Bioactive compounds, antioxidant and antibacterial properties of the pulp, peel and aril of the fruit of Clusia quadrangula (Clusiaceae)
DOI:
https://doi.org/10.21829/abm130.2023.2180Keywords:
antimicrobial properties, fatty acids, minerals, polyphenolsAbstract
Background and Aims: The Clusiaceae family is known for its bioactive compounds with beneficial antioxidant and anti-inflammatory properties. The objectives of this study were to 1) identify and quantify the individual polyphenol compounds in the methanolic extract from peel, pulp and aril of the fruit of Clusia quadrangula by UPLC-MSMS, evaluate their antioxidant properties, 2) analyze the fatty acid profile, minerals composition and 3) determine the antibacterial activity against pathogenic bacteria of the methanolic extract.
Methods: Physicochemical properties, antioxidants and bioactive compounds, fatty acid profile and mineral content were analyzed using a Microplate Spectrophotometer, Ultra High Performance Liquid Chromatography coupled with a triple quadrupole Mass Spectrometer, Gas Chromatography coupled with a Mass Spectrometer and Microwave Plasma Atomic Emission Spectroscopy.
Key results: Twenty phenolic compounds were identified and quantified plus the precursor shikimic acid (103.55 µg/g solids). Procyanidin B2 (41.56 µg/g solids), (−)-epicatechin (34.07 µg/g solids), and ellagic acid (27.58 µg/g solids) were found in greater quantity in the methanolic extract of the pulp. Palmitic and linoleic acid were the most abundant fatty acids in the pulp, peel, and aril, and linolenic acid was present in the pulp. The pulp also exhibited the highest amount of total polyphenolic compounds (24.33 mg GAE/g) and reducing power evaluated by FRAP (18.697 mg ET/g). Analysis of the minerals revealed that all fractions are rich in magnesium, potassium, sodium, and calcium. The results showed that the methanolic extract of the different parts of the fruit had antibacterial properties against Salmonella typhi, Escherichia coli, Staphylococcus aureus, and Enterococcus faecalis.
Conclusions: These results indicate that different parts of the C. quadrangula fruit are a rich source of natural antioxidants and possess antibacterial properties. Therefore, it can be considered for use as ingredient or additive in the cosmetic, pharmaceutical, or food industries.
Downloads
References
Ayahi, I. A., R. A. Oderinde, B. O. Ogunkoya, A. Egunyomi and V. O. Taiwo. 2007. Chemical analysis and preliminary toxicological evaluation of Garcinia mangostana seeds and seed oil. Food Chemistry 101(3): 999-1004. DOI: https://doi.org/10.1016/j.foodchem.2006.02.053 DOI: https://doi.org/10.1016/j.foodchem.2006.02.053
Bai, J., Y. Wu, X. Liu, K. Zhong, Y. Huang and H. Gao. 2015. Antibacterial activity of shikimic acid from pine needles of Cedrus deodara against Staphylococcus aureus through damage to cell membrane. International Journal of Molecular Sciences 16(11): 27145-27155. DOI: https://doi.org/10.3390/ijms161126015 DOI: https://doi.org/10.3390/ijms161126015
Bai, J. R., K. Zhong, Y. P. Wu, G. Elena and H. Gao. 2019. Antibiofilm activity of shikimic acid against Staphylococcus aureus. Food Control 95: 327-333. DOI: https://doi.org/10.1016/j.foodcont.2018.08.020 DOI: https://doi.org/10.1016/j.foodcont.2018.08.020
Compagnone, R. S., A. Castillo Suarez, S. G. Leitao and F. Delle Monache. 2008. Flavonoids, benzophenones and a new euphane derivative from Clusia columnaris Engl. Brazilian Journal of Pharmacognosy 18(1): 6-10. DOI: https://doi.org/10.1590/S0102-695X2008000100003 DOI: https://doi.org/10.1590/S0102-695X2008000100003
Da Silva, M. C. and S. R. Paiva. 2012. Antioxidant activity and flavonoid content of Clusia fluminensis Planch. & Triana. Anais da Brasileira de Ciencias 84(3): 609-616. DOI: https://doi.org/10.1590/S0001-37652012000300004 DOI: https://doi.org/10.1590/S0001-37652012000300004
Del Valle, H. B., A. L. Yaktine, C. L. Taylor and A. C. Ross. 2011. Dietary Reference Intakes for Calcium and Vitamin D. National Academies Press. Washington, DC., USA. 662 pp.
