The antimicrobial and antioxidant potentials of Annona species (A. muricata, A. squamosa, and A. reticulata) through leaf infusions

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NURMIATI NURMIATI
PERIADNADI PERIADNADI
SONIA FARMILA SYAHRIL
TRI WIDYA EDELWIS

Abstract

Abstract. Nurmiati N, Periadnadi P, Syahril SF, Edelwis TW. 2024. The antimicrobial and antioxidant potentials of Annona species (A. muricata, A. squamosa, and A. reticulata) through leaf infusions. Biodiversitas 25: 3422-3430. This study aimed to determine the antimicrobial and antioxidant potential of infusions derived from dried leaves of Soursop (Annona muricata L.), Sugar Apple (Annona squamosa L.), and Custard Apple (Annona reticulata L.). Using a nested pattern experimental method, this research aimed to evaluate the potential of these plant extracts in inhibiting microbial growth and antioxidant properties. The experiment used in this research is a nested experimental design with 2 factors and 3 replications, where factor A represents the extract type, while factor B represents the test microorganism. The antibacterial assay was conducted using the disk diffusion and dilution methods against Staphylococcus aureus, Escherichia coli, and Candida albicans. Minimum Inhibitory Concentration (MIC) and Minimum Lethal Concentration (MLC) are determined. Antioxidant activity was assessed using the 2,2-diphenyl-1-picrylhydrazyl (DPPH) method, while Total Phenolic Content (TPC) and carotenoid levels were measured using Folin-Ciocalteu and spectrophotometric methods, respectively. The results showed that the infusion of dried custard apple leaves had the highest growth inhibition against S. aureus ATCC 29213, with a zone of inhibition of 10.65 mm. However, these effects were not significantly different for E. coli American Type Culture Collection (ATCC) 25922 and C. albicans. The dried custard apple leaf infusion showed an inhibition rate of 48.58% against S. aureus, compared to the positive control chloramphenicol (0.1 mg/mL), and inhibition rates of 24.57% against E. coli and 28.70% against C. albicans, compared to the positive control fluconazole (0.1 mg/mL). The results revealed that the Minimum Inhibitory Concentration (MIC) of soursop and custard apple leaf extracts against S. was 6.25%, with a Minimum Lethal Concentration (MLC) of 12.5%. The MIC of sugar apple leaf extract against S. aureus was 6.25%, with an MLC of 25%. The antioxidant activity of the soursop leaf extract had the highest antioxidant activity, with the IC50 value of 38.56 ?g/mL. The custard apple leaf extract had the highest polyphenol content (38.97 mgGAE/mL). The fresh sugar apple leaf extract emerged as the leader in carotenoid content, recording an impressive 548.84 ?mol/g. This research revealed the potential bioactivity of the infusions derived from dried leaves of Soursop, Sugar Apple, and Custard Apple for antimicrobial efficacy and potent antioxidant properties. Therefore, they might have the potential as novel therapeutic agents and nutraceuticals.

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References
Ahmad SK, Odunayo OO, Zhang, B, Huda, N, Benjakul S. 2021. Pulsed electric field assisted process for extraction of bioactive compounds from custard apple (Annona squamosa) leaves. Food Chem 359: 129976. DOI: 10.1016/j.foodchem.2021.129976.
Ahmed B, Floc’h, JB, Lahrach Z, Hijri M. 2021. Phytate and microbial suspension amendments increased soybean growth and shifted microbial community structure. Microorganisms 9 (9): 1–21. DOI: 10.3390/microorganisms9091803.
Balouiri M, Sadiki M, Ibnsouda SK. 2016. Methods for in vitro evaluating antimicrobial activity: A review. J Pharm Anal 6 (2): 71–79. DOI: 10.1016/j.jpha.2015.11.005.
Bitwell C, Indra SS, Luke C, Kakoma MK. 2023. A review of modern and conventional extraction techniques and their applications for extracting phytochemicals from plants. Sci African 19 : e01585. DOI: 10.1016/j.sciaf.2023.e01585.
