Synergistic Antibacterial Interaction of Geraniol and Biogenic Silver Nanoparticles on Methicillin-Resistant Staphylococcus aureus

Author:

Castro Isabela Madeira de12ORCID,Antunes Camila2ORCID,Valentim Camila Cristina2,Spoladori Laís Fernanda de Almeida12ORCID,Suzukawa Helena Tiemi12ORCID,Correia Guilherme Ferreira12ORCID,Silva-Rodrigues Gislaine12ORCID,Borges Paulo Henrique Guilherme12ORCID,Bartolomeu-Gonçalves Guilherme23ORCID,Silva Mariana Luiza4ORCID,Bispo Marcelle de Lima Ferreira4ORCID,Machado Rayanne Regina Beltrame5ORCID,Nakamura Celso Vataru15ORCID,Nakazato Gerson1ORCID,Pinge-Filho Phileno16ORCID,Tavares Eliandro Reis127ORCID,Yamauchi Lucy Megumi12ORCID,Yamada-Ogatta Sueli Fumie123ORCID

Affiliation:

1. Programa de Pós-graduação em Microbiologia, Universidade Estadual de Londrina, Londrina 86055-900, Paraná, Brazil

2. Laboratório de Biologia Molecular de Microrganismos, Universidade Estadual de Londrina, Londrina 86055-900, Paraná, Brazil

3. Programa de Pós-graduação em Fisiopatologia Clínica e Laboratorial, Universidade Estadual de Londrina, Londrina 86038-350, Paraná, Brazil

4. Laboratório de Síntese de Moléculas Medicinais, Departamento de Química, Centro de Ciências Exatas e da Terra, Universidade Estadual de Londrina, Londrina 86055-900, Paraná, Brazil

5. Laboratório de Inovação Tecnológica no Desenvolvimento de Fármacos e Cosméticos, Universidade Estadual de Maringá, Maringá 87020-900, Paraná, Brazil

6. Laboratório de Imunopatologia Experimental, Departmento of Imunologia, Parasitologia e Patologia Geral, Universidade Estadual de Londrina, Londrina 86055-900, Paraná, Brazil

7. Departamento de Medicina, Pontifícia Universidade Católica do Paraná, Londrina 86067-000, Paraná, Brazil

Abstract

Since ancient times, plants have been used in folk medicine to treat different diseases. Plants offer exceptional chemical diversity with a wide range of biological activities, and have therefore been the most promising sources for the discovery and development of drugs, including antimicrobial agents. This study reports the antibacterial effect of geraniol (GER), alone and in combination with biogenic silver nanoparticles (bioAgNPs), produced using the aqueous extract of Trichilia catigua bark, against planktonic and sessile cells of methicillin-resistant Staphylococcus aureus (MRSA), one of the main opportunistic and potentially fatal human pathogens. GER had a time-dependent bactericidal effect on planktonic cells, impairing the cell membrane integrity. In addition, GER inhibited the staphyloxanthin production, and molecular docking analyses supported the in silico affinity of GER to dehydrosqualene synthase (CrtM) and 4,4′-diaponeurosporen-aldehyde dehydrogenase (AldH), which are key enzymes within the pigment biosynthesis pathway in S. aureus. GER treatment increased the sensitivity of MRSA to hydrogen peroxide killing. GER displayed synergism with bioAgNPs against planktonic and sessile cells, inhibiting bacterial adhesion and the viability of biofilms formed on abiotic surfaces. MRSA planktonic and sessile cells treated with GER or GER/bioAgNPs displayed severe morphological and ultrastructural alterations. Notably, neither GER nor its combination caused in vitro and in vivo toxicity in mammalian cells and Galleria mellonella larvae, respectively. These findings suggest that the combination of GER/bioAgNPs may be a promising strategy to control MRSA infections.

Funder

Financiadora de Estudos e Projetos (FINEP) - MCTI

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Fundação Araucária - PR

Publisher

MDPI AG

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