1887

Chapter 15 : Role of the Mucus Layer in Bacterial Colonization of the Intestine

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

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Role of the Mucus Layer in Bacterial Colonization of the Intestine, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap15-1.gif /docserver/preview/fulltext/10.1128/9781555817619/9781555813239_Chap15-2.gif

Abstract:

This chapter focuses on the mucus layer of the intestinal tract and its role in colonization of the intestine by enteric bacteria. The gel-like mucus layer of the intestine is dynamic in that it is continuously being renewed by secretion of stored or newly synthesized components, sloughed or eroded by mechanical forces, and degraded by the indigenous flora. In addition to the major gel-forming mucins present, the mucus layer contains a variety of proteins, carbohydrates, lipids, nucleic acids, and other components that originate from a number of sources. The presence of the intestinal mucus layer as a viscous physical barrier and the need for bacteria to reach and maintain themselves in an appropriate environmental niche has led many investigators to propose chemotaxis and motility as important aspects of colonization for the microorganisms that exhibit these properties. In the case of the normal flora of the large intestine, association with the mucosal surface appears to be a critical aspect of colonization and, depending on the organism, may or may not involve direct adhesion to epithelial cells. The lumen of the upper intestine may contain a number of microorganisms, but the rate of bacterial growth in the lumen in these regions does not does not appear to be high enough to compensate for the rapid flow of luminal contents. The types of experiments being used to elucidate the carbon nutrition for colonization of can and should be extended to include other members of the intestinal microflora.

Citation: Laux D, Cohen P, Conway T. 2005. Role of the Mucus Layer in Bacterial Colonization of the Intestine, p 199-212. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch15

Key Concept Ranking

Type III Secretion System
0.43477035
Type 1 Fimbriae
0.40609363
0.43477035
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555817619.chap15
1. Allen, A., 1989. Gastrointestinal mucus, p. 359382. In J. G. Forte (ed.), Handbook of Physiology. The Gastrointestinal System. Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion, vol. III. American Physiology Society, Bethesda, Md.
2. Allen, A.,, A. Bell,, M. Mantle,, and J. P. Pearson. 1982. The structure and physiology of gastrointestinal mucus. Adv. Exp. Med. Biol. 144:115133.
3. Allen, A.,, and L. C. Hoskins,. 1988. Colonic mucus in health and disease, p. 6594. In J. B. Kirsner, and R. G. Shorter (ed.), Diseases of the Rectum and Colon. The Williams & Wilkins Co., Baltimore, Md.
4. Allen-Vercoe, E.,, A. R. Sayers,, and M. J. Woodward. 1999. Virulence of Salmonella enterica serotype Enteritidis aflagellate and afimbriate mutants in a day-old chick model. Epidemiol. Infect. 122:395402.
5. Allen-Vercoe, E.,, and M. J. Woodward. 1999. The role of flagella, but not fimbriae, in the adherence of Salmonella enterica serotype Enteritidis to chick gut explant. J. Med. Microbiol. 48:771780.
6. Apperloo-Renkema, H. Z.,, B. D. VanderWaaij,, and D. Van der Waaij. 1990. Determination of colonization resistance of the digestive tract by biotyping of Enterobacteriaceae. Epidemiol. Infect. 105:355361.
7. Atuma, C.,, V. Strugala,, A. Allen,, and L. Holm. 2001. The adherent gastrointestinal mucus gel layer: thickness and physical state in vivo. Am. J. Physiol. Ser G. 280:G922G929.
8. Beachey, E. H. 1981. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J. Infect. Dis. 143:325345.
9. Bernet, M. F.,, D. Brassart,, J. R. Neeser,, and A. L. Servin. 1994. Lactobacillus acidophilus LA1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35:483489.
10. Blomfield, I. C.,, and M. van der Woude,. 2002. Regulation and function of phase variation in Escherichia coli, p. 89113. In M. Wilson (ed.), Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Cambridge University Press, Cambridge, United Kingdom.
