Bioactivity of gallic acid–conjugated silica nanoparticles against Paenibacillus larvae and their host, Apis mellifera honeybee

Apidologie - Tập 50 - Trang 616-631 - 2019
Enzo Domínguez1,2, María P. Moliné1,2,3, María S. Churio3,2, Valeria B. Arce4,2, Daniel O. Mártire5,2, Sara N. Mendiara6, Brenda S. Álvarez1,2, Liesel B. Gende1,2, Natalia Damiani1,2
1Centro de Investigación en Abejas Sociales (CIAS), Instituto de Investigaciones en Producción Sanidad y Ambiente (IIPROSAM), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Comisión de Investigaciones Científicas de la provincia de Buenos Aires (CIC), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata, Buenos Aires, Argentina
2Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), CABA, Argentina
3Departamento de Química, Facultad de Ciencias Exactas y Naturales (FCEyN). Instituto de Investigaciones Físicas de Mar del Plata (IFIMAR), CONICET, Universidad Nacional de Mar del Plata, Mar del Plata, Buenos Aires, Argentina
4Centro de Investigaciones Ópticas (CIOp), CONICET - CIC - Universidad Nacional de La Plata (UNLP), Manuel B. Gonnet, Buenos Aires, Argentina
5Instituto de Investigaciones Fisicoquímicas Teóricas y Aplicadas (INIFTA), CONICET, Universidad Nacional de La Plata (UNLP), La Plata, Buenos Aires, Argentina
6Departamento de Química, Facultad de Ciencias Exactas y Naturales (FCEyN), Universidad Nacional de Mar del Plata (UNMdP), Mar del Plata, Buenos Aires, Argentina

Tóm tắt

The aim of this work was to evaluate antimicrobial activity against Paenibacillus larvae and oral toxicity against workers and larvae of Apis mellifera of gallic acid (GA) and two nanohybrids of GA and silica. Also, the physicochemical, structural, and energetic properties of GA and the nanohybrids were determined through structure–activity relationship (SAR). The minimum inhibitory concentration (MIC) against P. larvae was determined. GA showed MIC values between 62.5 and 125 μg/ml, whereas the nanoparticle functionalized through the GA carboxylic moiety (NP2) showed the best antimicrobial activity with a MIC value of 23 μg GA/ml for four of the five isolates used. SAR analysis showed that electronegativity, chemical hardness, and dipolar moment are reliable estimators of the antimicrobial activity. NP2 showed the lowest toxicity against workers and was innocuous for bee larvae. Therefore, the nanohybrid NP2 was the best antibacterial and resulted in non-toxic against workers and larvae of honeybees, becoming a potentially effective and safe agent for the treatment of American Foulbrood disease.

Tài liệu tham khảo

Ahmad, I., Farrukh, A., Mohammad, O. (2006) Modern Phytomedicine, Turning Medicinal Plants Into Drugs. John Wiley & Sons, Weinheim Akagawa, M., Shigemitsu, T., Suyama, K. (2003) Production of hydrogen peroxide by polyphenols and polyphenol-rich beverages under quasi-physiological conditions. Biosci. Biotechnol. Biochem. 67 (12), 2632–2640 Al-Sehemi, A.G., Irfan, A., Alrumman, S.A., Hesham A.E. (2016) Antibacterial activities, DFT and QSAR studies of quinazolinone compounds. Bull. Chem. Soc. Ethiop. 30 (2), 307–316 Antunez, K., Harriet, J., Gende, L.B., Maggi, M., Eguaras, M., Zunino, P. (2008) Efficacy of natural propolis extract in the control of American Foulbrood. Vet. Microbiol. 131 (3–4), 324–331 Arakawa, H., Maeda, M., Okubo, S., Shimamura, T. (2004) Role of hydrogen peroxide in bactericidal action of catechin. Biol. Pharm. Bull. 27 (3), 277–281 Arce, V.B. (2010) Modificación y caracterización de nanopartículas de sílice. Doctoral thesis. Facultad de Ciencias Exactas, Universidad Nacional de la Plata, Argentina Arce, V.B., Bertolotti, S.G., Oliveira, F.J., Airoldi, C., Arques, A., Santos-Juanes, L., Gonzalez, MC., Cobos, C.J., Allegretti, P.E., Mártire, D.O. (2012) Triplet state of 4-methoxybenzyl alcohol chemisorbed on silica nanoparticles. Photochem. Photobiol. Sci. 11 (6), 1032–1040 Aupinel, P., Fortini, D., Dufour, H., Tasei, J.N., Michaud, B., Odoux, J.F., Delegue, M.H.P. (2005) Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. B. Insectol. 