Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1996 Sep;64(9):3497–3503. doi: 10.1128/iai.64.9.3497-3503.1996

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.

N J Sweeney 1, P Klemm 1, B A McCormick 1, E Moller-Nielsen 1, M Utley 1, M A Schembri 1, D C Laux 1, P S Cohen 1
PMCID: PMC174254  PMID: 8751890

Abstract

Escherichia coli F-18 is a human fecal isolate that makes type 1 fimbriae, encoded by the fim gene cluster, and is an excellent colonizer of the streptomycin-treated mouse intestine. E. coli F-18 fimA::tet, lacking type 1 fimbriae, was constructed by bacteriophage P1 transduction of the fim region of the E. coli K-12 strain ORN151, containing the tetracycline resistance gene from Tn10 inserted in the fimA gene, into E. coli F-18. E. coli F-18 fimA::tet was found to occupy a distinct niche in the streptomycin-treated mouse intestine when fed in small numbers (10(4) CFU) to mice, along with large numbers (10(10) CFU) of E. coli F-18, as defined by the ability of the E. coli F-18 fimA::tet strain to grow and colonize only 1 order of magnitude below E. coli F-18. The same effect was observed when mice already colonized with E. coli F-18 were fed small numbers of E. coli F-18 fimA::tet. Experiments which show that the E. coli K-12 gene responsible for this effect is not fim::tet but gntP, which maps immediately downstream of the fim gene cluster, are presented. gntP encodes a high-affinity gluconate permease, suggesting that the distinct niche in the mouse large intestine is defined by the presence of gluconate. The data presented here support the idea that small numbers of an ingested microorganism can colonize the intestine as long as it can utilize an available nutrient better than any of the other resident species can.