11. Boddicker, J. D.,, N. A. Ledeboer,, J. Jagnow,, B. D. Jones,, and S. Clegg. 2002. Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar Typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol. Microbiol. 45:12551265.
12. Borrelio, S. P., 1986. Microbial flora of the gastro-intestinal tract, p. 216. In M. J. Hill (ed.), Microbial Metabolism in the Digestive Tract. CRC Press, Inc., Boca Raton, Fla.
13. Brook, I. 1999. Bacterial interference. Crit. Rev. Microbiol. 25:155172.
14. Chang, D. E.,, D. J. Smalley,, D. L. Tucker,, M. P. Leatham,, W. E. Norris,, S. J. Stevenson,, A. B. Anderson,, J. E. Grissom,, D. C. Laux,, P. S. Cohen,, and T. Conway. 2004. Carbon nutrition of Escherichia coli in the mouse intestine. Proc. Nat. Acad. Sci. USA 101:74277432.
15. Cohen, P. S.,, J. C. Arruda,, T. J. Williams,, and D. C. Laux. 1985. Adhesion of a human fecal Escherichia coli strain to mouse colonic mucus. Infect. Immun. 48:139145.
16. Cohen, P. S.,, R. Rossoll,, V. J. Cabelli,, S. L. Yang,, and D. C. Laux. 1983. Relationship between the mouse-colonizing ability of a human fecal Escherichia coli strain and its ability to bind a specific mouse colonic mucous gel protein. Infect. Immun.40:6269.
17. Correa, N. E.,, C. M. Lauriano,, R. McGee,, and K. E. Klose. 2000. Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol. Microbiol. 35:743755.
18. Dean, E. A. 1990. Comparison of receptors for 987P pili of enterotoxigenic Escherichia coli in the small intestines of neonatal and older pig. Infect. Immun. 58:40304035.
19. Dekker, J.,, J. W. Rossen,, H. A. Buller,, and A. W. Einerhand. 2002. The MUC family: an obituary. Trends Biochem. Sci. 27:126131.
20. Dibb-Fuller, M. P.,, E. Allen-Vercoe,, C. J. Thorns,, and M. J. Woodward. 1999. Fimbriae- and flagella-mediated association with and invasion of cultured epithelial cells by Salmonella enteritidis. Microbiology 145:10231031.
21. Drasar, B. S.,, and P. A. Barrow. 1985. The bacterial flora of the normal intestine, p. 1940, Intestinal Microbiology, vol. 10. American Society for Microbiology, Washington, D.C.
22. Drumm, B.,, A. M. Roberton,, and P. M. Sherman. 1988. Inhibition of attachment of Escherichia coli RDEC-1 to intestinal microvillus membranes by rabbit ileal mucus and mucin in vitro. Infect. Immun. 56:24372442.
23. Dubos, R. 1966. Staphylococci and infection immunity. Am. J. Dis. Child. 105:643645.
24. Ducluzeau, R.,, M. Bellier,, and P. Raibaud. 1970. Transit through the digestive tract of the inocula of several bacterial strains introduced “per os” into axenic and “holoxenic” mice. The antagonistic effect of the microflora of the gastrointestinal tract. Zentbl. Bakteriol. Orig. 213:533548. (In German.)
25. Eaton, K. A.,, D. R. Morgan,, and S. Krakowka. 1992. Motility as a factor in the colonisation of gnotobiotic piglets by Helicobacter pylori. J. Med. Microbiol. 37:123127.
26. Eaton, K. A.,, S. Suerbaum,, C. Josenhans,, and S. Krakowka. 1996. Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes. Infect. Immun. 64:24452448.
27. Falk, P. G.,, L. V. Hooper,, T. Midtvedt,, and J. I. Gordon. 1998. Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62:11571170.
28. Finegold, S. M.,, V. L. Sutter,, and G. E. Mathisen,. 1983. Normal indigenous intestinal microflora, p. 331. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, Inc., New York, N.Y.
29. Forstner, J. F.,, and G. G. Forstner,. 1994. Gastrointestinal mucus, p. 12551283. In L. R. Johnson (ed.), Physiology of the Gastrointestinal Tract, 3rd ed., vol. 2. Raven Press, New York, N.Y.