58 (2), 107–111 Ben Arfa, A., Combes, S., Preziosi-Belloy, L., Gontard, N., Chalier, P. (2006) Antimicrobial activity of carvacrol related to its chemical structure. Lett. Appl. Microbiol. 43 (2), 149–154 Bogdanov, S. (2006) Contaminants of bee products. Apidologie 37 (1), 1–18. Borges, A., Ferreira, C., Saavedra, M.J., Simões, M. (2013) Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb. Drug Resist. 19 (4), 256–265. Bravo, L. (1998) Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance. Nutr. Rev. 56 (11), 317–333 Carrión, S.M. (2013) Estudio Teórico de las Propiedades Estructurales, Electrónicas, y de la Reactividad. Doctoral thesis. Facultad de Ciencias Exactas– Universidad Nacional de La Plata. La Plata. Chang, H.J., Kim, H.J., Chun, H.S. (2007) Quantitative structure–activity relationship (QSAR) for neuroprotective activity of terpenoids. Life Sci. 80 (9), 835–841. Chanwitheesuk, A., Teerawutgulrag, A., Kilburn, J.D., Rakariyatham, N. (2007) Antimicrobial gallic acid from Caesalpinia mimosoides Lamk. Food Chem. 100 (3), 1044–1048 Cho, Y.S., Kim, S.K., Ahn, C.B., Je, J.Y. (2011) Preparation, characterization, and antioxidant properties of gallic acid-grafted-chitosans. Carbohydr. Polym. 83 (4), 1617–1622 CLSI. (2018) Methods for dilution antimicrobial susceptibility test for bacteria that grow aerobically. 11th ed. CLSI standard M07. Wayne, PA: Clinical and Laboratory Standards Institute Damiani, N., Fernández, N.J., Porrini, M.P., Gende, L.B., Álvarez, E., Buffa, F., Brasesco, C., Maggi, M.D., Marcangeli, J.A., Eguaras, M.J. (2014) Laurel leaf extracts for honeybee pest and disease management: antimicrobial, microsporicidal, and acaricidal activity. Parasitol. Res. 113 (2), 701–709 Damiani, N., Porrini, M.P., Lancia, J.P., Álvarez, E., Garrido, P.M., Domínguez, E., Gende, L.B., Eguaras, M.J. (2017) Effect of propolis oral intake on physiological condition of young worker honey bees, Apis mellifera L. J. Apicult. Sci. 61 (2), 193–202 de Almeida Vaucher, R., Giongo, J.L., Bolzan, L.P., Côrrea, M.S., Fausto, V.P., et al. (2015) Antimicrobial activity of nanostructured Amazonian oils against Paenibacillus species and their toxicity on larvae and adult worker bees. J. Asia Pac. Entomol. 18 (2), 205–210 Deligiannakis, Y., Sotiriou, G.A., Pratsinis, S.E. (2012) Antioxidant and antiradical SiO2 nanoparticles covalently functionalized with gallic acid. ACS Appl. Mater. Interfaces 4 (12), 6609–6617 Djukic, M., Brzuszkiewicz, E., Fünfhaus, A., Voss, J., Gollnow, K., Poppinga, L., Liesegang, H., Garcia-Gonzalez, E., Genersch, E., Daniel, R. (2014) How to kill the honey bee larva: Genomic potential and virulence mechanisms of Paenibacillus larvae. PLoS ONE 9 (3), e90914 Duffy, L.L., Osmond-McLeod, M.J., Judy, J., King, T. (2018) Investigation into the antibacterial activity of silver, zinc oxide and copper oxide nanoparticles against poultry-relevant isolates of Salmonella and Campylobacter. Food Control 92, 293–300. Ebert, T., Kevan, P., Bishop, B., Kevan, S., Downer, R., (2007) Oral toxicity of essential oils and organic acids fed to honey bees (Apis mellifera). J. Apicult. Res. Bee World 46 (4), 220–224 Eguaras, M., Ruffinengo, S. (2006) Estrategia para el control de Varroa. Ed. Martin, Mar del Plata Ensuncho, A.E., Robles, J.R., Figueredo, S.F. (2017) Modelado de las relaciones cuantitativas estructura-actividad (QSAR) de los derivados 5-(Nitroheteroaril)-1,3,4-tiadiazol con actividad leishmanicida. Inf. Tecnol. 28 (2), 191–202 Eslami, A., Pasanphan, W., Wagner, B., Buettner, G., (2010) Free radicals produced by the oxidation of gallic acid: An electron paramagnetic resonance study. Chem. Cent. J. 4 (1), 15 Evans, J.D. (2003) Diverse origins of tetracycline resistance in the honey bee bacterial pathogen Paenibacillus larvae. J. Invertebr. Pathol. 