An escherichia coli nissle 1917 missense mutant colonizes the streptomycin-treated mouse intestine better than the wild type but is not a better probiotic

Jimmy Adediran, Mary P. Leatham-Jensen, Matthew E. Mokszycki, Jakob Frimodt-Møller, Karen A. Krogfelt, Krystyna Kazmierczak, Linda Kenney, Tyrrell Conway, Paul S. Cohena

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

Previously we reported that the streptomycin-treated mouse intestine selected for two different Escherichia coli MG1655 mutants with improved colonizing ability: nonmotile E. coli MG1655 flhDC deletion mutants that grew 15% faster in vitro in mouse cecal mucus and motile E. coli MG1655 envZ missense mutants that grew slower in vitro in mouse cecal mucus yet were able to cocolonize with the faster-growing flhDC mutants. The E. coli MG1655 envZ gene encodes a histidine kinase that is a member of the envZ-ompR two-component signal transduction system, which regulates outer membrane protein profiles. In the present investigation, the envZP41L gene was transferred from the intestinally selected E. coli MG1655 mutant to E. coli Nissle 1917, a human probiotic strain used to treat gastrointestinal infections. Both the E. coli MG1655 and E. coli Nissle 1917 strains containing envZP41L produced more phosphorylated OmpR than their parents. The E. coli Nissle 1917 strain containing envZP41L also became more resistant to bile salts and colicin V and grew 50% slower in vitro in mucus and 15% to 30% slower on several sugars present in mucus, yet it was a 10-fold better colonizer than E. coli Nissle 1917. However, E. coli Nissle 1917 envZP41L was not better at preventing colonization by enterohemorrhagic E. coli EDL933. The data can be explained according to our "restaurant" hypothesis for commensal E. coli strains, i.e., that they colonize the intestine as sessile members of mixed biofilms, obtaining the sugars they need for growth locally, but compete for sugars with invading E. coli pathogens planktonically

Original languageEnglish (US)
Pages (from-to)670-682
Number of pages13
JournalInfection and immunity
Volume82
Issue number2
DOIs
StatePublished - Feb 1 2014
Externally publishedYes

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Probiotics
Streptomycin
Intestines
Escherichia coli
Mucus
Colicins
Enterohemorrhagic Escherichia coli
Restaurants
Biofilms
Bile Acids and Salts
Genes
Signal Transduction
Membrane Proteins

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

Adediran, J., Leatham-Jensen, M. P., Mokszycki, M. E., Frimodt-Møller, J., Krogfelt, K. A., Kazmierczak, K., ... Cohena, P. S. (2014). An escherichia coli nissle 1917 missense mutant colonizes the streptomycin-treated mouse intestine better than the wild type but is not a better probiotic. Infection and immunity, 82(2), 670-682. https://doi.org/10.1128/IAI.01149-13

An escherichia coli nissle 1917 missense mutant colonizes the streptomycin-treated mouse intestine better than the wild type but is not a better probiotic. / Adediran, Jimmy; Leatham-Jensen, Mary P.; Mokszycki, Matthew E.; Frimodt-Møller, Jakob; Krogfelt, Karen A.; Kazmierczak, Krystyna; Kenney, Linda; Conway, Tyrrell; Cohena, Paul S.

In: Infection and immunity, Vol. 82, No. 2, 01.02.2014, p. 670-682.

Research output: Contribution to journalArticle

Adediran, J, Leatham-Jensen, MP, Mokszycki, ME, Frimodt-Møller, J, Krogfelt, KA, Kazmierczak, K, Kenney, L, Conway, T & Cohena, PS 2014, 'An escherichia coli nissle 1917 missense mutant colonizes the streptomycin-treated mouse intestine better than the wild type but is not a better probiotic', Infection and immunity, vol. 82, no. 2, pp. 670-682. https://doi.org/10.1128/IAI.01149-13
Adediran, Jimmy ; Leatham-Jensen, Mary P. ; Mokszycki, Matthew E. ; Frimodt-Møller, Jakob ; Krogfelt, Karen A. ; Kazmierczak, Krystyna ; Kenney, Linda ; Conway, Tyrrell ; Cohena, Paul S. / An escherichia coli nissle 1917 missense mutant colonizes the streptomycin-treated mouse intestine better than the wild type but is not a better probiotic. In: Infection and immunity. 2014 ; Vol. 82, No. 2. pp. 670-682.
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abstract = "Previously we reported that the streptomycin-treated mouse intestine selected for two different Escherichia coli MG1655 mutants with improved colonizing ability: nonmotile E. coli MG1655 flhDC deletion mutants that grew 15{\%} faster in vitro in mouse cecal mucus and motile E. coli MG1655 envZ missense mutants that grew slower in vitro in mouse cecal mucus yet were able to cocolonize with the faster-growing flhDC mutants. The E. coli MG1655 envZ gene encodes a histidine kinase that is a member of the envZ-ompR two-component signal transduction system, which regulates outer membrane protein profiles. In the present investigation, the envZP41L gene was transferred from the intestinally selected E. coli MG1655 mutant to E. coli Nissle 1917, a human probiotic strain used to treat gastrointestinal infections. Both the E. coli MG1655 and E. coli Nissle 1917 strains containing envZP41L produced more phosphorylated OmpR than their parents. The E. coli Nissle 1917 strain containing envZP41L also became more resistant to bile salts and colicin V and grew 50{\%} slower in vitro in mucus and 15{\%} to 30{\%} slower on several sugars present in mucus, yet it was a 10-fold better colonizer than E. coli Nissle 1917. However, E. coli Nissle 1917 envZP41L was not better at preventing colonization by enterohemorrhagic E. coli EDL933. The data can be explained according to our {"}restaurant{"} hypothesis for commensal E. coli strains, i.e., that they colonize the intestine as sessile members of mixed biofilms, obtaining the sugars they need for growth locally, but compete for sugars with invading E. coli pathogens planktonically",
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