Chapter 18 : Aggregation and Dispersal on Mucosal Surfaces

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Aggregation and Dispersal on Mucosal Surfaces, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap18-1.gif /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap18-2.gif


This chapter considers two additional facets of adherence: (i) that in addition to adhering to a surface, bacteria often adhere to each other; and (ii) that colonization is sometimes promoted by relinquishing adherence. It focuses on bacterial aggregation. Bacteria adhering to mucosal surfaces commonly exhibit interbacterial aggregation or agglutination, perhaps with relatively few points of anchorage to the substratum. On the mucosa, interbacterial aggregation presumably plays the same biophysical role as it does on abiotic substrata, although data to this effect are few. Recent studies demonstrated that aggregation mediated by antigen 43 (Ag43) protects bacteria from HO-dependent killing. The study of aggregation and biofilm formation by staphylococcal species continues to represent the paradigm for bacterial infections. Bacterial aggregation and microcolony formation are considered to be an initial stage of biofilm formation. Biofilms of represent bacteria embedded in an alginate polysaccharide matrix. Instead of a shortening and thickening of the fimbriae as seen with enteropathogenic (EPEC), meningococci (MC) shed their fimbriae completely and initiate a complex signal transduction cascade within the cell. Dispersin mutants are deficient in colonization of the streptomycin-treated mouse model, suggesting that enteroaggregative (EAEC) mutants exhibiting collapsed fimbriae and hyperaggretation are not able to establish colonization of the intestine. Although each bacterium interacting with a mucosal surface must modify its colonization approach to fit its particular life-style and survival strategy, comparative biology continues to indentify new conserved general functions such as aggregation and its counterpoint, dispersal.

Citation: Nataro J, Jansen A. 2005. Aggregation and Dispersal on Mucosal Surfaces, p 253-263. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch18

Key Concept Ranking

Type III Secretion System
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of Figure 1
Figure 1

Dispersal of biofilm colonies of various oral bacteria growing attached to polystyrene petri dishes. The growing colonies release cells into the medium, and the released cells attach to the surface of the petri dish and form new colonies, enabling the biofilms to spread. The bacteria were stained with crystal violet. (A) (B) (C) (D) Bar, 0.5 μm in panel A and 2 μm in others. Panels A and C from reference 35. Courtesy of Dr. Jeffery Kaplan.

Citation: Nataro J, Jansen A. 2005. Aggregation and Dispersal on Mucosal Surfaces, p 253-263. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch18
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Mutation in the dispersin-encoding gene results in collapse of AAF/II fimbriae onto the surface of the bacterium, precluding interbacterial adherence at a distance. (A) 042. (B) 042