Dżugan, M., D. Grabek-Lejko, S. Swacha, M. Tomczyk, S. Bednarska and I. Kapusta. 2020. Physicochemical quality parameters antibacterial properties and cellular antioxidant activity of Polish buckwheat honey. Food Bioscience 34: 100538. DOI: https://doi.org/10.1016/j.fbio.2020.100538 DOI: https://doi.org/10.1016/j.fbio.2020.100538
Fei, P., M. A. Ali, S. Gong, Q. Sun, X. Bi, S. Liu and L. Guo. 2018. Antimicrobial activity and mechanism of action of olive oil polyphenols extract against Cronobacter sakazakii. Food Control 94: 289-294. DOI: https://doi.org/10.1016/j.foodcont.2018.07.022 DOI: https://doi.org/10.1016/j.foodcont.2018.07.022
Ferreira-Oliveira, R., C. Amorim-Camara, M. F. Agra, T. M. Sarmento-Silva. 2012. Biflavonoids from the unripe fruits of Clusia paralicola and their antioxidant activity. Natural Product Communications 7(12): 1597-1600. DOI: https://doi.org/10.1177/1934578X1200701215 DOI: https://doi.org/10.1177/1934578X1200701215
Fu, C., A. E. K. Loo, F. P. P. Chia and D. Huang. 2007. Oligomeric procyanidins from mangosteen pericarps. Journal of Agricultural and Food Chemistry 55(19): 7689-7694. DOI: https://doi.org/10.1021/jf071166n DOI: https://doi.org/10.1021/jf071166n
Giusti, M. M. and R. E. Wrolstad. 2001. Anthocyanins. Characterization and Measurement with UV-Visible Spectroscopy. Current Protocols in Food Analytical Chemistry. Unit, 1: F1.2.1-13. DOI: https://doi.org/10.1002/0471142913.faf0102s00 DOI: https://doi.org/10.1002/0471142913.faf0102s00
Hornero, D. and M. I. Mínguez. 2001. Rapid spectrophotometric determination of red and yellow isochromic carotenoid fractions in paprika and red pepper oleoresins. Journal of Agricultural and Food Chemistry 49(8): 3584-3588. DOI: https://doi.org/10.1021/jf010400l DOI: https://doi.org/10.1021/jf010400l
Huang, L., K. P. Yang, Q. Zhao, H. J. Li, J. Y. Wang and Y. C. Wu. 2022. Corrosion resistance and antibacterial activity of procyanidin B2 as a novel environment-friendly inhibitor for Q235 steel in 1 M HCl solution. Bioelectrochemistry 143: 107969. DOI: https://doi.org/10.1016/j.bioelechem.2021.107969 DOI: https://doi.org/10.1016/j.bioelechem.2021.107969
Huerta-Reyes, M., M. C. Basualdo, L. Lozada, M. Jiménez-Estrada, C. Soler and R. Reyes-Chilpa. 2004. HIV Inhibition by extracts of Clusiaceae species from Mexico. Biological and Pharmaceutical Bulletin 27(6): 916-920. DOI: https://doi.org/10.1248/bpb.27.916 DOI: https://doi.org/10.1248/bpb.27.916
Jacota, S. and H. Dani. 1982. A new colorimetric technique for the estimation of vitamin C using Folin phenol reagent. Analytical Biochemistry 127(1): 178-182. DOI: https://doi.org/10.1016/0003-2697(66)90168-0 DOI: https://doi.org/10.1016/0003-2697(82)90162-2
Juárez-Trujillo, N., J. L. Monribot-Villanueva, V. M. Jiménez-Fernández, R. Suárez-Montaño, A. S. Aguilar-Colorado, J. A., Guerrero-Analco and M. Jiménez. 2018. Phytochemical characterization of Izote (Yucca elephantipes) flowers. Journal of Applied Botany and Food Quality 210: 202-210. DOI: https://doi.org/10.5073/JABFQ.2018.091.027
