9 · 89810.3389/fmicb.2018.00898 ↗
3. Lebeaux · Microbiol. Mol. Biol. Rev. · 2014 · 78 · 51010.1128/MMBR.00013-14 ↗
4. Luis Del Pozo · Expert Rev. Anti-Infect. Ther. · 2018 · 16 · 5110.1080/14787210.2018.1417036 ↗
5. A. Alvarez-Ordonez , L. M.Coughlan , R.Briandet and P. D.Cotter , in Annual Review of Food Science and Technology, Vol 10 , ed. M. P. Doyle and D. J. McClements , 2019 , vol. 10 , pp. 173–195
6. Leff · PLoS One · 2013 · 8 · e5931010.1371/journal.pone.0059310 ↗
7. Luna-Guevara · Int. J. Microbiol. · 2019 · 2019 · 289432810.1155/2019/2894328 ↗
8. Berger · Environ. Microbiol. · 2010 · 12 · 238510.1111/j.1462-2920.2010.02297.x ↗
9. Ávila-Quezada · N. Z. J. Crop Hortic. Sci. · 2010 · 38 · 4710.1080/01140671003767834 ↗
10. Kampmeier · Curr. Top. Microbiol. Immunol. · 2018 · 416 · 117
11. J. P. Cramer , in Emerging Infectious Diseases , ed. Ö. Ergönül , F. Can , L. Madoff and M. Akova , Academic Press , Amsterdam , 2014 , pp. 213–227 . 10.1016/B978-0-12-416975-3.00017-010.1016/B978-0-12-416975-3.00017-0 ↗
12. Köckerling · Front. Public Health · 2017 · 5 · 33210.3389/fpubh.2017.00332 ↗
13. Caprioli · Microbiol. Spectrum · 2014 · 2 · 110.1128/microbiolspec.EHEC-0014-2013 ↗
14. Kaper · Microbiol. Spectrum · 2014 · 2 · 110.1128/microbiolspec.EHEC-0028-2014 ↗
15. Boll · mBio · 2017 · 8 · e00717-1710.1128/mBio.00717-17 ↗
16. Rendon · Proc. Natl. Acad. Sci. U. S. A. · 2007 · 104 · 1063710.1073/pnas.0704104104 ↗
17. Lang · Emerging Microbes Infect. · 2018 · 7 · 110.1038/s41426-018-0209-8 ↗
18. Knutton · Pediatr. Res. · 1990 · 27 · 53010.1203/00006450-199005000-00031 ↗
19. Moreira · FEMS Microbiol. Lett. · 2003 · 226 · 7910.1016/S0378-1097(03)00561-5 ↗
20. P. Luthje and A.Brauner , in Advances in Microbial Physiology, Vol 65: Advances in Bacterial Pathogen Biology , ed. R. K. Poole , 2014 , vol. 65 , pp. 337–372
21. Klemm · Environ. Microbiol. Rep. · 2010 · 2 · 62810.1111/j.1758-2229.2010.00166.x ↗
22. Ageorges · FEMS Microbiol. Rev. · 2020 · 44 · 31410.1093/femsre/fuaa008 ↗
23. Monserrat-Martinez · Int. J. Mol. Sci. · 2019 · 20 · 125510.3390/ijms20061255 ↗
24. Psonis · EcoSal Plus · 2019 · 8 · 110.1128/ecosalplus.ESP-0033-2018 ↗
25. Geibel · Biochim. Biophys. Acta, Mol. Cell Res. · 2014 · 1843 · 155910.1016/j.bbamcr.2013.09.023 ↗
26. Korea · BioEssays · 2011 · 33 · 30010.1002/bies.201000121 ↗
27. Wurpel · PLoS One · 2013 · 8 · e5283510.1371/journal.pone.0052835 ↗
28. Dziva · Infect. Immun. · 2013 · 81 · 83810.1128/IAI.00585-12 ↗
29. Verma · Infect. Immun. · 2016 · 84 · 18710.1128/IAI.01138-15 ↗
30. Larsonneur · Environ. Microbiol. · 2016 · 18 · 522810.1111/1462-2920.13559 ↗
31. Gross · Phytochemistry · 1984 · 23 · 245710.1016/S0031-9422(00)84075-3 ↗
32. Sandhu · Mol. Plant · 2009 · 2 · 84010.1093/mp/ssp056 ↗
33. E. M. S. M. Gaspar , I. S.Nunes and J. F.Lopes , Xylose: Production, Consumption and Health Benefits , 2012 , pp. 43–67
34. Carson · Commun. Dis. Intell. Q. Rep. · 2003 · 27 Suppl · S143
35. Ofek · FEMS Immunol. Med. Microbiol. · 2003 · 38 · 18110.1016/S0928-8244(03)00228-1 ↗
36. Asadi · Infection · 2019 · 47 · 1310.1007/s15010-018-1222-5 ↗