Citation: Nataro J, Jansen A. 2005. Aggregation and Dispersal on Mucosal Surfaces, p 253-263. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch18
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Allison, D. G.,, D. J. Evans,, M. R. Brown,, and P. Gilbert. 1990. Possible involvement of the division cycle in dispersal of Escherichia coli from biofilms. J. Bacteriol. 172:16671669.
2. Anantha, R. P.,, K. D. Stone,, and M. S. Donnenberg. 1998. Role of BfpF, a member of the PilT family of putative nucleotide-binding proteins, in type IV pilus biogenesis and in interactions between enteropathogenic Escherichia coli and host cells. Infect. Immun. 66:122131.
3. Austin, J. W.,, G. Sanders,, W. W. Kay,, and S. K. Collinson. 1998. Thin aggregative fimbriae enhance Salmonella enteritidis biofilm formation. FEMS Microbiol. Lett. 162:295301.
4. Bassler, B. L. 2002. Small talk. Cell-to-cell communication in bacteria. Cell 109:421424.
5. Benitez, J. A.,, R. G. Spelbrink,, A. Silva,, T. E. Phillips,, C. M. Stanley,, M. Boesman-Finkelstein,, and R. A. Finkelstein. 1997. Adherence of Vibrio cholerae to cultured differentiated human intestinal cells: an in vitro colonization model. Infect. Immun. 65:34743477.
6. Bieber, D.,, S. W. Ramer,, C. Y. Wu,, W. J. Murray,, T. Tobe,, R. Fernandez,, and G. K. Schoolnik. 1998. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 280:21142118.
7. Booth, B. A.,, M. Boesman-Finkelstein,, and R. A. Finkelstein. 1983. Vibrio cholerae soluble hemagglutinin/protease is a metalloenzyme. Infect. Immun. 42:639644.
8. Boyd, A.,, and A. M. Chakrabarty. 1995. Pseudomonas aeruginosa biofilms: role of the alginate exopolysaccharide. J. Ind. Microbiol. 15:162168.
9. Boyd, A.,, and A. M. Chakrabarty. 1994. Role of alginate lyase in cell detachment of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 60:23552359.
10. Brading, M. G.,, J. Jass,, and H. M. Lappin-Scott,. 1995. Dynamics of bacterial biofilm formation, p. 4663. In H. M. Lappin-Scott, and J. W. Costerton (ed.), Microbial Biofilms. Cambridge University Press, Cambridge, United Kingdom.
11. Brown, P. K.,, C. M. Dozois,, C. A. Nickerson,, A. Zuppardo,, J. Terlonge,, and R. Curtiss, 3rd. 2001. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. Mol. Microbiol. 41:349363.
12. Cleary, J.,, L. C. Lai,, R. K. Shaw,, A. Straatman-Iwanowska,, M. S. Donnenberg,, G. Frankel,, and S. Knutton. 2004. Enteropathogenic Escherichia coli (EPEC) adhesion to intestinal epithelial cells: role of bundle-forming pili (BFP), EspA filaments and intimin. Microbiology 150:527538.
13. Collinson, S. K.,, S. C. Clouthier,, J. L. Doran,, P. A. Banser,, and W. W. Kay. 1996. Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J. Bacteriol. 178:662667.
14. Costerton, J. W.,, and P. S. Stewart,. 2000. Biofilms and device-related infections, p. 423439. In J. P. Nataro,, M. J. Blaser,, and S. Cunningham-Rundles (ed.), Persistent Bacterial Infections. American Society for Microbiology, Washington, D.C.
15. Costerton, J. W. 1999. Introduction to biofilm. Int. J. Antimicrob. Agents 11:217221,237-239.
16. Costerton, J. W.,, Z. Lewandowski,, D. E. Caldwell,, D. R. Korber,, and H. M. Lappin-Scott. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49:711745.
17. Costerton, J. W.,, P. S. Stewart,, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:13181322.
18. Costerton, W.,, R. Veeh,, M. Shirtliff,, M. Pasmore,, C. Post,, and G. Ehrlich. 2003. The application of biofilm science to the study and control of chronic bacterial infections. J. Clin. Investig. 112:14661477.
19. Danese, P. N.,, L. A. Pratt,, S. L. Dove,, and R. Kolter. 2000. The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms. Mol. Microbiol. 37:424432.
20. Donlan, R. M.,, and J. W. Costerton. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167193.
21. Dow, J. M.,, L. Crossman,, K. Findlay,, Y. Q. He,, J. X. Feng,, and J. L. Tang. 2003. Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc. Natl. Acad. Sci. USA 100: 1099511000.