Kilonzo, M. and D. Munisi. 2021. Antimicrobial activity and phytochemical analysis of Harrisonia abyssinica (Oliv) and Vepris simplicifolia (Verd) extracts used as traditional medicine in Tanzania. Saudi Journal of Biological Sciences 28(12): 7481-7485. DOI: https://doi.org/10.1016/j.sjbs.2021.08.041 DOI: https://doi.org/10.1016/j.sjbs.2021.08.041
Kshirsagar, P., S. Gaikwad, S. Pai, N. Desai and V. Bapat. 2022. Evaluation of antioxidant capacity and phytochemical investigation of eleven Clusiaceae members from Western Ghats, India. Biocatalysis and Agricultural Biotechnology 44: 102476. DOI: https://doi.org/10.1016/j.bcab.2022.102476 DOI: https://doi.org/10.1016/j.bcab.2022.102476
Lentz, D. L. 1993. Medicinal and other economic plants of the Paya of Honduras. Economic Botany 47(4): 358-370. DOI: https://doi.org/10.1007/BF02907349 DOI: https://doi.org/10.1007/BF02907349
López-López, A., A. I. Castellote-Bargalló, C. Campoy-Folgoso, M. Rivero-Urgel, R. Tormo-Carnicé, D. Infante-Pina and M. C. López-Sabater. 2001. The influence of dietary palmitic acid triacylglyceride position on the fatty acid, calcium and magnesium contents of at term newborn faeces. Early Human Development 65(2): S83-S94. DOI: https://doi.org/10.1016/s0378-3782(01)00210-9 DOI: https://doi.org/10.1016/S0378-3782(01)00210-9
Lupette, J. and C. Benning. 2020. Human health benefits of very-long-chain polyunsaturated fatty acids from microalgae. Biochimie 178: 15-25. DOI: https://doi.org/10.1016/j.biochi.2020.04.022 DOI: https://doi.org/10.1016/j.biochi.2020.04.022
Machado, M. M. P. and M. Emmerich. 1981. Presença de coléteres em Clusia lanceolata Cambess. Boletín del Museo Nacional de Historia Natural 59: 1-7.
Manach, C., A. Scalbert, C. Morand, C. Rémésy and L. Jiménez. 2004.. Polyphenols: food sources and bioavailability. The American Journal of Clinical Nutrition 79(5): 727-747. DOI: https://doi.org/10.1093/ajcn/79.5.727 DOI: https://doi.org/10.1093/ajcn/79.5.727
Mattos-Silva, K. M., B. Nunes-Luna, A. Joffili, S. Ribeiro-Paiva and C. Franca-Barros. 2019. Revealing the development of secretory structures in the leaves of Clusia fluminensis and Clusia lanceolata (Clusiaceae). Flora 256: 69-78. DOI: https://doi.org/10.1016/j.flora.2019.05.002 DOI: https://doi.org/10.1016/j.flora.2019.05.002
Mehrzadi, S., N. Bahrami, M. Mehraabani, M. Motevalian, E. Mansouri and M. Goudarzi. 2018. Ellagic acid: a promising protective remedy against testicular toxicity induced by arsenic. Biomedine & Pharmacotherapy 103: 1464-1472. DOI: https://doi.org/10.1016/j.biopha.2018.04.194 DOI: https://doi.org/10.1016/j.biopha.2018.04.194
Olivares, E. and G. Aguiar. 1999. Total and water-soluble calcium in six species of Clusiaceae. Flora 194(2): 179-188. DOI: https://doi.org/10.1016/S0367-2530(17)30896-4 DOI: https://doi.org/10.1016/S0367-2530(17)30896-4
Othman, L., A. Sleiman and R. M. Abdel-Massih. 2019. Antimicrobial activity of polyphenols and alkaloids in Middle Eastern plants. