Single-cell and single-molecule analysis deciphers the localization, adhesion, and mechanics of the biofilm adhesin LapA

ACS Chemical Biology

Volumn 9, Issue 2, 2014, Pages 485-494

  El Kirat Chatel, Sofiane ^a   Beaussart, Audrey ^a   Boyd, Chelsea D ^b   O'Toole, George A ^b   Dufreîne, Yves F ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; LAPA PROTEIN; LAPG PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIUM ADHERENCE; BIOFILM; CELL ADHESION; CELL DENSITY; CELL SURFACE; CELLULAR DISTRIBUTION; HYDROPHILICITY; HYDROPHOBICITY; MOLECULAR IMAGING; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PSEUDOMONAS FLUORESCENS; SINGLE CELL ANALYSIS; SPECTROSCOPY;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BIOFILMS; BIOMECHANICAL PHENOMENA; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MICROSCOPY, ATOMIC FORCE; PSEUDOMONAS FLUORESCENS;

EID: 84896691249     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb400794e     Document Type: Article

References (42)

1. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappin-Scott, H. M. (1995) Microbial biofilms Annu. Rev. Microbiol. 49, 711-745
2. Costerton, J. W., Stewart, P. S., and Greenberg, E. P. (1999) Bacterial biofilms: a common cause of persistent infections Science 284, 1318-1322
3. Davey, M. E. and O'Toole G, A. (2000) Microbial biofilms: from ecology to molecular genetics Microbiol. Mol. Biol. Rev. 64, 847-867
4. Kolter, R. and Greenberg, E. P. (2006) Microbial sciences: The superficial life of microbes Nature 441, 300-302
5. O'Toole, G., Kaplan, H. B., and Kolter, R. (2000) Biofilm formation as microbial development Annu. Rev. Microbiol. 54, 49-79
6. Dekkers, L. C., Bloemendaal, C. J., de Weger, L. A., Wijffelman, C. A., Spaink, H. P., and Lugtenberg, B. J. (1998) A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365 Mol. Plant-Microbe Interact. 11, 45-56
7. Dekkers, L. C., Phoelich, C. C., van der Fits, L., and Lugtenberg, B. J. (1998) A site-specific recombinase is required for competitive root colonization by Pseudomonas fluorescens WCS365 Proc. Natl. Acad. Sci. U.S.A. 95, 7051-7056
8. Dekkers, L. C., van der Bij, A. J., Mulders, I. H., Phoelich, C. C., Wentwoord, R. A., Glandorf, D. C., Wijffelman, C. A., and Lugtenberg, B. J. (1998) Role of the O-antigen of lipopolysaccharide, and possible roles of growth rate and of NADH:ubiquinone oxidoreductase (nuo) in competitive tomato root-tip colonization by Pseudomonas fluorescens WCS365 Mol. Plant-Microbe Interact. 11, 763-771
9. Simons, M., van der Bij, A. J., Brand, I., de Weger, L. A., Wijffelman, C. A., and Lugtenberg, B. J. (1996) Gnotobiotic system for studying rhizosphere colonization by plant growth-promoting Pseudomonas bacteria Mol. Plant-Microbe Interact. 9, 600-607
10. Duque, E., de la Torre, J., Bernal, P., Molina-Henares, M. A., Alaminos, M., Espinosa-Urgel, M., Roca, A., Fernandez, M., de Bentzmann, S., and Ramos, J. L. (2013) Identification of reciprocal adhesion genes in pathogenic and non-pathogenic Pseudomonas Environ. Microbiol. 15, 36-48
11. Newell, P. D., Boyd, C. D., Sondermann, H., and O'Toole, G. A. (2011) A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage PLoS Biol. 9, e1000587
12. O'Toole, G. A. and Kolter, R. (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis Mol. Microbiol. 28, 449-461
13. Spiers, A. J. and Rainey, P. B. (2005) The Pseudomonas fluorescens SBW25 wrinkly spreader biofilm requires attachment factor, cellulose fibre and LPS interactions to maintain strength and integrity Microbiology 151, 2829-2839
14. Haas, D. and Defago, G. (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads Nat. Rev. Microbiol. 3, 307-319
15. Picot, L., Abdelmoula, S. M., Merieau, A., Leroux, P., Cazin, L., Orange, N., and Feuilloley, M. G. (2001) Pseudomonas fluorescens as a potential pathogen: adherence to nerve cells Microbes Infect. 3, 985-995
16. Picot, L., Mezghani-Abdelmoula, S., Chevalier, S., Merieau, A., Lesouhaitier, O., Guerillon, J., Cazin, L., Orange, N., and Feuilloley, M. G. (2004) Regulation of the cytotoxic effects of Pseudomonas fluorescens by growth temperature Res. Microbiol. 155, 39-46
17. Hinsa, S. M., Espinosa-Urgel, M., Ramos, J. L., and O'Toole, G. A. (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein Mol. Microbiol. 49, 905-918