83 (1), 46–50 Fernández, N.J., Porrini, M.P., Podaza, E.A., Damiani, N., Liesel, B.G., Eguaras, M.J. (2014) A scientific note on the first report of honeybee venom inhibiting Paenibacillus larvae growth. Apidologie 45 (6), 719–721 Geerlings, P., De Proft, F., Langenaeker, W. (2003) Conceptual density functional theory. Chem. Rev. 103 (5), 1793–1874 Gende, L.B., Floris, I., Fritz, R., Eguaras, M.J. (2008) Antimicrobial activity of cinnamon (Cinnamomum zeylanicum) essential oil and its main components against Paenibacillus larvae from Argentine. B. Insectol. 61 (1), 1–4 Gende, L.B., Maggi, M., Damiani, N., Fritz, R., Eguaras, M.J., Floris, I. (2009) Advances in the apiary control of the honeybee American Foulbrood with Cinnamon (Cinnamomum zeylanicum) essential oil. B. insectol. 62 (1), 93–97 Gende, L.B., Maggi, M., Van Baren, C., Di Leo, A., Bandoni, A., Fritz, R., Eguaras, M.J. (2010) Antimicrobial and miticide activities of Eucalyptus globulus essential oils obtained from different Argentine regions. Span. J. Agric. Res. 8 (3), 642–650 Genersch, E. (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl. Microbiol. Biotechnol. 87 (1), 87–97 Giannakopoulos, E., Stathi, P., Dimos, K., Gournis, D., Sanakis, Y., Deligiannakis, Y. (2006) Adsorption and radical stabilization of humic-acid analogues and Pb 2+ on restricted phyllomorphous clay. Langmuir. 22 (16), 6863–6873 Hetrick, E.M., Shin, J.H., Stasko, N.A., Johnson, C.B., Wespe, D.A., Holmuhamedov, E., Schoenfisch, M.H. (2008) Bactericidal efficacy of nitric oxide-releasing silica nanoparticles. ACS Nano 2 (2), 235–246 Hinde, R.J. (2000) Quantum Chemistry, Fifth Edition (by I.N. Levine). J. Chem. Educ. 77 (12), 1564 Hu, H., Nie, L., Feng, S., Suo, J. (2013) Preparation, characterization and in vitro release study of gallic acid loaded silica nanoparticles for controlled release. Pharmazie. 68 (6), 401–405 Jin, Y., Li, A., Hazelton, S.G., Liang, S., John, C.L., Selid, P.D., Pierce, D.T., Zhao, J.X. (2009) Amorphous silica nanohybrids: Synthesis, properties and applications. Coord. Chem. Rev. 253 (23–24), 2998–3014 Kaplan, E.L., Meier, P. (1958) Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc. 53 (282), 457–481 Khan, S.U., Anjum, S.I., Ansari, M.J., Khan, M.H.U., Kamal, S., et al. (2018) Antimicrobial potentials of medicinal plant’s extract and their derived silver nanoparticles: A focus on honey bee pathogen. Saudi J. Biol. Sci., doi: https://doi.org/10.1016/j.sjbs.2018.02.01 Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kremen, C., Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proc. Biol. Sci. 274 (1608), 303–313 Kurita, N., Miyaji, M., Kurane, R., Takahara, Y. (1981) Antifungal activity of components of essential oils. Agric. Biol. Chem. 45 (4), 945–952 Lindberg, C.M., Melathopoulos, A.P., Winston, M.L. (2000) Laboratory evaluation of miticides to control Varroa jacobsoni (Acari: Varroidae), a honey bee (Hymenoptera: Apidae) parasite. J. Econ. Entomol. 93 (2), 189–198 Locatelli, C., Filippin-Monteiro, F.B., Creczynski-Pasa T.B. (2013) Alkyl esters of gallic acid as anticancer agents: A review. Eur. J. Med. Chem. 60, 233–239 Maggi, M.D., Ruffinengo, S.R., Gende, L.B., Sarlo, E.G., Eguaras, M.J, Bailac, P.N., Ponzi, M.I. (2010) Laboratory evaluations of Syzygium aromaticum (L.) Merr. et Perry essential oil against Varroa destructor. J. Essen. Oil Res. 22 (2), 119–122 Maistrello, L., Lodesani, M., Costa, C., Leonardi, F., Marani, G., Caldon, M., Mutinelli, F., Granato, A. (2008) Screening of natural compounds for the control of nosema disease in honeybees (Apis mellifera). Apidologie 39 (4), 436–445 Marino, T., Galano, A., Russo, N. (2014) Radical scavenging ability of gallic acid toward OH and OOH radicals. Reaction mechanism and rate constants from the density functional theory. J. Phys. Chem. B. 118 (35), 10380–10389 Martel, A.C., Zeggane, S., Aurières, C., Drajnudel, P., Faucon, J.P., Aubert, M. (2007) Acaricide residues in honey and wax after treatment of honey bee colonies with Apivar® or Asuntol® 50. Apidologie 38 (6), 534–544 Martínez, J., Simon, V., Gonzalez, B., Conget, P. (2010) A real-time PCR-based strategy for the detection of Paenibacillus larvae vegetative cells and spores to improve the diagnosis and the screening of American foulbrood. Lett. Appl. Microbiol. 