Chowdhury SS, Tareq AM, Tareq SM, Farhad S, Sayeed MA. 2021. Screening of antidiabetic and antioxidant potential along with phytochemicals of Annona genus: a review. Future J Pharm Sci 7: 12-17. DOI: 10.1186/s43094-021-00300-9.
Cruz-Casas DE, Aguilar CN, Ascacio-Valdés JA, Rodríguez-Herrera R, Chávez-González ML, Flores-Gallegos A.C. 2023. Bioactive protein hydrolysates obtained from amaranth by fermentation with lactic acid bacteria and Bacillus species. Heliyon 9 (2): 17-25. DOI: 10.1016/j.heliyon.2023.e13491.
Dias WLF, do Vale Junior EP, das Dores Alves de Oliveira M, Barbosa YLP, do Nascimento Silva J, da Costa Júnior JS, de Almeida PM, Martins FA. 2019. Cytogenotoxic effect, phytochemical screening and antioxidant potential of Jatropha mollissima (Pohl) Baill leaves. South African J Bot 123: 30–35. DOI: 10.1016/j.sajb.2019.02.007.
Dos Santos ÉL, Santana AC, Micheletti AC, Freire TV, Guterres ZR, Yoshida NC. 2023. Metabolomic profiling and assessment of antimicrobial, antioxidant and genotoxic potential of Unonopsis guatterioides R.E.Fr. (Annonaceae) fruits. Arab J Chem 16 (10): 1-15. DOI: 10.1016/j.arabjc.2023.105133.
El-Belely EF, Farag MMS, Said HA, Amin AS, Azab E, Gobouri AA, Fouda A. 2021. Green synthesis of zinc oxide nanoparticles (Zno-nps) using arthrospira platensis (class: Cyanophyceae) and evaluation of their biomedical activities. Nanomaterials 11 (1): 1–18. DOI: 10.3390/nano11010095.
Fonmboh DJ, Abah ER, Fokunang TE, Herve B, Teke GN, Rose NM, Borgia NN, Fokunang LB, Andrew BN, Kaba N, Bathelemy N, Ntungwen FC. 2020. An Overview of Methods of Extraction, Isolation and Characterization of Natural Medicinal Plant Products in Improved Traditional Medicine Research. Asian J Res Med Pharm Sci 9 (2): 31–57. DOI: 10.9734/ajrimps/2020/v9i230152.
Hashem AH, Attia MS, Kandil EK, Fawzi MM, Abdelrahman AS, Khader MS, Khodaira MA, Emam AE, Goma MA, Abdelaziz AM. 2023. Bioactive compounds and biomedical applications of endophytic fungi: a recent review. Microb Cell Fact 22 (1): 1–23. DOI: 10.1186/s12934-023-02118-x.
Herrera-Calderon O, Enciso-Roca E, Pari-Olarte B, Arroyo-Acevedo J. 2016. Phytochemical screening, antioxidant activity and analgesic effect of Waltheria ovata Cav. roots in mice. Asian Pacific J Trop Dis 6 (12): 1000–1003. DOI: 10.1016/S2222-1808(16)61172-6.
Idenyi JN, Eya JC, Nwankwegu AS, Nwoba EG. 2022. Aquaculture sustainability through alternative dietary ingredients: Microalgal value-added products Eng Microbiol 2 (4): 100049. DOI: 10.1016/j.engmic.2022.100049.
Jemikalajah J, Enwa FO, Chiedozie EC. 2021. Antibacterial Activity of Annona muricata (Soursop) Leaf Extract) On Escherichia coli and Pseudomonas aeruginosa. Turkish J Physiother Rehabil 32 (3): 13918–13923.
Kahraman C, Topcu G, Bedir E, Tatli II, Ekizoglu M, Akdemir ZS. 2019. Phytochemical screening and evaluation of the antimicrobial and antioxidant activities of Ferula caspica M. Bieb. extracts. Saudi Pharm J 27 (4): 525–531. DOI: 10.1016/j.jsps.2019.01.016.
