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 journalArticlepeer-review

227 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

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

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