Full Text

The Full Text of this article is available as a PDF (326.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson E. S. Viability of, and transfer of a plasmid from, E. coli K12 in human intestine. Nature. 1975 Jun 5;255(5508):502–504. doi: 10.1038/255502a0. [DOI] [PubMed] [Google Scholar]
  2. Anderson J. D., Gillespie W. A., Richmond M. H. Chemotherapy and antibiotic-resistance transfer between Enterobacteria in the human gastro-intestinal tract. J Med Microbiol. 1973 Nov;6(4):461–473. doi: 10.1099/00222615-6-4-461. [DOI] [PubMed] [Google Scholar]
  3. Apperloo-Renkema H. Z., Van der Waaij B. D., Van der Waaij D. Determination of colonization resistance of the digestive tract by biotyping of Enterobacteriaceae. Epidemiol Infect. 1990 Oct;105(2):355–361. doi: 10.1017/s0950268800047944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BOHNHOFF M., DRAKE B. L., MILLER C. P. Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc Soc Exp Biol Med. 1954 May;86(1):132–137. doi: 10.3181/00379727-86-21030. [DOI] [PubMed] [Google Scholar]
  5. BOHNHOFF M., MILLER C. P. Enhanced susceptibility to Salmonella infection in streptomycin-treated mice. J Infect Dis. 1962 Sep-Oct;111:117–127. doi: 10.1093/infdis/111.2.117. [DOI] [PubMed] [Google Scholar]
  6. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bloch C. A., Orndorff P. E. Impaired colonization by and full invasiveness of Escherichia coli K1 bearing a site-directed mutation in the type 1 pilin gene. Infect Immun. 1990 Jan;58(1):275–278. doi: 10.1128/iai.58.1.275-278.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  9. Bächi B., Kornberg H. L. Genes involved in the uptake and catabolism of gluconate by Escherichia coli. J Gen Microbiol. 1975 Oct;90(2):321–335. doi: 10.1099/00221287-90-2-321. [DOI] [PubMed] [Google Scholar]
  10. Caugant D. A., Levin B. R., Selander R. K. Genetic diversity and temporal variation in the E. coli population of a human host. Genetics. 1981 Jul;98(3):467–490. doi: 10.1093/genetics/98.3.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cohen P. S., Rossoll R., Cabelli V. J., Yang S. L., Laux D. C. 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. 1983 Apr;40(1):62–69. doi: 10.1128/iai.40.1.62-69.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Egan S. E., Fliege R., Tong S., Shibata A., Wolf R. E., Jr, Conway T. Molecular characterization of the Entner-Doudoroff pathway in Escherichia coli: sequence analysis and localization of promoters for the edd-eda operon. J Bacteriol. 1992 Jul;174(14):4638–4646. doi: 10.1128/jb.174.14.4638-4646.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. FRETER R. Experimental enteric Shigella and Vibrio infections in mice and guinea pigs. J Exp Med. 1956 Sep 1;104(3):411–418. doi: 10.1084/jem.104.3.411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. FRETER R. The fatal enteric cholera infection in the guinea pig, achieved by inhibition of normal enteric flora. J Infect Dis. 1955 Jul-Aug;97(1):57–65. doi: 10.1093/infdis/97.1.57. [DOI] [PubMed] [Google Scholar]
  15. Freter R., Brickner H., Botney M., Cleven D., Aranki A. Mechanisms that control bacterial populations in continuous-flow culture models of mouse large intestinal flora. Infect Immun. 1983 Feb;39(2):676–685. doi: 10.1128/iai.39.2.676-685.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Freter R., Brickner H., Fekete J., Vickerman M. M., Carey K. E. Survival and implantation of Escherichia coli in the intestinal tract. Infect Immun. 1983 Feb;39(2):686–703. doi: 10.1128/iai.39.2.686-703.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Herrero M., de Lorenzo V., Timmis K. N. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol. 1990 Nov;172(11):6557–6567. doi: 10.1128/jb.172.11.6557-6567.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Istúriz T., Palmero E., Vitelli-Flores J. Mutations affecting gluconate catabolism in Escherichia coli. Genetic mapping of the locus for the thermosensitive gluconokinase. J Gen Microbiol. 1986 Nov;132(11):3209–3219. doi: 10.1099/00221287-132-11-3209. [DOI] [PubMed] [Google Scholar]
  19. Klemm P., Christiansen G. Three fim genes required for the regulation of length and mediation of adhesion of Escherichia coli type 1 fimbriae. Mol Gen Genet. 1987 Jul;208(3):439–445. doi: 10.1007/BF00328136. [DOI] [PubMed] [Google Scholar]
  20. Klemm P. The fimA gene encoding the type-1 fimbrial subunit of Escherichia coli. Nucleotide sequence and primary structure of the protein. Eur J Biochem. 1984 Sep 3;143(2):395–399. doi: 10.1111/j.1432-1033.1984.tb08386.x. [DOI] [PubMed] [Google Scholar]
  21. Klemm P., Tong S., Nielsen H., Conway T. The gntP gene of Escherichia coli involved in gluconate uptake. J Bacteriol. 1996 Jan;178(1):61–67. doi: 10.1128/jb.178.1.61-67.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Marshall B., Schluederberg S., Tachibana C., Levy S. B. Survival and transfer in the human gut of poorly mobilizable (pBR322) and of transferable plasmids from the same carrier E. coli. Gene. 1981 Aug;14(3):145–154. doi: 10.1016/0378-1119(81)90110-4. [DOI] [PubMed] [Google Scholar]
  23. Maurer L., Orndorff P. E. Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili. J Bacteriol. 1987 Feb;169(2):640–645. doi: 10.1128/jb.169.2.640-645.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. McCormick B. A., Franklin D. P., Laux D. C., Cohen P. S. 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. 1989 Oct;57(10):3022–3029. doi: 10.1128/iai.57.10.3022-3029.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Moore W. E., Holdeman L. V. Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl Microbiol. 1974 May;27(5):961–979. doi: 10.1128/am.27.5.961-979.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ritzenthaler P., Mata-Gilsinger M., Stoeber F. Construction and expression of hybrid plasmids containing Escherichia coli K-12 uxu genes. J Bacteriol. 1980 Sep;143(3):1116–1126. doi: 10.1128/jb.143.3.1116-1126.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. SEARS H. J., BROWNLEE I. Further observations on the persistence of individual strains of Escherichia coli in the intestinal tract of man. J Bacteriol. 1952 Jan;63(1):47–57. doi: 10.1128/jb.63.1.47-57.1952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. SEARS H. J., BROWNLEE I., UCHIYAMA J. K. Persistence of individual strains of Escherichia coli in the intestinal tract of man. J Bacteriol. 1950 Feb;59(2):293–301. doi: 10.1128/jb.59.2.293-301.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. SEARS H. J., JANES H., SALOUM R., BROWNLEE I., LAMOREAUX L. F. Persistence of individual strains of Escherichia coli in man and dog under varying conditions. J Bacteriol. 1956 Mar;71(3):370–372. doi: 10.1128/jb.71.3.370-372.1956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Slomiany A., Yano S., Slomiany B. L., Glass G. B. Lipid composition of the gastric mucous barrier in the rat. J Biol Chem. 1978 Jun 10;253(11):3785–3791. [PubMed] [Google Scholar]
  31. Smith H. W. Survival of orally administered E. coli K 12 in alimentary tract of man. Nature. 1975 Jun 5;255(5508):500–502. doi: 10.1038/255500a0. [DOI] [PubMed] [Google Scholar]
  32. Taylor P. A., leB Williams P. J. Theoretical studies on the coexistence of competing species under continuous-flow conditions. Can J Microbiol. 1975 Jan;21(1):90–98. doi: 10.1139/m75-013. [DOI] [PubMed] [Google Scholar]
  33. Yoon H., Klinzing G., Blanch H. W. Competition for mixed substrates by microbial populations. Biotechnol Bioeng. 1977 Aug;19(8):1193–1210. doi: 10.1002/bit.260190809. [DOI] [PubMed] [Google Scholar]
  34. Zablotny R., Fraenkel D. G. Glucose and gluconate metabolism in a mutant of Escherichia coli lacking gluconate-6-phosphate dehydrase. J Bacteriol. 1967 May;93(5):1579–1581. doi: 10.1128/jb.93.5.1579-1581.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zwaig N., Nagel de Zwaig R., Istúriz T., Wecksler M. Regulatory mutations affecting the gluconate system in Escherichia coli. J Bacteriol. 1973 May;114(2):469–473. doi: 10.1128/jb.114.2.469-473.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. de Lorenzo V., Herrero M., Jakubzik U., Timmis K. N. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol. 1990 Nov;172(11):6568–6572. doi: 10.1128/jb.172.11.6568-6572.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. van der Waaij D., Berghuis-de Vries J. M., Lekkerkerk Lekkerkerk-v Colonization resistance of the digestive tract in conventional and antibiotic-treated mice. J Hyg (Lond) 1971 Sep;69(3):405–411. doi: 10.1017/s0022172400021653. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES