Mouse intestine selects nonmotile flhDC mutants of Escherichia coli MG1655 with increased colonizing ability and better utilization of carbon sources

Infection and Immunity

Volumn 73, Issue 12, 2005, Pages 8039-8049

  Leatham, Mary P ^a   Stevenson, Sarah J ^a   Gauger, Eric J ^a   Krogfelt, Karen A ^b   Lins, Jeremy J ^a   Haddock, Traci L ^a   Autieri, Steven M ^a   Conway, Tyrrell ^c   Cohen, Paul S ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b STATENS SERUM INSTITUT   (Denmark)

^c UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; FUCOSE; GLUCONIC ACID; GLUCURONIC ACID; MANNOSE; N ACETYLGLUCOSAMINE; RIBOSE; STREPTOMYCIN; SUGAR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GROWTH; CARBON UTILIZATION; CATABOLISM; CONTROLLED STUDY; ESCHERICHIA COLI; ESCHERICHIA COLI MG1655; FLHDC GENE; GENE MUTATION; GENETIC SELECTION; INTESTINE INFECTION; MOUSE; NONHUMAN; OPERON; PRIORITY JOURNAL; REGULATOR GENE;

ANIMALS; CARBOHYDRATE METABOLISM; DNA-BINDING PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENES, BACTERIAL; GLUCONATES; INTESTINES; MICE; TRANS-ACTIVATORS;

EID: 28444483927     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.12.8039-8049.2005     Document Type: Article

References (46)

