Ceragenin-mediated disruption of Pseudomonas aeruginosa biofilms

PLoS One. 2024 Feb 12;19(2):e0298112. doi: 10.1371/journal.pone.0298112. eCollection 2024.

Abstract

Background: Microbial biofilms, as a hallmark of cystic fibrosis (CF) lung disease and other chronic infections, remain a desirable target for antimicrobial therapy. These biopolymer-based viscoelastic structures protect pathogenic organisms from immune responses and antibiotics. Consequently, treatments directed at disrupting biofilms represent a promising strategy for combating biofilm-associated infections. In CF patients, the viscoelasticity of biofilms is determined mainly by their polymicrobial nature and species-specific traits, such as Pseudomonas aeruginosa filamentous (Pf) bacteriophages. Therefore, we examined the impact of microbicidal ceragenins (CSAs) supported by mucolytic agents-DNase I and poly-aspartic acid (pASP), on the viability and viscoelasticity of mono- and bispecies biofilms formed by Pf-positive and Pf-negative P. aeruginosa strains co-cultured with Staphylococcus aureus or Candida albicans.

Methods: The in vitro antimicrobial activity of ceragenins against P. aeruginosa in mono- and dual-species cultures was assessed by determining minimum inhibitory concentration (MIC) and minimum bactericidal/fungicidal concentration (MBC/MFC). Inhibition of P. aeruginosa mono- and dual-species biofilms formation by ceragenins alone and in combination with DNase I or poly-aspartic acid (pASP) was estimated by the crystal violet assay. Additionally, the viability of the biofilms was measured by colony-forming unit (CFU) counting. Finally, the biofilms' viscoelastic properties characterized by shear storage (G') and loss moduli (G"), were analyzed with a rotational rheometer.

Results: Our results demonstrated that ceragenin CSA-13 inhibits biofilm formation and increases its fluidity regardless of the Pf-profile and species composition; however, the Pf-positive biofilms are characterized by elevated viscosity and elasticity parameters.

Conclusion: Due to its microbicidal and viscoelasticity-modifying properties, CSA-13 displays therapeutic potential in biofilm-associated infections, especially when combined with mucolytic agents.

MeSH terms

  • Anti-Bacterial Agents / pharmacology
  • Anti-Infective Agents* / pharmacology
  • Aspartic Acid
  • Biofilms
  • Cystic Fibrosis*
  • Deoxyribonuclease I
  • Expectorants
  • Humans
  • Microbial Sensitivity Tests
  • Pseudomonas Infections*
  • Pseudomonas aeruginosa
  • Steroids*

Substances

  • ceragenins
  • Aspartic Acid
  • Expectorants
  • Anti-Bacterial Agents
  • Anti-Infective Agents
  • Deoxyribonuclease I
  • Steroids

Grants and funding

This work was made possible through the generous financial support from various sources. We acknowledge the grants received from the National Science Centre, Poland (UMO-2018/30/M/NZ6/00502, RB) and the Medical University of Bialystok (SUB/1/DN/22/006/1122, MZ). Additionally, part of the study utilized equipment acquired by the Medical University of Białystok under the RPOWP 2007-2013 funding, Priority I, Axis 1.1, contract No. UDA564 RPPD.01.01.00-20-001/15-00 dated 26.06.2015. We affirm that the funders played no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. We declare that there was no additional external funding received for this study.