Porphyrin-Loaded Lignin Nanoparticles Against Bacteria: A Photodynamic Antimicrobial Chemotherapy Application

Nidia Maldonado-Carmona; Guillaume Marchand; Nicolas Villandier; Tan-Sothea Ouk; Mariette M Pereira; Mário J F Calvete; Claude Alain Calliste; Andrzej Żak; Marta Piksa; Krzysztof J Pawlik; Katarzyna Matczyszyn; Stéphanie Leroy-Lhez

doi:10.3389/fmicb.2020.606185

Porphyrin-Loaded Lignin Nanoparticles Against Bacteria: A Photodynamic Antimicrobial Chemotherapy Application

Front Microbiol. 2020 Nov 17:11:606185. doi: 10.3389/fmicb.2020.606185. eCollection 2020.

Affiliations

¹ PEIRENE Laboratory, Faculty of Sciences and Techniques, University of Limoges, Limoges, France.
² Laboratory of Catalysis and Fine Chemistry, Department of Chemistry, University of Coimbra, Coimbra, Portugal.
³ PEIRENE Laboratory, Faculty of Pharmacy, University of Limoges, Limoges, France.
⁴ Electron Microscopy Laboratory, Wrocław University of Science and Technology, Wrocław, Poland.
⁵ Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, Wrocław, Poland.
⁶ Advanced Materials Engineering and Modelling Group, Faculty of Chemistry, Wrocław University of Science and Technology, Wrocław, Poland.

Abstract

The need for alternative strategies to fight bacteria is evident from the emergence of antimicrobial resistance. To that respect, photodynamic antimicrobial chemotherapy steadily rises in bacterial eradication by using light, a photosensitizer and oxygen, which generates reactive oxygen species that may kill bacteria. Herein, we report the encapsulation of 5,10,15,20-tetrakis(4-hydroxyphenyl)-21H,23H-porphyrin into acetylated lignin water-dispersible nanoparticles (THPP@AcLi), with characterization of those systems by standard spectroscopic and microscopic techniques. We observed that THPP@AcLi retained porphyrin's photophysical/photochemical properties, including singlet oxygen generation and fluorescence. Besides, the nanoparticles demonstrated enhanced stability on storage and light bleaching. THPP@AcLi were evaluated as photosensitizers against two Gram-negative bacteria, Escherichia coli and Pseudomonas aeruginosa, and against three Gram-positive bacteria, Staphylococcus aureus, Staphylococcus epidermidis, and Enterococcus faecalis. THPP@AcLi were able to diminish Gram-positive bacterial survival to 0.1% when exposed to low white LED light doses (4.16 J/cm²), requiring concentrations below 5 μM. Nevertheless, the obtained nanoparticles were unable to diminish the survival of Gram-negative bacteria. Through transmission electron microscopy observations, we could demonstrate that nanoparticles did not penetrate inside the bacterial cell, exerting their destructive effect on the bacterial wall; also, a high affinity between acetylated lignin nanoparticles and bacteria was observed, leading to bacterial flocculation. Altogether, these findings allow to establish a photodynamic antimicrobial chemotherapy alternative that can be used effectively against Gram-positive topic infections using the widely available natural polymeric lignin as a drug carrier. Further research, aimed to inhibit the growth and survival of Gram-negative bacteria, is likely to enhance the wideness of acetylated lignin nanoparticle applications.

Keywords: antimicrobial alternatives; nanoparticles; photodynamic antimicrobial therapy; tetrapyrrolic compounds; valorized lignin.