18. Ivanov, I. E., Boyd, C. D., Newell, P. D., Schwartz, M. E., Turnbull, L., Johnson, M. S., Whitchurch, C. B., O'Toole, G. A., and Camesano, T. A. (2012) Atomic force and super-resolution microscopy support a role for LapA as a cell-surface biofilm adhesin of Pseudomonas fluorescens Res. Microbiol. 163, 685-691
19. Monds, R. D., Newell, P. D., Gross, R. H., and O'Toole, G. A. (2007) Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA Mol. Microbiol. 63, 656-679
20. Yousef, F. and Espinosa-Urgel, M. (2007) In silico analysis of large microbial surface proteins Res. Microbiol. 158, 545-550
21. Navarro, M. V., Newell, P. D., Krasteva, P. V., Chatterjee, D., Madden, D. R., O'Toole, G. A., and Sondermann, H. (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis PLoS Biol. 9, e1000588
22. Newell, P. D., Monds, R. D., and O'Toole, G. A. (2009) LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1 Proc. Natl. Acad. Sci. U.S.A. 106, 3461-3466
23. Boyd, C. D. and O'Toole, G. A. (2012) Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems Annu. Rev. Cell. Dev. Biol. 28, 439-462
24. Romling, U., Galperin, M. Y., and Gomelsky, M. (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger Microbiol. Mol. Biol. Rev. 77, 1-52
25. Boyd, C. D., Chatterjee, D., Sondermann, H., and O'Toole, G. A. (2012) LapG, required for modulating biofilm formation by Pseudomonas fluorescens Pf0-1, is a calcium-dependent protease J. Bacteriol. 194, 4406-4414
26. Hinsa, S. M. and O'Toole, G. A. (2006) Biofilm formation by Pseudomonas fluorescens WCS365: a role for LapD Microbiology 152, 1375-1383
27. Helenius, J., Heisenberg, C. P., Gaub, H. E., and Muller, D. J. (2008) Single-cell force spectroscopy J. Cell Sci. 121, 1785-1791
28. Müller, D. J., Helenius, J., Alsteens, D., and Dufreîne, Y. F. (2009) Force probing surfaces of living cells to molecular resolution Nat. Chem. Biol. 5, 383-390
29. Dupres, V., Menozzi, F. D., Locht, C., Clare, B. H., Abbott, N. L., Cuenot, S., Bompard, C., Raze, D., and Dufrene, Y. F. (2005) Nanoscale mapping and functional analysis of individual adhesins on living bacteria Nat. Methods 2, 515-520
30. Hinterdorfer, P. and Dufrene, Y. F. (2006) Detection and localization of single molecular recognition events using atomic force microscopy Nat. Methods 3, 347-355
31. Beaussart, A., El-Kirat-Chatel, S., Herman, P., Alsteens, D., Mahillon, J., Hols, P., and Dufrene, Y. F. (2013) Single-cell force spectroscopy of probiotic bacteria Biophys. J. 104, 1886-1892
32. Alsteens, D., Garcia, M. C., Lipke, P. N., and Dufrene, Y. F. (2010) Force-induced formation and propagation of adhesion nanodomains in living fungal cells Proc. Natl. Acad. Sci. U.S.A. 107, 20744-20749
33. McNab, R., Forbes, H., Handley, P. S., Loach, D. M., Tannock, G. W., and Jenkinson, H. F. (1999) Cell wall-anchored CshA polypeptide (259 kDas) in Streptococcus gordonii forms surface fibrils that confer hydrophobic and adhesive properties J. Bacteriol. 181, 3087-3095
34. Fuqua, C. (2010) Passing the baton between laps: adhesion and cohesion in Pseudomonas putida biofilms Mol. Microbiol. 77, 533-536
35. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M., and Gaub, H. E. (1997) Reversible unfolding of individual titin immunoglobulin domains by AFM Science 276, 1109-1112
36. Rief, M., Pascual, J., Saraste, M., and Gaub, H. E. (1999) Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles J. Mol. Biol. 286, 553-561
37. Griessl, M. H., Schmid, B., Kassler, K., Braunsmann, C., Ritter, R., Barlag, B., Stierhof, Y. D., Sturm, K. U., Danzer, C., Wagner, C., Schaffer, T. E., Sticht, H., Hensel, M., and Muller, Y. A. (2013) Structural insight into the giant Ca(2)(+)-binding adhesin SiiE: implications for the adhesion of Salmonella enterica to polarized epithelial cells Structure 21, 741-752
38. Beaussart, A., Alsteens, D., El-Kirat-Chatel, S., Lipke, P. N., Kucharikova, S., Van Dijck, P., and Dufrene, Y. F. (2012) Single-molecule imaging and functional analysis of Als adhesins and mannans during Candida albicans morphogenesis ACS Nano 6, 10950-10964
39. Henrici, A. T. (1933) Studies of freshwater bacteria: I. A direct microscopic technique J. Bacteriol. 25, 277-287
40. Zobell, C. E. (1937) The influence of solid surface upon the physiological activities of bacteria in seawater J. Bacteriol. 33, 86
41. Zobell, C. E. (1943) The effect of solid surfaces upon bacterial activity J. Bacteriol. 46, 39-56
42. Monds, R. D., Newell, P. D., Schwartzman, J. A., and O'Toole, G. A. (2006) Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1 Appl. Environ. Microbiol. 72, 1910-1924