22. Finkelstein, R. A.,, and L. F. Hanne. 1982. Purification and characterization of the soluble hemagglutinin (cholera lectin) produced by Vibrio cholerae. Infect. Immun. 36:11991208.
23. Frick, I. M.,, M. Morgelin,, and L. Bjorck. 2000. Virulent aggregates of Streptococcus pyogenes are generated by homophilic protein-protein interactions. Mol. Microbiol. 37: 12321247.
24. Gilbert, P.,, D. J. Evans,, and M. R. Brown. 1993. Formation and dispersal of bacterial biofilms in vivo and in situ. J. Appl. Bacteriol. 74(Suppl):67S78S.
25. Hase, C. C.,, and R. A. Finkelstein. 1991. Cloning and nucleotide sequence of the Vibrio cholerae hemagglutinin/ protease (HA/protease) gene and construction of an HA/ protease-negative strain. J. Bacteriol. 173:33113317.
26. Hase, C. C.,, and R. A. Finkelstein. 1990. Comparison of the Vibrio cholerae hemagglutinin/protease and the Pseudomonas aeruginosa elastase. Infect. Immun. 58:40114015.
27. Hasman, H.,, T. Chakraborty,, and P. Klemm. 1999. Antigen- 43-mediated autoaggregation of Escherichia coli is blocked by fimbriation. J. Bacteriol. 181:48344841.
28. Henderson, I. R.,, M. Meehan,, and P. Owen. 1997. Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol. Lett. 149:115120.
29. Henderson, I. R.,, M. Meehan,, and P. Owen. 1997. A novel regulatory mechanism for a novel phase-variable outer membrane protein of Escherichia coli. Adv. Exp. Med. Biol. 412: 349355.
30. Henderson, I. R.,, and P. Owen. 1999. The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving Dam and oxyR. J. Bacteriol. 181:21322141.
31. Henrichsen, J. 1983. Twitching motility. Annu. Rev. Microbiol. 37:8193.
32. Jones, G. W.,, G. D. Abrams,, and R. Freter. 1976. Adhesive properties of Vibrio cholerae: adhesion to isolated rabbit brush border membranes and hemagglutinating activity. Infect. Immun. 14:232239.
33. Kaiser, D. 2000. Bacterial motility: how do pili pull? Curr. Biol. 10:R777R780.
34. Kaiser, D. 1979. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc. Natl. Acad. Sci. USA 76: 59525956.
35. Kaplan, J. B.,, and D. H. Fine. 2002. Biofilm dispersal of Neisseria subflava and other phylogenetically diverse oral bacteria. Appl. Environ. Microbiol. 68:49434950.
36. Kaplan, J. B.,, M. F. Meyenhofer,, and D. H. Fine. 2003. Biofilm growth and detachment of Actinobacillus actinomycetemcomitans. J. Bacteriol. 185:13991404.
37. Kaplan, J. B.,, C. Ragunath,, N. Ramasubbu,, and D. H. Fine. 2003. Detachment of Actinobacillus actinomycetemcomitans biofilm cells by an endogenous beta-hexosaminidase activity. J. Bacteriol. 185:46934698.
38. Kjaergaard, K.,, M. A. Schembri,, H. Hasman,, and P. Klemm. 2000. Antigen 43 from Escherichia coli induces inter- and intraspecies cell aggregation and changes in colony morphology of Pseudomonas fluorescens. J. Bacteriol. 182:47894796.
39. Knutton, S.,, R. K. Shaw,, R. P. Anantha,, M. S. Donnenberg,, and A. A. Zorgani. 1999. The type IV bundle-forming pilus of enteropathogenic Escherichia coli undergoes dramatic alterations in structure associated with bacterial adherence, aggregation and dispersal. Mol. Microbiol. 33:499509.
40. Mah, T. F.,, B. Pitts,, B. Pellock,, G. C. Walker,, P. S. Stewart,, and G. A. O’Toole. 2003. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306310.
41. Maira-Litran, T.,, A. Kropec,, D. Goldmann,, and G. B. Pier. 2004. Biologic properties and vaccine potential of the staphylococcal poly-N-acetyl glucosamine surface polysaccharide. Vaccine 22:872879.
42. Mattick, J. S. 2002. Type IV pili and twitching motility. Annu. Rev. Microbiol. 56:289314.
43. McBride, M. J. 2001. Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55:4975.
44. McCormick, B. A.,, P. Klemm,, K. A. Krogfelt,, R. L. Burghoff,, L. Pallesen,, D. C. Laux,, and P. S. Cohen. 1993. Escherichia coli F-18 phase locked ‘on’ for expression of type 1 fimbriae is a poor colonizer of the streptomycin-treated mouse large intestine. Microb. Pathog. 14:3343.
45. Merz, A. J.,, M. So,, and M. P. Sheetz. 2000. Pilus retraction powers bacterial twitching motility. Nature 407:98102.