30. Franklin, D. P.,, D. C. Laux,, T. J. Williams,, M. C. Falk,, and P. S. Cohen. 1990. Growth of Salmonella typhimurium SL5319 and Escherichia coli F-18 in mouse cecal mucus: role of peptides and iron. FEMS Micobiol. Ecol. 74:229240.
31. Freter, R. 1956. Experimental enteric Shigella and Vibrio infections in mice and guinea pigs. J. Exp. Med. 104:411418.
32. Freter, R., 1992. Factors affecting the microecology of the gut, p. 111144. In R. Fuller (ed.), Probiotics: the Scientific Basis. Chapman & Hall, London, United Kingdom.
33. Freter, R., 1988. Mechanisms of bacterial colonization of the mucosal surfaces of the gut, p. 4560. In J. A. Roth (ed.), Virulence Mechanisms of Bacterial Pathogens. American Society for Microbiology, Washington, D.C.
34. Freter, R., 1983. Mechanisms that control the microflora in the large intestine, p. 3354. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, Inc., New York, N.Y.
35. Freter, R. 1972. Parameters affecting the association of vibrios with the intestinal surface in experimental cholera. Infect. Immun. 6:134141.
36. Freter, R.,, P. C. O’Brien,, and M. S. Macsai. 1981. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect. Immun. 34:234240.
37. Gardel, C. L.,, and J. J. Mekalanos. 1996. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect. Immun. 64:22462255.
38. Gewirtz, A. T.,, T. A. Navas,, S. Lyons,, P. J. Godowski,, and J. L. Madara. 2001. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167:18821885.
39. Gewirtz, A. T.,, P. O. Simon, Jr.,, C. K. Schmitt,, L. J. Taylor,, C. H. Hagedorn,, A. D. O’Brien,, A. S. Neish,, and J. L. Madara. 2001. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J. Clin. Investig. 107:99109.
40. Giron, J. A.,, A. G. Torres,, E. Freer,, and J. B. Kaper. 2002. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol. Microbiol. 44:361379.
41. Guentzel, M. N.,, and L. J. Berry. 1975. Motility as a virulence factor for Vibrio cholerae. Infect. Immun. 11:890897.
42. He, G.,, R. A. Shankar,, M. Chzhan,, A. Samouilov,, P. Kuppusamy,, and J. L. Zweier. 1999. Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proc. Natl. Acad. Sci. USA 96:45864591.
43. Hentges, D. J., 1983. Role of the intestinal microflora in host defense against infection, p. 311331. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, Inc., New York, N.Y.
44. Hentges, D. J.,, J. U. Que,, S. W. Casey,, and A. J. Stein. 1984. The influence of streptomycin on colonization in mice. Microecol. Theor. 14:5362.
45. Hooper, L. V.,, T. Midtvedt,, and J. I. Gordon. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu. Rev. Nutr. 22:283307.
46. Hooper, L. V.,, J. Xu,, P. G. Falk,, T. Midtvedt,, and J. I. Gordon. 1999. A molecular sensor that allows a gut commensal to control its nutrient foundation in a competitive ecosystem. Proc. Natl. Acad. Sci. USA 96:98339838.
47. Hoskins, L. C.,, M. Agustines,, W. B. McKee,, E. T. Boulding,, M. Kriaris,, and G. Niedermeyer. 1985. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. J. Clin. Investig. 75:944953.
48. Hudault, S.,, J. Guignot,, and A. L. Servin. 2001. Escherichia coli strains colonising the gastrointestinal tract protect germfree mice against Salmonella typhimurium infection. Gut 49:4755.
49. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379433.
50. Hughes, K. T.,, K. L. Gillen,, M. J. Semon,, and J. E. Karlinsey. 1993. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 262:12771280.
51. Jonsson, H.,, E. Strom,, and S. Roos. 2001. Addition of mucin to the growth medium triggers mucus-binding activity in different strains of Lactobacillus reuteri in vitro. FEMS Microbiol. Lett. 204:1922.
