Enterococcus faecalis-derived adenine enhances enterohaemorrhagic Escherichia coli Type 3 Secretion System-dependent virulence

Nat Microbiol. 2024 Sep;9(9):2448-2461. doi: 10.1038/s41564-024-01747-1. Epub 2024 Jul 4.

Abstract

Interactions between microbiota and enteric pathogens can promote colonization resistance or enhance pathogenesis. The pathobiont Enterococcus faecalis increases enterohaemorrhagic E. coli (EHEC) virulence by upregulating Type 3 Secretion System (T3SS) expression, effector translocation, and attaching and effacing (AE) lesion formation on enterocytes, but the mechanisms underlying this remain unknown. Using co-infection of organoids, metabolomics, supplementation experiments and bacterial genetics, here we show that co-culture of EHEC with E. faecalis increases the xanthine-hypoxanthine pathway activity and adenine biosynthesis. Adenine or E. faecalis promoted T3SS gene expression, while transcriptomics showed upregulation of adeP expression, which encodes an adenine importer. Mechanistically, adenine relieved High hemolysin activity (Hha)-dependent repression of T3SS gene expression in EHEC and promoted AE lesion formation in an AdeP-dependent manner. Microbiota-derived purines, such as adenine, support multiple beneficial host responses; however, our data show that this metabolite also increases EHEC virulence, highlighting the complexity of pathogen-microbiota-host interactions in the gut.

MeSH terms

  • Adenine* / metabolism
  • Adenine* / pharmacology
  • Animals
  • Coculture Techniques
  • Enterococcus faecalis* / genetics
  • Enterococcus faecalis* / metabolism
  • Enterococcus faecalis* / pathogenicity
  • Enterocytes / metabolism
  • Enterocytes / microbiology
  • Enterohemorrhagic Escherichia coli* / genetics
  • Enterohemorrhagic Escherichia coli* / metabolism
  • Enterohemorrhagic Escherichia coli* / pathogenicity
  • Escherichia coli Infections / microbiology
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Gastrointestinal Microbiome
  • Gene Expression Regulation, Bacterial*
  • Hemolysin Proteins / genetics
  • Hemolysin Proteins / metabolism
  • Host-Pathogen Interactions
  • Humans
  • Hypoxanthine / metabolism
  • Mice
  • Type III Secretion Systems* / genetics
  • Type III Secretion Systems* / metabolism
  • Virulence
  • Virulence Factors / genetics
  • Virulence Factors / metabolism
  • Xanthine / metabolism

Substances

  • Type III Secretion Systems
  • Adenine
  • Escherichia coli Proteins
  • Hemolysin Proteins
  • Xanthine
  • Hypoxanthine
  • Virulence Factors