Skip to main content

Advertisement

Log in

Photodynamic inactivation of Klebsiella pneumoniae biofilms and planktonic cells by 5-aminolevulinic acid and 5-aminolevulinic acid methyl ester

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

The treatment of Klebsiella pneumoniae, particularly extended-spectrum β-lactamase (ESBL)-producing K. pneumoniae, is currently a great challenge. Photodynamic antimicrobial chemotherapy is a promising approach for killing antibiotic-resistant bacteria. The aim of this study was to evaluate the capacity of 5-aminolevulinic acid (5-ALA) and its derivative 5-ALA methyl ester (MAL) in the presence of white light to cause photodynamic inactivation (PDI) of K. pneumoniae planktonic and biofilm cells. In the presence of white light, 5-ALA and MAL inactivated planktonic cells in a concentration-dependent manner. Biofilms were also sensitive to 5-ALA and MAL-mediated PDI. The mechanisms by which 5-ALA and MAL caused PDI of ESBL-producing K. pneumonia were also investigated. Exposure of K. pneumonia to light in the presence of either 5-ALA or MAL induced cleavage of genomic DNA and the rapid release of intracellular biopolymers. Intensely denatured cytoplasmic contents and aggregated ribosomes were also detected by transmission electron microscopy. Scanning electron microscopy showed that PDI of biofilms caused aggregated bacteria to detach and that the bacterial cell envelope was damaged. This study provides insights into 5-ALA and MAL-mediated PDI of ESBL-producing K. pneumoniae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Shon AS, Bajwa RPS, Russo TA (2013) Hypervirulent Klebsiella pneumoniae: a new and dangerous breed. Virulence 4(2):107–118

    Article  PubMed  PubMed Central  Google Scholar 

  2. Pitout JDD, Laupland KB (2008) Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 8(3):159–166

    Article  CAS  PubMed  Google Scholar 

  3. Bradford PA (2001) Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 14(4):933–951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Vardakas KZ et al (2012) Carbapenems versus alternative antibiotics for the treatment of bacteraemia due to Enterobacteriaceae producing extended-spectrum β-lactamases: a systematic review and meta-analysis. J Antimicrob Chemother. doi:10.1093/jac/dks301

    PubMed  Google Scholar 

  5. Denis TGS et al (2011) All you need is light: antimicrobial photoinactivation as an evolving and emerging discovery strategy against infectious disease. Virulence 2(6):509–520

    Article  Google Scholar 

  6. Celli JP et al (2010) Imaging and photodynamic therapy: mechanisms, monitoring, and optimization. Chem Rev 110(5):2795–2838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Castano AP, Mroz P, Hamblin MR (2006) Photodynamic therapy and anti-tumor immunity. Nat Rev Cancer 6:535–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Wood S et al (2006) Erythrosine is a potential photosensitizer for the photodynamic therapy of oral plaque biofilms. J Antimicrob Chemother 57(4):680–684

    Article  CAS  PubMed  Google Scholar 

  9. Komerik N, Wilson M (2002) Factors influencing the susceptibility of gram-negative bacteria to toluidine blue O-mediated lethal photosensitization. J Appl Microbiol 92(4):618–623

    Article  CAS  PubMed  Google Scholar 

  10. Haidaris CG et al (2013) Effective photodynamic therapy against microbial populations in human deep tissue abscess aspirates. Laser Surg Med 45(8):509–516

    Google Scholar 

  11. Rossoni RD et al (2010) Comparison of the efficacy of rose bengal and erythrosine in photodynamic therapy against Enterobacteriaceae. Laser Med Sci 25(4):581–596

    Article  Google Scholar 

  12. Harris F, Pierpoint L (2012) Photodynamic therapy based on 5-aminolevulinic acid and its use as an antimicrobial agent. Med Res Rev 32(6):1292–1327

    Article  CAS  PubMed  Google Scholar 

  13. Li X et al (2013) Effects of 5-aminolevulinic acid-mediated photodynamic therapy on antibiotic-resistant staphylococcal biofilm: an in vitro study. J Surg Res 184(2):1013–1021

    Article  CAS  PubMed  Google Scholar 

  14. Fotinos N et al (2008) Effects on gram-negative and gram-positive bacteria mediated by 5-aminolevulinic acid and 5-aminolevulinic acid derivatives. Animicrob Agents Chemother 52(4):1366–1373

    Article  CAS  Google Scholar 

  15. Nitzan Y et al (2004) ALA induced photodynamic effects on gram positive and negative bacteria. Photochem Photobiol Sci 3:430–435

