Antibacterial activity of seed extracts of various species of the Annonaceae family cultivated in Colombia
Abstract
Public health concerns increase due to microbial propagation and the resistance to existing drugs; therefore, new alternatives are sought, such as the use of natural sources that are antimicrobial agents. Thus, the aim of this study was to evaluate the antibacterial potential of ethanolic extracts of seeds of the species Annona muricata (L.), Annona cherimola (Miller), Annona glabra (L.), Annona reticulata (L.), Rollinia mucosa ([Jacq.] Baillon) and Annona montana (Macfad.) of the Annonaceae family cultivated in Colombia. The bacterial strains correspond to: Staphylococcus aureus (Rosenbach), Enterococcus faecalis ([Andrewes and Horder] Schleifer and Kilpper-Bölz), Bacillus subtilis ([Ehrenberg] Cohn), Escherichia coli ([Migula] Castellani and Chalmers) and Pseudomonas aeruginosa ([J.Schröter] Migula). The antibacterial activity evaluation was performed using the agar diffusion method, each microorganism was inoculated in the medium in a concentration range of 0.2-0.5% v/v and the activity was measured by measuring the inhibition halo. A phytochemical assay was performed to identify the main metabolites to which the activity was attributed. Among the results obtained, it was found the extract of A. montana showed activity against the five bacterial strains, followed by A. glabra; the highest percentage of inhibition achieved was of A. cherimola with 79.86±3.81% activity against E. faecalis; A. reticulata and R. mucosa presented susceptibility only against two bacterial strains, the contrary, the extract of A. muricata did not present any response. The main types of metabolites identified and those attributed to antibacterial potential corresponded to alkaloids, saponins and terpenoids. The above indicates that the plants extract of Annonaceae showed antimicrobial effects. This suggest that species of this family are potential sources of compounds with antibacterial properties, which broadens the knowledge of natural extracts of Colombian materials for use in pharmacotherapy and as alternative for synthetic antibacterial agents.
Keywords
Annona montana, Annona glabra, Bactericide, Bacteriostatic, Plant extract, Inhibition, Rollinia
References
- BIBLIOGRAPHIC REFERENCES
- Aguilar-Hernández, G., B.A. López-Romero, A. Pérez-Larios, J.M. Ruvalcaba-Gómez, I. Castellanos-Huerta, G. Tellez-Isaias, V.M. Petrone-García, L.M. Anaya-Esparza, and E. Montalvo-González. 2023. Antibacterial activity of crude extract and purified acetogenins from Annona muricata seeds. Appl. Sci. 13(1), 558. Doi: https://doi.org/10.3390/app13010558
- Aguilar-Villalva, R., G.A. Molina, B.L. España-Sánchez, L.F. Díaz-Peña, A. Elizalde-Mata, E. Valerio, C. Aranza-Ricardo, and M. Estevez. 2021. Antioxidant capacity and antibacterial activity from Annona cherimola phytochemicals by ultrasound-assisted extraction and its comparison to conventional methods. Arab. J. Chem. 14(7), 103239. https://doi.org/10.1016/j.arabjc.2021.103239
- Arabski, M., S. Wąsik, K. Dworecki, and W. Kaca. 2009. Laser interferometric and cultivation methods for measurement of colistin/ampicilin and saponin interactions with smooth and rough of Proteus mirabilis lipopolysaccharides and cells. J. Microbiol. Methods 77(2), 178-183. Doi: https://doi.org/10.1016/J.MIMET.2009.01.020
- Barbieri, R., E. Coppo, A. Marchese, M. Daglia, E. Sobarzo-Sánchez, S.F. Nabavi, and S.M. Nabavi. 2017. Phytochemicals for human disease: An update on plant-derived compounds antibacterial activity. Microbiol. Res. 196, 44-68. Doi: https://doi.org/10.1016/J.MICRES.2016.12.003
- Barboza, T.J.S., A.F. Ferreira, A.C.P.R. Ignacio, and N. Albarello. 2015. Antimicrobial activity of Anonna mucosa (Jacq.) grown in vivo and obtained by in vitro culture. Braz. J. Microbiol. 46(3), 785-789. Doi: https://doi.org/10.1590/S1517-838246320140468
- Berić, T., M. Biočanin, S. Stanković, I. Dimkić, T. Janakiev, D. Fira, and J. Lozo. 2018. Identification and antibiotic resistance of Bacillus spp. isolates from natural samples. Arch. Biol. Sci. 70(3), 581-588. Doi: https://doi.org/10.2298/ABS180302019B