52. Karjalainen, T.,, M. C. Barc,, A. Collignon,, S. Trolle,, H. Boureau,, J. Cotte-Laffitte,, and P. Bourlioux. 1994. Cloning of a genetic determinant from Clostridium difficile involved in adherence to tissue culture cells and mucus. Infect. Immun. 62:43474355.
53. Karjalainen, T.,, A. J. Waligora-Dupriet,, M. Cerquetti,, P. Spigaglia,, A. Maggioni,, P. Mauri,, and P. Mastrantonio. 2001. Molecular and genomic analysis of genes encoding surfaceanchored proteins from Clostridium difficile. Infect. Immun. 69:34423446.
54. Kennedy, M. J.,, E. L. Rosey,, and R. J. Yancey, Jr. 1997. Characterization of flaA- and flab- mutants of Serpulina hyodysenteriae: both flagellin subunits, FlaA and FlaB, are necessary for full motility and intestinal colonization. FEMS Microbiol. Lett. 153:119128.
55. Ketyi, I. 1994. Effectiveness of antibiotics on the autochthonous Escherichia coli of mice in the intestinal biofilm versus its planktonic phase. Acta Microbiol. Immunol. Hung. 41:189195.
56. Kolenbrander, P. E. 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu. Rev. Microbiol. 54:413437.
57. Kresse, A. U.,, F. Ebel,, and C. A. Guzman,. 2002. Functional modulation of pathogenic bacteria upon contact with host target cells, p. 203220. In M. Wilson (ed.), Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Cambridge University Press, Cambridge, United Kingdom.
58. Krivan, H. C.,, D. P. Franklin,, W. Wang,, D. C. Laux,, and P. S. Cohen. 1992. Phosphatidylserine found in intestinal mucus serves as a sole source of carbon and nitrogen for salmonellae and Escherichia coli. Infect. Immun. 60:39433946.
59. Krogfelt, K. A.,, B. A. McCormick,, R. L. Burghoff,, D. C. Laux,, and P. S. Cohen. 1991. Expression of Escherichia coli F-18 type 1 fimbriae in the streptomycin-treated mouse large intestine. Infect. Immun. 59:15671568.
60. Kutsukake, K. 1994. Excretion of the anti-sigma factor through a flagellar substructure couples flagellar gene expression with flagellar assembly in Salmonella typhimurium. Mol. Gen. Genet. 243:605612.
61. Lamont, J. T. 1992. Mucus: the front line of intestinal mucosal defense. Ann. N. Y. Acad. Sci. 664:190201.
62. La Ragione, R. M.,, A. R. Sayers,, and M. J. Woodward. 2000. The role of fimbriae and flagella in the colonization, invasion and persistence of Escherichia coli O78:K80 in the day-oldchick model. Epidemiol. Infect. 124:351363.
63. Laux, D. C.,, E. F. McSweegan,, and P. S. Cohen. 1984. Adhesion of enterotoxigenic Escherichia coli to immobilized intestinal mucosal preparations: a model of adhesion to mucosal surface components. J. Microbiol. Methods 2:2739.
64. Lee, A. 1985. Neglected niches. The microbial ecology of the gastrointestinal tract. Adv. Microb. Ecol. 8:115162.
65. Licht, T. R.,, B. B. Christensen,, K. A. Krogfelt,, and S. Molin. 1999. Plasmid transfer in the animal intestine and other dynamic bacterial populations: the role of community structure and environment. Microbiology 145:26152622.
66. Lievin, V.,, I. Peiffer,, S. Hudault,, F. Rochat,, D. Brassart,, J. R. Neeser,, and A. L. Servin. 2000. Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut 47:646652.
67. Lindahl, M.,, and I. Carlstedt. 1990. Binding of K99 fimbriae of enterotoxigenic Escherichia coli to pig small intestinal mucin glycopeptides. J. Gen. Microbiol. 136:16091614.