    Article  CAS  PubMed  Google Scholar 

  16. Yow CMN, Fung K, Wong KC (2011) Photodynamic inactivation of multi-drug resistant pathogens in Hong Kong. Hong Kong Med J 17(Suppl 2):S24–28

    Google Scholar 

  17. Peng Z et al (2011) Quaternized chitosan inhibits icaA transcription and biofilm formation by Staphylococcus on a titanium surface. Antimicrob Agents Chemother 55(2):860–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Chen CZ, Cooper SL (2002) Interactions between dendrimer biocides and bacterial membranes. Biomaterials 23(16):3359–3368

    Article  CAS  PubMed  Google Scholar 

  19. Je JY, Kim SK (2006) Antimicrobial action of novel chitin derivative. Biochim Biophys Acta 1760(1):104–109

    Article  CAS  PubMed  Google Scholar 

  20. Spesia MB et al (2009) Mechanistic insight of the photodynamic inactivation of Escherichia coli by a tetracationic zinc(II) phthalocyanine derivative. Photodiagn Photodyn Ther 6(1):52–61

    Article  CAS  Google Scholar 

  21. Spesia MB, Duraniti EN (2013) Photodynamic inactivation mechanism of Streptococcus mitis sensitized by zinc (II) 2, 9, 16, 23-tetrakis [2-(N, N, N-trimethylamino) ethoxy] phthalocyanine. J Photochem Photobiol B 125(5):179–187

    Article  CAS  PubMed  Google Scholar 

  22. Caminos DA et al (2008) Mechanisms of Escherichia coli photodynamic inactivation by an amphiphilic tricationic porphyrin and 5, 10, 15, 20-tetra (4-N, N, N-trimethylammoniumphenyl) porphyrin. Photochem Photobiol Sci 7:1071–1078

    Article  CAS  PubMed  Google Scholar 

  23. Fotinos N et al (2006) 5-Aminolevulinic acid derivatives in photomedicine: characteristics, application and perspectives. Photochem Photobiol 82(4):994–1015

    Article  CAS  PubMed  Google Scholar 

  24. Demidova T, Hamblin M (2005) Effects of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 49(6):2329–2335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sutherland IW (2001) The biofilm matrix-an immobilized but dynamic microbial environment. Trends Microbiol 9(5):222–227

    Article  CAS  PubMed  Google Scholar 

  26. Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138

    Article  CAS  PubMed  Google Scholar 

  27. Lee C et al (2004) 5-Aminolaevulinic acid mediated photodynamic antimicrobial chemotherapy on Pseudomonas aeruginosa planktonic and biofilm cultures. J Photochem Photobiol B 75(1–2):21–25

    Article  CAS  PubMed  Google Scholar 

  28. Mah TFC, Toole GAO’ (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39

    Article  CAS  PubMed  Google Scholar 

  29. Gad F et al (2004) Effects of growth phase and extracellular slime on photodynamic inactivation of gram-positive pathogenic bacteria. Antimicrob Agents Chemother 48(6):2173–2178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bertoloni G et al (2000) Photosensitizing activity of hematoporphyrin on Staphylococcus aureus cells. Biochim Biophys Acta 1475(2):169–174

    Article  CAS  PubMed  Google Scholar 

  31. Capella M, Coelho AM, Menezes S (1996) Effect of glucose on photodynamic action of methylene blue in Escherichia coli cells. Photochem Photobiol 64(1):205–210

    Article  CAS  PubMed  Google Scholar 

  32. Choi SS, Lee HK, Chae HS (2012) Comparison of in vitro photodynamic antimicrobial activity of protoporphyrin IX between endoscopic white light and newly developed narrowband endoscopic light against Helicobacter pylori 26695. J Photochem Photobiol B 117(5):55–60

    Article  CAS  PubMed  Google Scholar 

  33. Nitzan Y, Ashkenazi H (2001) Photoinactivation of Acinetobacter baumannii and Escherichia coli B by cationic hydrophilic porphyrin at various light wavelengths. Curr Microbiol 42(6):408–414

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are really grateful for assistance from Professor Kewu Yang at the College of Chemistry and Materials Science, Northwest University, China. This work was supported by the National Natural Science Foundation of China (81401710), China Postdoctoral Science Foundation (2014M562424 and 2015T81034), and the Fundamental Research Funds for the Central Universities.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sean P. Nair or Jiru Xu.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, C., Zhou, Y., Wang, L. et al. Photodynamic inactivation of Klebsiella pneumoniae biofilms and planktonic cells by 5-aminolevulinic acid and 5-aminolevulinic acid methyl ester. Lasers Med Sci 31, 557–565 (2016). https://doi.org/10.1007/s10103-016-1891-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-016-1891-1

Keywords

Navigation