Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae

Bärbel Stecher, Rémy Denzler, Lisa Maier, Florian Bernet, Mandy J Sanders, Derek J Pickard, Manja Barthel, Astrid M Westendorf, Karen A Krogfelt, Alan W Walker, Martin Ackermann, Ulrich Dobrindt, Nicholas R Thomson, Wolf-Dietrich Hardt

Research output: Contribution to journalArticle

171 Citations (Scopus)

Abstract

The mammalian gut harbors a dense microbial community interacting in multiple ways, including horizontal gene transfer (HGT). Pangenome analyses established particularly high levels of genetic flux between Gram-negative Enterobacteriaceae. However, the mechanisms fostering intraenterobacterial HGT are incompletely understood. Using a mouse colitis model, we found that Salmonella-inflicted enteropathy elicits parallel blooms of the pathogen and of resident commensal Escherichia coli. These blooms boosted conjugative HGT of the colicin-plasmid p2 from Salmonella enterica serovar Typhimurium to E. coli. Transconjugation efficiencies of ~100% in vivo were attributable to high intrinsic p2-transfer rates. Plasmid-encoded fitness benefits contributed little. Under normal conditions, HGT was blocked by the commensal microbiota inhibiting contact-dependent conjugation between Enterobacteriaceae. Our data show that pathogen-driven inflammatory responses in the gut can generate transient enterobacterial blooms in which conjugative transfer occurs at unprecedented rates. These blooms may favor reassortment of plasmid-encoded genes between pathogens and commensals fostering the spread of fitness-, virulence-, and antibiotic-resistance determinants.
Original languageEnglish
Pages (from-to)1269-1274
Number of pages6
JournalPNAS
Volume109
Issue number4
DOIs
Publication statusPublished - 24 Jan 2012

Fingerprint

Horizontal Gene Transfer
Enterobacteriaceae
Inflammation
Foster Home Care
Bacteriocin Plasmids
Plasmids
Escherichia coli
Salmonella enterica
Microbiota
Colitis
Microbial Drug Resistance
Salmonella
Virulence
Genes

Keywords

  • animals
  • bacteriocin plasmids
  • base sequence
  • biological evolution
  • colitis
  • computational biology
  • DNA primers
  • enterobacteriaceae
  • Escherichia coli
  • gene transfer, horizontal
  • mice
  • molecular sequence data
  • oligonucleotide array sequence analysis
  • phylogeny
  • RNA, ribosomal, 16S
  • Salmonella typhimurium
  • sequence alignment
  • sequence analysis, DNA

Cite this

Stecher, B., Denzler, R., Maier, L., Bernet, F., Sanders, M. J., Pickard, D. J., ... Hardt, W-D. (2012). Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. PNAS, 109(4), 1269-1274. https://doi.org/10.1073/pnas.1113246109

Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. / Stecher, Bärbel; Denzler, Rémy; Maier, Lisa; Bernet, Florian; Sanders, Mandy J; Pickard, Derek J; Barthel, Manja; Westendorf, Astrid M; Krogfelt, Karen A; Walker, Alan W; Ackermann, Martin; Dobrindt, Ulrich; Thomson, Nicholas R; Hardt, Wolf-Dietrich.

In: PNAS, Vol. 109, No. 4, 24.01.2012, p. 1269-1274.

Research output: Contribution to journalArticle

Stecher, B, Denzler, R, Maier, L, Bernet, F, Sanders, MJ, Pickard, DJ, Barthel, M, Westendorf, AM, Krogfelt, KA, Walker, AW, Ackermann, M, Dobrindt, U, Thomson, NR & Hardt, W-D 2012, 'Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae', PNAS, vol. 109, no. 4, pp. 1269-1274. https://doi.org/10.1073/pnas.1113246109
Stecher B, Denzler R, Maier L, Bernet F, Sanders MJ, Pickard DJ et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. PNAS. 2012 Jan 24;109(4):1269-1274. https://doi.org/10.1073/pnas.1113246109
Stecher, Bärbel ; Denzler, Rémy ; Maier, Lisa ; Bernet, Florian ; Sanders, Mandy J ; Pickard, Derek J ; Barthel, Manja ; Westendorf, Astrid M ; Krogfelt, Karen A ; Walker, Alan W ; Ackermann, Martin ; Dobrindt, Ulrich ; Thomson, Nicholas R ; Hardt, Wolf-Dietrich. / Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. In: PNAS. 2012 ; Vol. 109, No. 4. pp. 1269-1274.
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