68. Lloyd, A. B.,, R. B. Cumming,, and R. D. Kent. 1977. Prevention of Salmonella typhimurium infection in poultry by pretreatment of chickens and poults with intestinal extracts. Aust. Vet. J. 53:8287.
69. Lockman, H. A.,, and R. Curtiss, 3rd. 1990. Salmonella typhimurium mutants lacking flagella or motility remain virulent in BALB/c mice. Infect. Immun. 58:137143.
70. Macfarlane, S.,, A. J. McBain,, and G. T. Macfarlane. 1997. Consequences of biofilm and sessile growth in the large intestine. Adv. Dent. Res. 11:5968.
71. Mack, D. R.,, and P. L. Blain-Nelson. 1995. Disparate in vitro inhibition of adhesion of enteropathogenic Escherichia coli RDEC-1 by mucins isolated from various regions of the intestinal tract. Pediatr. Res. 37:7580.
72. Mack, D. R.,, and P. M. Sherman. 1991. Mucin isolated from rabbit colon inhibits in vitro binding of Escherichia coli RDEC-1. Infect. Immun. 59:10151023.
73. MacNab, R. M., 1996. Flagella and motility, p. 123145. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella:Cellular and Molecular Biology, 2nd ed., vol. 1. ASM Press, Washington, D.C.
74. Mantle, M.,, L. Basaraba,, S. C. Peacock,, and D. G. Gall. 1989. Binding of Yersinia enterocolitica to rabbit intestinal brush border membranes, mucus, and mucin. Infect. Immun. 57:32923299.
75. Mantle, M.,, and S. D. Husar. 1993. Adhesion of Yersinia enterocolitica to purified rabbit and human intestinal mucin. Infect. Immun. 61:23402346.
76. Mantle, M.,, and S. D. Husar. 1994. Binding of Yersinia enterocolitica to purified, native small intestinal mucins from rabbits and humans involves interactions with the mucin carbohydrate moiety. Infect. Immun. 62:12191227.
77. McCormick, B. A.,, D. P. Franklin,, D. C. Laux,, and P. S. Cohen. 1989. Type 1 pili are not necessary for colonization of the streptomycin-treated mouse large intestine by type 1-piliated Escherichia coli F-18 and E. coli K-12. Infect. Immun. 57:30223029.
78. 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.
79. McCormick, B. A.,, D. C. Laux,, and P. S. Cohen. 1990. Neither motility nor chemotaxis plays a role in the ability of Escherichia coli F-18 to colonize the streptomycin-treated mouse large intestine. Infect. Immun. 58:29572961.
80. McCormick, B. A.,, B. A. Stocker,, D. C. Laux,, and P. S. Cohen. 1988. Roles of motility, chemotaxis, and penetration through and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestine of streptomycin-treated mice. Infect. Immun. 56:22092217.
81. McSweegan, E.,, D. H. Burr,, and R. I. Walker. 1987. Intestinal mucus gel and secretory antibody are barriers to Campylobacter jejuni adherence to INT 407 cells. Infect. Immun. 55:14311435.
82. McSweegan, E.,, and R. I. Walker. 1986. Identification and characterization of two Campylobacter jejuni adhesins for cellular and mucous substrates. Infect. Immun. 53:141148.
83. Midtvedt, T. 1985. The influence of antibiotics upon microflora- associated characteristics in man and animals. Prog. Clin. Biol. Res. 181:241244.
84. Miranda, R. L.,, T. Conway,, M. P. Leatham,, D. E. Chang,, W. E. Norris,, J. H. Allen,, S. J. Stevenson,, D. C. Laux,, and P. S. Cohen. 2004. Glycolytic and gluconeogenic growth of Escherichia coli O157:H7 (EDL933) and E. coli K-12 (MG1655) in the mouse intestine. Infect. Immun. 72:16661676.
85. Moens, S.,, and J. Vanderleyden. 1996. Functions of bacterial flagella. Crit. Rev. Microbiol. 22:67100.
86. Moller, A. K.,, M. P. Leatham,, T. Conway,, P. J. Nuijten,, L. A. de Haan,, K. A. Krogfelt,, and P. S. Cohen. 2003. An Escherichia coli MG1655 lipopolysaccharide deep-rough core mutant grows and survives in mouse cecal mucus but fails to colonize the mouse large intestine. Infect. Immun. 71:21422152.