50 (6), 603–610 Martínez-Castañon, G.A., Niño-Martínez, N., Martínez-Gutiérrez, F., Martínez-Mendoza, J.R., Ruíz, F. (2008) Synthesis and antibacterial activity of silver nanoparticles with different sizes. J. Nanoparticle Res. 10 (8), 1343–1348 Mohanraj, V.J., Chen, Y. (2006) Nanoparticles - A review. Trop. J. Pharm. Res. 5 (1), 561–573 Moreno-Álvarez, S.A., Martínez-Castañón, G.A., Niño-Martínez, N., Reyes-Macías, J. F., Patiño-Marín, N., Loyola-Rodríguez, J.P., Ruiz, F. (2010) Preparation and bactericide activity of gallic acid stabilized gold nanoparticles. J. Nanoparticle Res. 12 (8), 2741–2746 Nakamura, K., Yamada, Y., Ikai, H., Kanno, T., Sasaki K., Niwano, Y. (2012) Bactericidal action of photoirradiated gallic acid via reactive oxygen species formation. J. Agric. Food Chem. 60 (40), 10048–10054 Panagiota, S., Louloudi, M., Deligiannakis, Y. (2009) EPR study of phenolic radical stabilization by grafting on SiO2. Chem. Phys. Lett. 472 (1–3), 85–89 Pearson, R.G. (1986) Absolute electronegativity and hardness correlated with molecular orbital theory. Proc. Natl. Acad. Sci. U.S.A. 83 (22), 8440–8441 Porrini, M.P., Garrido, P.M., Gende, L.B., Rossini, C., Hermida, L., Marcángeli, J.A., Eguaras, M.J. (2017) Oral administration of essential oils and main components: Study on honey bee survival and Nosema ceranae development. J. Apicult. Res. 56 (5), 616–624 Pyrzynska, K., Biesaga, M. (2009) Analysis of phenolic acids and flavonoids in honey. Trends Analyt. Chem. 28 (7), 893–902 Sánchez-Maldonado, A.F., Schieber, A., Gänzle, M.G. (2011) Structure-function relationships of the antibacterial activity of phenolic acids and their metabolism by lactic acid bacteria: Antibacterial phenolic acids. J. Appl. Microbiol. 111 (5), 1176–1184 SENASA (2016) http://www.senasa.gob.ar/senasa-comunica/noticias/se-recuerda-que-no-esta-permitido-el-uso-de-antibioticos-en-las-colmenas Shimanuki, H. (1997) Bacteria. In: Flottum, K. (Ed.) Honey Bee Pests, Predators, and Disease, third ed. pp. 33–54, Medina, Ohio Shukla, Y.N., Srivastava, A., Kumar, S., Kumar, S. (1999) Phytotoxic and antimicrobial constituents of Argyreia speciosa and Oenothera biennis. J. Ethnopharmacol. 67 (2), 241–245 Taguri, T., Tanaka, T., Kouno, I. (2006) Antibacterial spectrum of plant polyphenols and extracts depending upon hydroxyphenyl structure. Biol. Pharm. Bull. 29 (11), 2226–2235 Versalovic, J., Schneider, M., De Bruijn, F.J., Lupski, J.R. (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods Mol. Cell. Biol. 5 (1), 25–40 Vianna Santos, R.C., Lopes, L.Q.S, dos Santos Alves, C.F., Fausto, V.P., Pizzutti, K., et al. (2014) Antimicrobial activity of tea tree oil nanoparticles against American and European foulbrood diseases agents. J. Asia Pac. Entomol. 17 (3), 343–347 Vico, T.A., Arce, V.B., Fangio, M.F., Gende, L.B., Bertran, C.A., Mártire, D.O., Churio, M.S. (2016) Two choices for the functionalization of silica nanoparticles with gallic acid: characterization of the nanomaterials and their antimicrobial activity against Paenibacillus larvae. J. Nanopart. Res. 18 (11), 348–360 Yah, C.S., Simate, G.S. (2015) Nanoparticles as potential new generation broad spectrum antimicrobial agents. DARU 23, 43 doi: https://doi.org/10.1186/s40199-015-0125-6 Yang, F.L., Li, X.G., Zhu, F., Lei, C.L. (2009) Structural characterization of nanoparticles loaded with garlic essential oil and their insecticidal activity against Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae). J. Agric. Food. Chem. 57 (21), 10156–10162 Yilmaz, Y., Toledo, R.T. (2004) Major flavonoids in grape seeds and skins: antioxidant capacity of catechin, epicatechin, and gallic acid. J. Agric. Food. Chem. 52 (2), 255–260