37. Cusumano · Sci. Transl. Med. · 2011 · 3 · 109ra11510.1126/scitranslmed.3003021 ↗
38. Ohlsson · ChemBioChem · 2002 · 3 · 77210.1002/1439-7633(20020802)3:8<772::AID-CBIC772>3.0.CO;2-8 ↗
39. Duvernoy · Nat. Commun. · 2018 · 9 · 110.1038/s41467-018-03446-y ↗
40. Cherepanov · Gene · 1995 · 158 · 910.1016/0378-1119(95)00193-A ↗
41. Korea · Environ. Microbiol. · 2010 · 12 · 195710.1111/j.1462-2920.2010.02202.x ↗
42. Wildling · Bioconjugate Chem. · 2011 · 22 · 123910.1021/bc200099t ↗
43. A. Ebner , L.Wildling , R.Zhu , C.Rankl , T.Haselgrubler , P.Hinterdorfer and H. J.Gruber , in Stm and Afm Studies On , Springer-Verlag Berlin , Berlin , 2008 , vol. 285 , pp. 29–76
44. Ebner · Bioconjugate Chem. · 2007 · 18 · 117610.1021/bc070030s ↗
45. Jacquot · J. Biomed. Nanotechnol. · 2014 · 10 · 336110.1166/jbn.2014.1905 ↗
46. Ebner · Ultramicroscopy · 2007 · 107 · 92210.1016/j.ultramic.2007.02.035 ↗
47. Schillers · J. Mol. Recognit. · 2016 · 29 · 9510.1002/jmr.2510 ↗
48. Xu · Nanotechnol. Rev. · 2018 · 7 · 60510.1515/ntrev-2018-0086 ↗
49. Polyakov · PLoS One · 2011 · 6 · e1888710.1371/journal.pone.0018887 ↗
50. Janshoff · Angew. Chem., Int. Ed. · 2000 · 39 · 321210.1002/1521-3773(20000915)39:18<3212::AID-ANIE3212>3.0.CO;2-X ↗
51. Ortiz · Macromolecules · 1999 · 32 · 78010.1021/ma981245n ↗
52. Wiercigroch · Spectrochim. Acta, Part A · 2017 · 185 · 31710.1016/j.saa.2017.05.045 ↗
53. Wells · J. Mol. Struct. · 1990 · 224 · 38510.1016/0022-2860(90)87031-R ↗
54. Zimmermann · Curr. Opin. Colloid Interface Sci. · 2019 · 44 · 17710.1016/j.cocis.2019.10.004 ↗
55. Song · Langmuir · 2007 · 23 · 543010.1021/la063168s ↗
56. Duval · Curr. Opin. Colloid Interface Sci. · 2010 · 15 · 18410.1016/j.cocis.2009.12.002 ↗
57. Gaboriaud · Langmuir · 2008 · 24 · 1098810.1021/la800258n ↗
58. Castelain · Eur. Biophys. J. · 2011 · 40 · 30510.1007/s00249-010-0648-1 ↗
59. Chen · J. Bacteriol. · 2011 · 193 · 171810.1128/JB.01395-10 ↗
60. Andersson · J. Mol. Biol. · 2012 · 415 · 91810.1016/j.jmb.2011.12.006 ↗
61. Forero · PLoS Biol. · 2006 · 4 · e29810.1371/journal.pbio.0040298 ↗
62. Pratt · Mol. Microbiol. · 1998 · 30 · 28510.1046/j.1365-2958.1998.01061.x ↗
63. Silverman · Integr. Biol. · 2010 · 2 · 2510.1039/B917761B ↗
64. de Haan · Biophys. J. · 2016 · 111 · 226310.1016/j.bpj.2016.09.050 ↗
65. Rheinlaender · Eur. Biophys. J. · 2012 · 41 · 56110.1007/s00249-012-0818-4 ↗
66. Castelain · PLoS One · 2016 · 11 · e015205310.1371/journal.pone.0152053 ↗
67. Pönisch · New J. Phys. · 2017 · 19 · 01500310.1088/1367-2630/aa5483 ↗
68. Pletikapic · J. Mol. Recognit. · 2012 · 25 · 30910.1002/jmr.2177 ↗
69. Alam · ACS Biomater. Sci. Eng. · 2019 · 5 · 209310.1021/acsbiomaterials.9b00213 ↗
70. Bos · FEMS Microbiol. Rev. · 1999 · 23 · 17910.1016/S0168-6445(99)00004-2 ↗
71. Pan · Mater. Horiz. · 2020 · 7 · 9310.1039/C9MH01191A ↗
72. Oh · Sci. Rep. · 2018 · 8 · 1724710.1038/s41598-018-35343-1 ↗
73. Eskhan · Colloid Polym. Sci. · 2014 · 292 · 34310.1007/s00396-013-3017-7 ↗
74. Busscher · Appl. Environ. Microbiol. · 2008 · 74 · 255910.1128/AEM.02839-07 ↗
75. Jacquot · Nanoscale · 2014 · 6 · 1266510.1039/C4NR03312D ↗
76. Yachdav · Nucleic Acids Res. · 2014 · 42 · W33710.1093/nar/gku366 ↗