Gut microbiota-derived butyrate selectively interferes with growth of carbapenem-resistant Escherichia coli based on their resistance mechanism

Gut Microbes. 2024 Jan-Dec;16(1):2397058. doi: 10.1080/19490976.2024.2397058. Epub 2024 Sep 18.

Abstract

We investigated consequences of resistance acquisition in Escherichia coli clinical isolates during anaerobic (continuous culture) growth and examined their sensitivity to butyrate, a hallmark metabolite of healthy gut microbiota. Strains were stratified based on carrying either a carbapenemase (CARB) or displaying porin malfunctioning (POR). POR displayed markedly altered growth efficiencies, lower membrane stability and increased sensitivity to butyrate compared with CARB. Major differences in global gene expression between the two groups during anaerobic growth were revealed involving increased expression of alternative substrate influx routes, the stringent response and iron acquisition together with lower expression of various stress response systems in POR. Longitudinal analyses during butyrate wash-in showed common responses for all strains as well as specific features of POR that displayed strong initial "overshoot" reactions affecting various stress responses that balanced out over time. Results were partly reproduced in a mutant strain verifying porin deficiencies as the major underlying mechanism for results observed in clinical isolates. Furthermore, direct competition experiments confirmed butyrate as key for amplifying fitness disadvantages based on porin malfunctioning. Results provide new (molecular) insights into ecological consequences of resistance acquisition and can assist in developing measures to prevent colonization and infection based on the underlying resistance mechanism.

Keywords: Antibiotic resistance; Escherichia coli; anaerobic cultivation; bacterial physiology; butyrate; gene expression; gut microbiota.

MeSH terms

  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Butyrates* / metabolism
  • Butyrates* / pharmacology
  • Carbapenem-Resistant Enterobacteriaceae / drug effects
  • Carbapenem-Resistant Enterobacteriaceae / genetics
  • Carbapenems / pharmacology
  • Escherichia coli Infections / microbiology
  • Escherichia coli Proteins / genetics
  • Escherichia coli Proteins / metabolism
  • Escherichia coli* / drug effects
  • Escherichia coli* / genetics
  • Escherichia coli* / growth & development
  • Escherichia coli* / metabolism
  • Gastrointestinal Microbiome* / drug effects
  • Humans
  • Porins / genetics
  • Porins / metabolism
  • beta-Lactamases / genetics
  • beta-Lactamases / metabolism

Substances

  • Butyrates
  • Anti-Bacterial Agents
  • Porins
  • beta-Lactamases
  • Carbapenems
  • Escherichia coli Proteins
  • carbapenemase
  • Bacterial Proteins

Grants and funding

This work was funded by DZIF [TTU_06_910 and I_07.003] and the DFG [project #456214861]. Marius Vital was additionally funded by HiChol [01GM2204].