87. Morooka, T.,, A. Umeda,, and K. Amako. 1985. Motility as an intestinal colonization factor for Campylobacter jejuni. J. Gen. Microbiol. 131:19731980.
88. Myhal, M. L.,, D. C. Laux,, and P. S. Cohen. 1982. Relative colonizing abilities of human fecal and K 12 strains of Escherichia coli in the large intestines of streptomycin-treated mice. Eur. J. Clin. Microbiol. 1:186192.
89. Neill, M. A., 1998. Treatment of disease due to Shiga toxinproducing Escherichia coli: Infectious disease management, p. 357363. In J. B. Kaper, and A. D. O’Brien (ed.), Escherichia coli O157:H7 and Other Shiga Toxin-Producing E. coli Strains. ASM Press, Washington, D.C.
90. Ottemann, K. M.,, and J. F. Miller. 1997. Roles for motility in bacterial-host interactions. Mol. Microbiol. 24:11091117.
91. Ouellette, A. J.,, and M. E. Selsted. 1996. Paneth cell defensins: endogenous peptide components of intestinal host defense. FASEB J. 10:12801289.
92. Ouwehand, A. C.,, E. Isolauri,, P. V. Kirjavainen,, S. Tolkko,, and S. J. Salminen. 2000. The mucus binding of Bifidobacterium lactis Bb12 is enhanced in the presence of Lactobacillus GG and Lact. delbrueckii subsp. bulgaricus. Lett. Appl. Microbiol. 30:1013.
93. Pavlovskis, O. R.,, D. M. Rollins,, R. L. Haberberger, Jr.,, A. E. Green,, L. Habash,, S. Strocko,, and R. I. Walker. 1991. Significance of flagella in colonization resistance of rabbits immunized with Campylobacter spp. Infect. Immun. 59:22592264.
94. Peekhaus, N.,, and T. Conway. 1998. What’s for dinner? Entner- Doudoroff metabolism in Escherichia coli. J. Bacteriol. 180:34953502.
95. Pierson, D. E., 2002. Induction of protein secretion by Yersinia enterocolitica through contact with eukaryotic cells, p. 183202. In M. Wilson (ed.), Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Cambridge University Press, Cambridge, United Kingdom.
96. Plano, G. V.,, J. B. Day,, and F. Ferracci. 2001. Type III export: new uses for an old pathway. Mol. Microbiol. 40:284293.
97. Postnova, T.,, O. G. Gomez-Duarte,, and K. Richardson. 1996. Motility mutants of Vibrio cholerae O1 have reduced adherence in vitro to human small intestinal epithelial cells as demonstrated by ELISA. Microbiology 142:27672776.
98. Poulsen, L. K.,, F. Lan,, C. S. Kristensen,, P. Hobolth,, S. Molin,, and K. A. Krogfelt. 1994. Spatial distribution of Escherichia coli in the mouse large intestine inferred from rRNA in situ hybridization. Infect. Immun. 62:51915194.
99. Poulsen, L. K.,, T. R. Licht,, C. Rang,, K. A. Krogfelt,, and S. Molin. 1995. Physiological state of Escherichia coli BJ4 growing in the large intestines of streptomycin-treated mice. J. Bacteriol. 177:58405845.
100. Pratt, L. A.,, and R. Kolter. 1998. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30:285293.
101. Probert, H. M.,, and G. R. Gibson. 2002. Bacterial biofilms in the human gastrointestinal tract. Curr. Issues Intest. Microbiol. 3:2327.
102. Relman, D. A.,, and S. Falkow. 2001. The meaning and impact of the human genome sequence for microbiology. Trends Microbiol. 9:206208.
103. Rickard, A. H.,, P. Gilbert,, N. J. High,, P. E. Kolenbrander,, and P. S. Handley. 2003. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 11:94100.