Kavithaa K, Paulpandi M, Ponraj T, Murugan K, Sumathi S. 2016. Induction of intrinsic apoptotic pathway in human breast cancer (MCF-7) cells through facile biosynthesized zinc oxide nanorods. Karbala Int J Mod Sci 2 (1): 46–55. DOI: 10.1016/j.kijoms.2016.01.002.
Kumar M, Changan S, Tomar M, Prajapati U, Saurabh V, Hasan M, Sasi M, Maheshwari C, Singh S, Dhumal S, Radha TM, Punia S, Satankar V, Amarowicz R, Mekhemar M. 2021. Custard apple (Annona squamosa L.) leaves: Nutritional composition, phytochemical profile, and health-promoting biological activities. Biomolecules 11 (5): 12-24. DOI: 10.3390/biom11050614.
Kumari A, Sharan L, Patnaik A. 2021. Annona reticulata L. phytoconstituents and pharmacology: A review. Int J Ecol Environ Sci 12 (2): 12-23.
Kuppusamy S, Venkateswarlu K, Megharaj M. 2020. Examining the polyphenol content, antioxidant activity and fatty acid composition of twenty-one different wastes of fruits, vegetables, oilseeds and beverages. SN Appl Sci 2: 1–13. DOI: 10.1007/s42452-020-2441-9.
Lima ARA, Baltazar-soares M, Garrido S, Carrera P, Piecho-santos AM, Peck MA, Silva G. 2021. Combined effect of prior pulsed electric field, dechlorophyllized soursop leaf extract and vacuum impregnation on melanosis inhibition and shelf-life extension of refrigerated Pacific white shrimp. Sci Total Environ 12 (3): 150167. DOI: 10.1016/j.foodcont.2024.110494.
Lingaraju K, Naika HR, Nagabhushana H, Nagaraju G. 2019. Euphorbia heterophylla (L.) mediated fabrication of ZnO NPs: Characterization and evaluation of antibacterial and anticancer properties. Biocatal Agric Biotechnol 18 (2): 100894. DOI: 10.1016/j.bcab.2018.10.011.
Mariychuk R, Porubská J, Ostafin M, ?aplovi?ová M, Eliašová A. 2020. Green synthesis of stable nanocolloids of monodisperse silver and gold nanoparticles using natural polyphenols from fruits of Sambucus nigra L. Appl Nanosci 12(1): 1-8. DOI: 10.1007/s13204-020-01324-y.
Medda S, Hajra A, Dey U, Bose P, Mondal NK. 2015. Biosynthesis of silver nanoparticles from Aloe vera leaf extract and antifungal activity against Rhizopus sp. and Aspergillus sp. Appl Nanosci 5 (2): 875–880. DOI: 10.1007/s13204-014-0387-1.
Ngbolua KTN, Inkoto CL, Bongo GN, Moke LE, Lufuluabo LG, Ashande CM, Tshibangu DST, Tshilanda DD, Mpiana PT. 2018. Phytochemistry and Bioactivity of Annona reticulata L. (Annonaceae): A Mini-review. South Asian Res J Nat Prod 1 (2): 1–11.
Nurmiati N, Periadnadi P, Alamsyah F, Sapalina F. 2018. Characterization and Potential of Acid Fermentative and Proteolytic Natural Microflora in Several Products of Traditional Dadih from Lembah Gumanti District West Sumatra, Indonesia. Int J Curr Microbiol Appl Sci 7 (3): 3151–3163. DOI: 10.20546/ijcmas.2018.703.364.
Patiño-Ruiz D, Sánchez-Botero L, Tejeda-Benitez L, Hinestroza J, Herrera A. 2020. Green synthesis of iron oxide nanoparticles using Cymbopogon citratus extract and sodium carbonate salt: Nanotoxicological considerations for potential environmental applications. Environ Nanotechnology Monit Manag 14 (2): 14-27. DOI: 10.1016/j.enmm.2020.100377.