- Bhardwaj, R., A. Yadav, P. Sharma, and R.A. Sharma. 2014. In vitro and in vivo GC-MS profile and antimicrobial activity of phytosterols of Datura stramonium. Res. J. Med. Plants 8(3), 112-120. Doi: https://doi.org/10.3923/rjmp.2014.112.120
- Boorn, K.L., Y.-Y. Khor, E. Sweetman, F. Tan, T.A. Heard, and K.A. Hammer. 2010. Antimicrobial activity of honey from the stingless bee Trigona carbonaria determined by agar diffusion, agar dilution, broth microdilution and time-kill methodology. J. Appl. Microbiol. 108(5), 1534-1543. Doi: https://doi.org/10.1111/j.1365-2672.2009.04552.x
- Calvo, J. and L. Martínez-Martínez. 2009. Mecanismos de acción de los antimicrobianos. Enferm. Infecc. Microbiol. Clin. 27(1), 44-52. https://doi.org/10.1016/j.eimc.2008.11.001
- Colombia Instituto Nacional de Salud. 2022. Protocolo de vigilancia de brotes de enfermedades transmitidas por alimentos, versión 4. Doi: https://doi.org/10.33610/infoeventos.14
- CLSI, Clinical and Laboratory Standards Institute. 2018. Performances standards for antimicrobial disk susceptibility test. 13th ed. CLSI document M02-A12. Wayne, PA.
- Çördük, N., S. Demirbas, and D.N. Hacioglu. 2017. A comparative study of the antimicrobial properties and antioxidant enzyme activities of field-grown and in vitro-propagated plants of endemicdigitalis trojana Ivanina. Arch. Biol. Sci. 69(4), 603-610. Doi: https://doi.org/10.2298/ABS161216004C
- Elisha, I.L., F.S. Botha, L.J. McGaw, and J.N. Eloff. 2017. The antibacterial activity of extracts of nine plant species with good activity against Escherichia coli against five other bacteria and cytotoxicity of extracts. BMC Complement. Altern. Med. 17(1), 133. Doi: https://doi.org/10.1186/s12906-017-1645-z
- Fernández, I.M., E.A. Chagas, S.A.S. Maldonado, J.A. Takahashi, R.S. Alemán, A.A. Melo Filho, R.C. Santos, P.R.E. Ribeiro, J.A.M. Fuentes, P.C. Chagas, and A.C.G. R. Melo. 2020. Antimicrobial activity and acetilcolinesterase inhibition of oils and Amazon fruit extracts. J. Med. Plants Res. 14(3), 88-97. https://doi.org/10.5897/JMPR2019.6790
- Galvão, S.S.L., A.S. Monteiro, E.P. Siqueira, M.R.Q. Bomfim, M.V. Dias-Souza, G.F. Ferreira, A.M.L. Denadai, Á.R.C. Santos, V.L. Santos, E.M. Souza-Fagundes, E.S. Fernandes and V. Monteiro-Neto. 2016. Annona glabra flavonoids act as antimicrobials by binding to Pseudomonas aeruginosa cell walls. Front. Microbiol. 7, 2053. Doi: https://doi.org/10.3389/fmicb.2016.02053
- García-Perez, J., J.B. Ulloa-rojas, and S. Mendoza-Elvira. 2021. Patógenos bacterianos y su resistencia a los antimicrobianos en los cultivos de tilapia en Guatemala. Uniciencia 35(2), 1-17. Doi: https://doi.org/10.15359/ru.35-2.4
- Gavrilović, M., M.D. Soković, M. Stanković, P.D. Marin, Z. Dajić-Stevanović, and P. Janaćković. 2016. Antimicrobial and antioxidative activity of various leaf extracts of Amphoricarposvis. (Asteraceae) taxa. Arch. Biol. Sci. 68(4), 803-810. Doi: https://doi.org/10.2298/ABS160112068G
- Giraldo, A.I. and G.E. Guerrero. 2018. Rollinia mucosa (Jacq.) Baillon (Annonaceae) active metabolites as alternative biocontrol agents against the lace bug Corythucha gossypii (Fabricius): An insect pest. Univ. Sci. 23(1), 21-34. Doi: https://doi.org/10.11144/Javeriana.SC23-1.rmjb
- Giraldo, A.I., G.E. Guerrero, J.P. Arrubla, L.M. Baena, D. Paredes, and M.A. Gomez. 2020. The effects of Annonaceae and Amaryllidaceae extracts in controlling the Thrips tabaci Lindeman (Thysanoptera: Thripidae). Rev. Bras. Cienc. Agrar. 15(2), 1-9. Doi: https://doi.org/10.5039/agraria.v15i2a6933
- Giraldo-Rivera, A.I. and G.E. Guerrero-Alvarez. 2019. Botanical biopesticides: Research and development trends, a focus on the Annonaceae family. Rev. Colomb. Cienc. Hortic. 13(3), 371-383. Doi: https://doi.org/10.17584/rcch.2019v13i3.9489
- Harahap, D., S. Niaci, V. Mardina, B. Zaura, I. Qanita, A. Purnama, K. Puspita, D.R. Rizki, and M. Iqhrammullah. 2022. Antibacterial activities of seven ethnomedicinal plants from family Annonaceae. J. Adv. Pharm. Technol. Res. 13(3), 148-153.