46. Nelson, E. T.,, J. D. Clements,, and R. A. Finkelstein. 1976. Vibrio cholerae adherence and colonization in experimental cholera: electron microscopic studies. Infect. Immun. 14:527547.
47. Nougayrede, J. P.,, P. J. Fernandes,, and M. S. Donnenberg. 2003. Adhesion of enteropathogenic Escherichia coli to host cells. Cell. Microbiol. 5:359372.
48. Ochiai, K.,, T. Kurita-Ochiai,, Y. Kamino,, and T. Ikeda. 1993. Effect of co-aggregation on the pathogenicity of oral bacteria. J. Med. Microbiol. 39:183190.
49. Pujol, C.,, E. Eugene,, M. Marceau,, and X. Nassif. 1999. The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion. Proc. Natl. Acad. Sci. USA 96:40174022.
50. Robert, A.,, A. Silva,, J. A. Benitez,, B. L. Rodriguez,, R. Fando,, J. Campos,, D. K. Sengupta,, M. Boesman-Finkelstein,, and R. A. Finkelstein. 1996. Tagging a Vibrio cholerae El Tor candidate vaccine strain by disruption of its hemagglutinin/ protease gene using a novel reporter enzyme: Clostridium thermocellum endoglucanase A. Vaccine 14:15171522.
51. Romling, U.,, Z. Bian,, M. Hammar,, W. D. Sierralta,, and S. Normark. 1998. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J. Bacteriol. 180:722731.
52. Schembri, M. A.,, L. Hjerrild,, M. Gjermansen,, and P. Klemm. 2003. Differential expression of the Escherichia coli autoaggregation factor antigen 43. J. Bacteriol. 185:22362242.
53. Schreiner, H. C.,, K. Sinatra,, J. B. Kaplan,, D. Furgang,, S. C. Kachlany,, P. J. Planet,, B. A. Perez,, D. H. Figurski,, and D. H. Fine. 2003. Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model. Proc. Natl. Acad. Sci. USA 100:72957300.
54. Sheikh, J.,, J. R. Czeczulin,, S. Harrington,, S. Hicks,, I. R. Henderson,, C. Le Bouguenec,, P. Gounon,, A. Phillips,, and J. P. Nataro. 2002. A novel dispersin protein in enteroaggregative Escherichia coli. J. Clin. Investig. 110:13291337.
55. Skerker, J. M.,, and H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA 98:69016904.
56. Stone, K. D.,, H. Z. Zhang,, L. K. Carlson,, and M. S. Donnenberg. 1996. A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for the biogenesis of a type IV pilus. Mol. Microbiol. 20:325337.
57. Stoodley, P.,, Z. Lewandowski,, J. D. Boyle,, and H. M. Lappin- Scott. 1999. The formation of migratory ripples in a mixed species bacterial biofilm growing in turbulent flow. Environ. Microbiol. 1:447455.
58. Sukupolvi, S.,, R. G. Lorenz,, J. I. Gordon,, Z. Bian,, J. D. Pfeifer,, S. J. Normark,, and M. Rhen. 1997. Expression of thin aggregative fimbriae promotes interaction of Salmonella typhimurium SR-11 with mouse small intestinal epithelial cells. Infect. Immun. 65:53205325.
59. Torres, A. G.,, N. T. Perna,, V. Burland,, A. Ruknudin,, F. R. Blattner,, and J. B. Kaper. 2002. Characterization of Cah, a calcium-binding and heat-extractable autotransporter protein of enterohaemorrhagic Escherichia coli. Mol. Microbiol. 45:951966.
60. Waldron, D. E.,, P. Owen,, and C. J. Dorman. 2002. Competitive interaction of the OxyR DNA-binding protein and the Dam methylase at the antigen 43 gene regulatory region in Escherichia coli. Mol. Microbiol. 44:509520.
61. Wall, D.,, and D. Kaiser. 1999. Type IV pili and cell motility. Mol. Microbiol. 32:110.
62. Wolgemuth, C.,, E. Hoiczyk,, D. Kaiser,, and G. Oster. 2002. How myxobacteria glide. Curr. Biol. 12:369377.
63. Zhu, J.,, and J. J. Mekalanos. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev.Cell 5:647656.
64. Zhu, J.,, M. B. Miller,, R. E. Vance,, M. Dziejman,, B. L. Bassler,, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:31293134.
65. Zogaj, X.,, W. Bokranz,, M. Nimtz,, and U. Romling. 2003. Production of cellulose and curli fimbriae by members of the family Enterobacteriaceae isolated from the human gastrointestinal tract. Infect. Immun. 71:41514158.
66. Zolfaghar, I.,, D. J. Evans,, and S. M. Fleiszig. 2003. Twitching motility contributes to the role of pili in corneal infection caused by Pseudomonas aeruginosa. Infect. Immun. 71:53895393.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error