104. Robertson, J. M.,, G. Grant,, E. Allen-Vercoe,, M. J. Woodward,, A. Pusztai,, and H. J. Flint. 2000. Adhesion of Salmonella enterica var Enteritidis strains lacking fimbriae and flagella to rat ileal explants cultured at the air interface or submerged in tissue culture medium. J. Med. Microbiol. 49:691696.
105. Rojas, M.,, F. Ascencio,, and P. L. Conway. 2002. Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Appl. Environ. Microbiol. 68:23302336.
106. Rolfe, R. D. 1984. Role of volatile fatty acids in colonization resistance to Clostridium difficile. Infect. Immun. 45:185191.
107. Roos, S.,, and H. Jonsson. 2002. A high-molecular-mass cellsurface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148:433442.
108. Roos, S.,, F. Karner,, L. Axelsson,, and H. Jonsson. 2000. Lactobacillus mucosae sp. nov., a new species with in vitro mucusbinding activity isolated from pig intestine. Int. J. Syst. Evol. Microbiol. 50:251258.
109. Rozee, K. R.,, D. Cooper,, K. Lam,, and J. W. Costerton. 1982. Microbial flora of the mouse ileum mucous layer and epithelial surface. Appl. Environ. Microbiol. 43:14511463.
110. Salyers, A. A.,, and J. A. Z. Leedle,. 1983. Carbohydrate metabolism in the human colon, p. 129146. In D. J. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, Inc., New York, N.Y.
111. Savage, D. C., 1984. Adherence of the normal flora, p. 310. In E. C. Boedeker (ed.), Attachment of Organisms to the Gut Mucosa, vol. 1. CRC Press, Inc., Boca Raton, Fla.
112. Savage, D. C., 1983. Associations of indigenous microorganisms with gastrointestinal epithelial surfaces, p. 5578. In D. H. Hentges (ed.), Human Intestinal Microflora in Health and Disease. Academic Press, Inc., New York, N.Y.
113. Savage, D. C., 1985. Effects on host animals of bacteria adhering to epithelial surfaces, p. 437463. In D. C. Savage, and M. Fletcher (ed.), Bacterial Adhesion: Mechanisms and Physiological Significance. Plenum Press, New York, N.Y.
114. Sheikh, J.,, S. Hicks,, M. Dall’Agnol,, A. D. Phillips,, and J. P. Nataro. 2001. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol. Microbiol. 41:983997.
115. Simon, G. L.,, and S. L. Gorbach. 1984. Intestinal flora in health and disease. Gastroenterology 86:174193.
116. Slater, J. H., 1988. Microbial populations and community dynamics, p. 5174. In J. M. Lynch, and J. E. Hobbie (ed.), Microorganisms in Action: Concepts and Applications in Microbial Ecology. Blackwell Scientific Publications Ltd., Oxford, United Kingdom.
117. Smith, C. J.,, J. B. Kaper,, and D. R. Mack. 1995. Intestinal mucin inhibits adhesion of human enteropathogenic Escherichia coli to HEp-2 cells. J. Pediatr. Gastroenterol. Nutr. 21:269276.
118. Stanton, T. B.,, and D. C. Savage. 1984. Motility as a factor in bowel colonization by Roseburia cecicola, an obligately anaerobic bacterium from the mouse caecum. J. Gen. Microbiol. 130:173183.
119. Stock, J. B.,, and M. G. Surette,. 1996. Chemotaxis, p. 11031129. In F. C. Neidhardt,, R. Curtiss III,, J. L. Ingraham,, E. C. C. Lin,, K. B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: 2nd ed., vol. 1. ASM Press, Washington, D.C.
120. Strous, G. J.,, and J. Dekker. 1992. Mucin-type glycoproteins. Crit. Rev. Biochem. Mol. Biol. 27:5792.
121. Sweeney, N. J.,, P. Klemm,, B. A. McCormick,, E. Moller- Nielsen,, M. Utley,, M. A. Schembri,, D. C. Laux,, and P. S. Cohen. 1996. The Escherichia coli K-12 gntP gene allows E. coli F-18 to occupy a distinct nutritional niche in the streptomycin- treated mouse large intestine. Infect. Immun. 64:34973503.