- Haykal, T., P. Nasr, M.H. Hodroj, R.I. Taleb, R. Sarkis, M.N.E. Moujabber, and S. Rizk. 2019. Annona cherimola seed extract activates extrinsic and intrinsic apoptotic pathways in leukemic cells. Toxins 11(9), 506. Doi: https://doi.org/10.3390/toxins11090506
- Hovenkamp, E., I. Demonty, J. Plat, D. Lütjohann, R.P. Mensink, and E.A. Trautwein. 2008. Biological effects of oxidized phytosterols: A review of the current knowledge. Prog. Lipid Res. 47(1), 37-49. Doi: https://doi.org/10.1016/j.plipres.2007.10.001
- Iyanda-Joel, W.O., E.A. Omonigbehin, E.E.J. Iweala, and S.N. Chinedu. 2019. Antibacterial studies on fruit-skin and leaf extracts of Annona muricata in Ota, Nigeria. IOP Conf. Ser.: Earth Environ. Sci. 331(1), 120-129. https://doi.org/10.1088/1755-1315/331/1/012029
- Ji, J., J. Yang, L. Huang, and Z. Kang. 2016. A novel antifungal peptide purified from Bacillus subtilis strain EDR4. Arch. Biol. Sci. 68(2), 319-324. Doi: https://doi.org/10.2298/ABS150325022J
- Khalil, N., M. Ashour, S. Fikry, A.N. Singab, and O. Salama. 2018. Chemical composition and antimicrobial activity of the essential oils of selected Apiaceous fruits. Future J. Pharm. Sci. 4(1), 88-92. Doi: https://doi.org/10.1016/J.FJPS.2017.10.004
- Krinski, D., A. Massaroli, and M. Machado. 2014. Potencial inseticida de plantas da familia Annonaceae. Rev. Bras. Frutic. 36(Spl. 1), 225-242. Doi: https://doi.org/10.1590/S0100-29452014000500027
- León-Méndez, G., N. Pajaro-Castro, and C. Granados-Conde. 2020. Annona squamosa una fuente de acetogeninas en la actualidad. Ciencia y Salud Virtual 12(2), 88-101.
- Maas, P.J.M., L.Y.T. Westra, L.W. Chatrou, N. Verspagen, H. Rainer, N.A. Zamora, and R.H.J. Erkens. 2019. Twelve new and exciting Annonaceae from the Neotropics. PhytoKeys 126, 25-69. Doi: https://doi.org/10.3897/phytokeys.126.33913
- Maillard, J.-Y. 2002. Bacterial target sites for biocide action. J. Appl. Microbiol. 92(Spl. 1), 16-27. Doi: https://doi.org/10.1046/j.1365-2672.92.5s1.3.x
- Malik, T.A., A.N. Kamili, M.Z. Chishti, S. Ahad, M.A. Tantry, P.R. Hussain, and R.K. Johri. 2017. Breaking the resistance of Escherichia coli: Antimicrobial activity of Berberis lycium Royle. Microb. Pathog. 102, 12-20. Doi: https://doi.org/10.1016/j.micpath.2016.11.011
- Maya, C.A., T.A. Madrid, and J.E. Parra. 2021. Efecto de Bacillus subtilis sobre metabolitos sanguíneos y parámetros productivos en pollo de engorde. Biotecnol. Sector Agropecuario Agroind. 19(1), 105-116. Doi: https://doi.org/https://doi.org/10.18684/bsaa.v19.n1.2021.1468
- Mosquera, T., A. Medrano, and M.E. Maldonado. 2020. Extractos naturales una alternativa conservante en la industria cosmética. Rev. Iber. Sist. Tecnol. Inf. (E30), 139-149.
