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Volume 169, Issue 7

Decolonizing drug-resistant with phage and probiotics: breaking the frequency-dependent dominance of residents Open Access

Abstract

Widespread antibiotic resistance in commensal bacteria creates a persistent challenge for human health. Resident drug-resistant microbes can prevent clinical interventions, colonize wounds post-surgery, pass resistance traits to pathogens or move to more harmful niches following routine interventions such as catheterization. Accelerating the removal of resistant bacteria or actively decolonizing particular lineages from hosts could therefore have a number of long-term benefits. However, removing resident bacteria via competition with probiotics, for example, poses a number of ecological challenges. Resident microbes are likely to have physiological and numerical advantages and competition based on bacteriocins or other secreted antagonists is expected to give advantages to the dominant partner, via positive frequency dependence. Since a narrow range of genotypes (primarily those belonging to the clonal group ST131) cause a significant proportion of multidrug-resistant infections, this group presents a promising target for decolonization with bacteriophage, as narrow-host-range viral predation could lead to selective removal of particular genotypes. In this study we tested how a combination of an ST131-specific phage and competition from the well-known probiotic Nissle strain could displace ST131 under aerobic and anaerobic growth conditions . We showed that the addition of phage was able to break the frequency-dependent advantage of a numerically dominant ST131 isolate. Moreover, the addition of competing Nissle could improve the ability of phage to suppress ST131 by two orders of magnitude. Low-cost phage resistance evolved readily in these experiments and was not inhibited by the presence of a probiotic competitor. Nevertheless, combinations of phage and probiotic produced stable long-term suppression of ST131 over multiple transfers and under both aerobic and anaerobic growth conditions. Combinations of phage and probiotic therefore have real potential for accelerating the removal of drug-resistant commensal targets.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AMR , antagonistic competition , drug resistance , frequency dependence , phage therapy and resistance management
Funding
This study was supported by the:
  • Lister Institute of Preventive Medicine
    • Principle Award Recipient: Stinekevan Houte
  • Biotechnology and Biological Sciences Research Council (Award BB/R010781/1)
    • Principle Award Recipient: Stinekevan Houte
  • Biotechnology and Biological Sciences Research Council (Award BB/S017674/1)
    • Principle Award Recipient: Stinekevan Houte
  • Medical Research Council (Award MR/N013824/1)
    • Principle Award Recipient: BenRaymond
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2024-05-15
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Decolonizing drug-resistant E. coli with phage and probiotics: breaking the frequency-dependent dominance of residents
Microbiology 169, 001352 (2023); https://doi.org/10.1099/mic.0.001352
/content/journal/micro/10.1099/mic.0.001352
/content/journal/micro/10.1099/mic.0.001352
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