1. Anderson, J. D., W. A. Gillespie, and M. H. Richmond. 1973. Chemotherapy and antibiotic-resistance transfer between enterobacteria in the human gastro-intestinal tract. J. Med. Microbiol. 6:461-473.
2. Barker, C. S., B. M. Prüß, and P. Matsumura. 2004. Increased motility of Escherichia coli by insertion sequence element integration into the regulatory region of the flhD operon. J. Bacteriol. 186:7529-7537.
3. Bartlett, D. H., B. B. Frantz, and P. Matsumura. 1988. Flagellar transcriptional activators FlbB and FlaI: gene sequences and 5′ consensus sequences of operons under FlbB and FlaI control. J. Bacteriol. 170:1575-1581.
4. Bausch, C., M. Ramsey, and T. Conway. 2004. Transcriptional organization and regulation of the L-idonic acid pathway (GntII system) in Escherichia coli. J. Bacteriol. 186:1388-1397.
5. Blair, D. F., and H. C. Berg. 1988. Restoration of torque in defective flagellar motors. Science 242:1678-1681.
6. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
7. Brenner, D. J. 1984. Facultatively anaerobic gram-negative rods, p. 408-516. In N. R. Krieg (ed.), Bergey's manual of systematic bacteriology, vol. 1. Williams & Wilkins, Baltimore, Md.
8. 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. Natl. Acad. Sci. USA 101:7427-7432.
9. Cohen, P. S., and D. C. Laux. 1995. Bacterial adhesion to and penetration of intestinal mucus in vitro. Methods Enzymol. 253:309-315.
10. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
11. Favre-Bonte, S., T. R. Licht, C. Forestier, and K. A. Krogfelt. 1999. Klebsiella pneumoniae capsule expression is necessary for colonization of large intestines of streptomycin-treated mice. Infect. Immun. 67:6152-6156.
12. Francez-Charlot, A., B. Laugel, A. Van Gemert, N. Dubarry, F. Wiorowski, M. P. Castanie-Cornet, C. Gutierrez, and K. Cam. 2003. RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49:823-832.
13. 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 Microbiol. Ecol. 74: 229-240.
14. Freter, R. 1992. Factors affecting the microecology of the gut, p. 111-144. In R. Fuller (ed.), Probiotics: the scientific basis. Chapman & Hall, London, England.
15. Freter, R., H. Brickner, M. Botney, D. Cleven, and A. Aranki. 1983. Mechanisms that control bacterial populations in continuous-flow culture models or mouse large intestinal flora. Infect. Immun. 39:676-685.
16. Freter, R., H. Brickner, J. Fekete, M. M. Vickerman, and K. E. Carey. 1983. Survival and implantation of Escherichia coli in the intestinal tract. Infect. Immun. 39:686-703.
17. Giron, J. A. 2005. Role of flagella in mucosal colonization, p. 213-235. In J. P. Nataro, P. S. Cohen, H. L. T. Mobley, and J. N. Weiser (ed.), Colonization of mucosal surfaces. ASM Press, Washington, D.C.
18. Hentges, D. J. 1983. Role of the intestinal microflora in host defense against infection, p. 311-331. In D. J. Hentges (ed.), Human intestinal microflora in health and disease. Academic Press, Inc., New York, N.Y.
19. Hentges, D. J., J. U. Que, S. W. Casey, and A. J. Stein. 1984. The influence of streptomycin on colonization resistance in mice. Microecol. Ther. 14:53-62.
20. Kameue, C., T. Tsukahara, K. Yamada, H. Koyama, Y. Iwasaki, K. Nakayama, and K. Ushida. 2004. Dietary sodium gluconate protects rats from large bowel cancer by stimulating butyrate production. J. Nutr. 134: 940-944.
21. Ko, M., and C. Park. 2000. H-NS-dependent regulation of flagellar synthesis is mediated by a LysR family protein. J. Bacteriol. 182:4670-4672.
22. Lehnen, D., C. Blumer, T. Polen, B. Wackwitz, V. F. Wendisch, and G. Unden. 2002. LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol. Microbiol. 45:521-532.
23. Licht, T. R., T. Tolker-Nielsen, K. Holmstrøm, K. A. Krogfelt, and S. Molin. 1999. Inhibition of Escherichia coli precursor 16S rRNA processing by mouse intestinal contents. Environ. Microbiol. 1:23-32.
24. Macnab, R. M. 1996. Flagella and motility, p. 123-145. 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.
25. McCormick, B. A., D. C. Laux, and P. S. Cohen. 1990.1990. 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. 58:2957-5961.
26. McCormick, B. A., B. A. D. Stocker, D. C. Laux, and P. S. Cohen. 1988. The role of motility, chemotaxis, penetration through, and growth in intestinal mucus in the ability of an avirulent strain of Salmonella typhimurium to colonize the large intestines of streptomycin-treated mice. Infect. Immun. 56:2209-2217.
27. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
28. Miller, C. P., and M. Bohnhoff, 1963. Changes in the mouse's enteric microflora associated with enhanced susceptibility to Salmonella infection following streptomycin-treatment. J. Infect. Dis. 113:59-66.
29. 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. 72:1666-1676.
30. Møller, A. K., M. P. Leatham, T. Conway, P. J. M. Nuyten, L. A. M. 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: 2142-2152.
31. - strains. J. Bacteriol. 186:2319-2327.
32. Moore, W. E. C., and L. V. Holdeman. 1974. Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl. Microbiol. 27:961-979.
33. Nevola, J. J., D. C. Laux, and P. S. Cohen. 1987. In vivo colonization of the mouse large intestine and in vitro penetration of intestinal mucus by an avirulent strain of Salmonella typhimurium and its lipopolysaccharide-deficient mutant. Infect. Immun. 55:2884-2890.
34. Newman, J. V., R. Kolter, D. C. Laux, and P. S. Cohen. 1994. The role of leuX in Escherichia coli colonization of the streptomycin-treated mouse large intestine. Microb. Pathog. 17:301-311.
35. Peekhaus, N., and T. Conway. 1998. What's for dinner? Entner-Doudoroff metabolism in Escherichia coli. J. Bacteriol. 180:3495-3502.
36. Prüß, B. M., J. W. Campbell, T. K. Van Dyk, C. Zhu, Y. Kogan, and P. Matsumura. 2003. FlhD/FlhC is a regulator of anaerobic respiration and the Entner-Doudoroff pathway through induction of the methyl-accepting chemotaxis protein Aer. J. Bacteriol. 185:534-543.
37. Prüß, B. M., X. Liu, W. Hendrickson, and P. Matsumura. 2001. FlhD/FlhC-regulated promoters analyzed by gene array and lacZ gene fusions. FEMS Microbiol. Lett. 197:91-97,
38. Prüß, B. M., and P. Matsumura. 1996. A regulator of the flagellar regulon of Escherichia coli, flhD, also affects cell division. J. Bacteriol. 178:668-674.
39. Revel, H. R. 1966. Restriction and nonglucosylated T-even bacteriophage: properties of permissive mutants of Escherichia coli B and K12. Virology 31:688-701.
40. Schmitt, C. K. J. S. Ikeda, S. C. Darnell, P. R. Watson, J. Bispham, T. S. Wallis, D. L. Weinstein, E. S. Metcalf, and A. D. O'Brien. 2001. Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect. Immun. 69:5619-5625.
41. Shin, S., and C. Park. 1995. Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J. Bacteriol. 177: 4696-4702.
42. Stintzi, A., D. Marlow, K. Palyada, H. Naikare, R. Panciera, L. Whitworth, and C. Clarke. 2005. Use of genome-wide expression profiling and mutagenesis to study the intestinal lifestyle of Campylobacter jejuni. Infect. Immun. 73:1797-1810.
43. 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. 64:3497-3503.
44. Sweeney, N. J., D. C. Laux, and P. S. Cohen. 1996. Escherichia coli F-18 and K-12 eda mutants do not colonize the streptomycin-treated mouse large intestine. Infect. Immun. 64:3504-3511.
45. van der Waaij, D., J. M. Berghuis de Vries, and J. E. C. Lekkerkerk. 1971. Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J. Hyg. 69:405-441.
46. 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 growth in mucus. Infect. Immun. 56:1030-1035.