- Mullins, J.T. 1990. Regulatory mechanisms of β‐glucan synthases in bacteria, fungi, and plants. Physiol. Plant. 78(2), 309-314. Doi: https://doi.org/10.1111/j.1399-3054.1990.tb02096.x
- Nájera-Arce, C., P. Álvarez-Fitz, D. Pérez-Castro, J. Toribio-Jiménez, and N. Castro-Alarcón. 2018. Actividad antibacteriana de diatomeas marinas aisladas de Acapulco, Guerrero, México. Rev. Biol. Mar. Oceanogr. 53(2), 195-207. Doi: https://doi.org/10.22370/rbmo.2018.53.2.1293
- Osorio, E., G.J. Arango, N. Jiménez, F. Alzate, G. Ruiz, D. Gutiérrez, M.A. Paco, A. Giménez, and S. Robledo. 2007. Antiprotozoal and cytotoxic activities in vitro of Colombian Annonaceae. J. Ethnopharmacol. 111(3), 630-635. Doi https://doi.org/10.1016/j.jep.2007.01.015
- Palacios, S., R. Rodríguez, A.C. Flores, M.L. Chávez, R. Ramos, E.P. Segura, and A. Ilina. 2019. Alternativas para el control de bacterias transmitidas por alimentos. CienciAcierta 57, 1-10.
- Perrone, A., S. Yousefi, A. Salami, A. Papini, and F. Martinelli. 2022. Botanical, genetic, phytochemical and pharmaceutical aspects of Annona cherimola Mill. Sci. Hortic. 296, 110896. Doi: https://doi.org/10.1016/j.scienta.2022.110896
- Pinto, N.C.C., L.M. Campos, A.C.S. Evangelista, A.S.O. Lemos, T.P. Silva, R.C.N. Melo, C.C. Lourenço, M.J. Salvador, A.C.M. Apolônio, E. Scio, and R.L. Fabri. 2017. Antimicrobial Annona muricata L. (soursop) extract targets the cell membranes of Gram-positive and Gram-negative bacteria. Ind. Crops Prod. 107, 332-340. Doi: https://doi.org/10.1016/j.indcrop.2017.05.054
- Rabea, E.I., M.E.-T. Badawy, C.V. Stevens, G. Smagghe, and W. Steurbaut. 2003. Chitosan as antimicrobial agent: Applications and mode of action. Biomacromolecules 4(6), 1457-1465. Doi: https://doi.org/10.1021/bm034130m
- Rodríguez, C.N., A.G. Zarate, and L.C. Sánchez. 2017. Actividad antimicrobiana de cuatro variedades de plantas frente a patógenos de importancia clínica en Colombia. Nova 15(27), 119-129.
- Saleem, M., M. Nazir, M.S. Ali, H. Hussain, Y.S. Lee, N. Riaz, and A. Jabbar. 2003. Antimicrobial natural products: an update on future antibioticdrug candidates. Nat. Prod. Rep. 27(2), 238-254. Doi: https://doi.org/10.1039/B916096E
- Torres-Chati, J., J. León-Quispe, and G. Tomas-Chota. 2017. Actividad antibacteriana y antifúngica de extractos de hojas de Luma chequen (Molina) A. Gray arrayán frente a patógenos de origen clínico. Rev. Soc. Ven. Microbiol. 37(1), 10-16.
- Tojola, O.B., L. Lajide, B.J. Owolabi, M. Olaleye, and S.O. Okoh. 2019. Antifungal activities of ethyl acetate and methanol extracts of Annona muricata aerial part. Int. J. Innov. Res. Dev. 8(8), 41-44. Doi: https://doi.org/10.24940/ijird/2019/v8/i8/aug19027