Rajendran R, Mani A. 2020. Photocatalytic, antibacterial and anticancer activity of silver-doped zinc oxide nanoparticles. J Saudi Chem Soc 24 (4): 1010–1024. DOI: 10.1016/j.jscs.2020.10.008
Ramalingam V, Rajaram R. 2018. Enhanced antimicrobial, antioxidant and anticancer activity of Rhizophora apiculata: An experimental report. 3 Biotech 8: 12-21. DOI: 10.1007/s13205-018-1222-2.
Ramyabharathi S, Meena KS, Rajendran L, Raguchander T, Jonathan EI. 2020. Potential of a rhizobacterium Bacillus subtilis (Bbv 57) on Fusarium oxysporum f. sp. gerberae and Meloidogyne incognita infecting Gerbera grown in protected cultivation. Eur J Plant Pathol 158 (3): 615–632. DOI: 10.1007/s10658-020-02087-6.
Rohmah J, Margareta FA. 2023. Antioxidant Activity, Total Flavonoids and Total Phenolics Content of Infusion, and Decoction of White Agathi (Sesbania grandiflora (L.) Pers.) Leaves Extracts. AIP Conf Proc 13 (12): 2642. DOI: 10.1063/5.0110918.
Shrestha R, Thenissery A, Khupse R, Rajashekara G. 2023. Strategies for the Preparation of Chitosan Derivatives for Antimicrobial, Drug Delivery, and Agricultural Applications: A Review. Molecules 28 (3):15-23. DOI: 10.3390/molecules28227659.
Tiwari V, Mishra N, Gadani K, Solanki PS, Shah NA, Tiwari M. 2018. Mechanism of anti-bacterial activity of zinc oxide nanoparticle against Carbapenem-Resistant Acinetobacter baumannii. Front Microbiol 9 (3): 1218. DOI: 10.3389/fmicb.2018.01218.
Uchegbu R, Ukpai K, Iwu I, Akalazu J. 2017. Evaluation of the Antimicrobial Activity and Chemical Composition of the Leaf Extract of Annona muricata Linn (Soursop) Grown in Eastern Nigeria. Arch Curr Res Int 7 (3): 1–7. DOI: 10.9734/acri/2017/31929.
Viñas-Ospino A, Pani? M, Radoj?i?- Redovnikovi? I, Blesa J, Esteve MJ. 2023. Using novel hydrophobic deep eutectic solvents to improve a sustainable carotenoid extraction from orange peels. Food Biosci 53 (2): 23-31. DOI: 10.1016/j.fbio.2023.102570.
Vishvakarma P, Mandal S, Verma A, Author-Prabhakar VCA. 2023. International Journal of Pharma Professional’S Research a Review on Current Aspects of Nutraceuticals and Dietary Supplements.Antibiotics 14 (2): 78–91.
Wang Y, Zhang M, Zhan C. 2023. A review on the nested distribution pattern (nestedness): Analysis methods, mechanisms and conservation implications. Biodivers Sci 31 (3): 1–17. DOI: 10.17520/biods.2023314.
Weng Z, Zeng F, Wang M, Guo S, Tang Z, Itagaki K, Lin Y, Shen X, Cao Y, Duan J, Wang F. 2024. Antimicrobial activities of lavandulylated flavonoids in Sophora flavences against methicillin-resistant Staphylococcus aureus via membrane disruption. J Adv Res 57 (3): 197–212. DOI: 10.1016/j.jare.2023.04.017.
Werdiningsih W, Zahro A. 2020. Determination of flavonoid and phenol levels from Srikaya (Annona squamosal L) leaves and their activity as antioxidants. J Wiyata 7 (3): 157–170.
Yun D, Yan Y, Liu J. 2022. Isolation, structure and biological activity of polysaccharides from the fruits of Lycium ruthenicum Murr: A review. Carbohydr Polym 291 (3): 119618. DOI: 10.1016/j.carbpol.2022.119618.