122. Sweeney, N. J.,, D. C. Laux,, and P. S. Cohen. 1996. Escherichia coli F-18 and E. coli K-12 eda mutants do not colonize the streptomycin-treated mouse large intestine. Infect. Immun. 64:35043511.
123. Sylvester, F. A.,, D. Philpott,, B. Gold,, A. Lastovica,, and J. F. Forstner. 1996. Adherence to lipids and intestinal mucin by a recently recognized human pathogen, Campylobacter upsaliensis. Infect. Immun. 64:40604066.
124. Takata, T.,, S. Fujimoto,, and K. Amako. 1992. Isolation of nonchemotactic mutants of Campylobacter jejuni and their colonization of the mouse intestinal tract. Infect. Immun. 60:35963600.
125. Tannock, G. W., 1997. Normal microbiota of the gastrointestinal tract of rodents, p. 187215. In R. I. Mackie,, B. A. White,, and R. E. Isaacson (ed.), Gastrointestinal Microbiology, vol. 2. Chapman & Hall, London, United Kingdom.
126. Tasteyre, A.,, M. C. Barc,, A. Collignon,, H. Boureau,, and T. Karjalainen. 2001. Role of FliC and FliD flagellar proteins of Clostridium difficile in adherence and gut colonization. Infect. Immun. 69:79377940.
127. Taylor, C.,, and I. S. Roberts,. 2002. The regulation of capsule expression, p. 115138. In M. Wilson (ed.), Bacterial Adhesion to Host Tissues: Mechanisms and Consequences. Cambridge University Press, Cambridge, United Kingdom.
128. Taylor, P. A.,, and P. J. Williams. 1975. Theoretical studies on the coexistence of competing species under continuous-flow conditions. Can. J. Microbiol. 21:9098.
129. Tilman, D. 1982. Resource competition and community structure. Monogr. Popul. Biol. 17:1296.
130. Van de Bovenkamp, J. H.,, J. Mahdavi,, A. M. Korteland-Van Male,, H. A. Buller,, A. W. Einerhand,, T. Boren,, and J. Dekker. 2003. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter 8:521532.
131. van der Waaij, D.,, J. M. Berghuis-de Vries,, and J. E. Lekkerkerk. 1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. (London) 69:405411.
132. Vimal, D. B.,, M. Khullar,, S. Gupta,, and N. K. Ganguly. 2000. Intestinal mucins: the binding sites for Salmonella typhimurium. Mol. Cell. Biochem. 204:107117.
133. Wadolkowski, E. A.,, D. C. Laux,, and P. S. Cohen. 1988. Colonization of the streptomycin-treated mouse large intestine by a human fecal Escherichia coli strain: role of adhesion to mucosal receptors. Infect. Immun. 56:10361043.
134. Waligora, A. J.,, C. Hennequin,, P. Mullany,, P. Bourlioux,, A. Collignon,, and T. Karjalainen. 2001. Characterization of a cell surface protein of Clostridium difficile with adhesive properties. Infect. Immun. 69:21442153.
135. Wassenaar, T. M.,, B. A. van der Zeijst,, R. Ayling,, and D. G. Newell. 1993. Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J. Gen. Microbiol. 139:11711175.
136. Xu, J.,, and J. I. Gordon. 2003. Inaugural Article. Honor thy symbionts. Proc. Natl. Acad. Sci. USA 100:1045210459.
137. Young, G. M.,, J. L. Badger,, and V. L. Miller. 2000. Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect. Immun. 68:43234326.

Tables

Generic image for table
Table 1

MG1655 and EDL933 global regulatory mutant colonizations

Citation: Laux D, Cohen P, Conway T. 2005. Role of the Mucus Layer in Bacterial Colonization of the Intestine, p 199-212. In Nataro J, Cohen P, Mobley H, Weiser J (ed), Colonization of Mucosal Surfaces. ASM Press, Washington, DC. doi: 10.1128/9781555817619.ch15

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