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RelA Mutant Enterococcus faecium with Multiantibiotic Tolerance Arising in an Immunocompromised Host.

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A mutation in the relA gene in vancomycin-resistant Enterococcus faecium (VRE) caused antibiotic tolerance in biofilms, hindering treatment in an immunocompromised patient. Novel ClpP-activating antibiotics successfully eradicated these resistant VRE biofilms.

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Area of Science:

  • Microbiology
  • Genetics
  • Infectious Diseases

Background:

  • Antibiotic resistance, particularly in immunocompromised patients, poses a significant clinical challenge.
  • Vancomycin-resistant Enterococcus faecium (VRE) infections can be persistent and difficult to treat.
  • Immunocompromised states may facilitate the emergence of novel bacterial resistance mechanisms.

Purpose of the Study:

  • To investigate the mechanisms of antibiotic resistance in a persistent VRE bacteremia case in an infant with leukemia.
  • To identify genetic mutations responsible for treatment failure in VRE infections.
  • To evaluate novel therapeutic strategies against antibiotic-tolerant VRE biofilms.

Main Methods:

  • Whole-genome sequencing of serial VRE isolates from a patient with persistent bacteremia.
  • Phenotypic characterization of VRE isolates, including antibiotic susceptibility testing (MICs) and biofilm growth assays.
  • Transcriptomic analysis to understand the impact of identified mutations on bacterial gene expression.
  • In vitro testing of a ClpP-activating antibiotic against VRE biofilms.

Main Results:

  • A single missense mutation (L152F) in the relA gene was identified, leading to constitutive activation of the stringent response and elevated ppGpp levels.
  • The relA mutant VRE exhibited tolerance to high doses of linezolid and daptomycin specifically within biofilms, despite susceptibility in planktonic growth.
  • The mutation caused a broad shift in gene expression, contributing to biofilm-specific antibiotic tolerance.
  • An experimental ClpP-activating antibiotic was effective in eradicating the VRE mutant from established biofilms.
  • The relA mutation was associated with reduced biofilm formation and population density, indicating a fitness trade-off.

Conclusions:

  • Clinically relevant relA mutations can emerge during prolonged VRE infections in immunocompromised hosts.
  • Activation of the stringent response via relA mutations confers antibiotic tolerance, particularly in biofilms, leading to delayed eradication.
  • Targeting biofilm-specific resistance mechanisms, such as with ClpP-activating antibiotics, offers a promising therapeutic avenue for difficult-to-treat VRE infections.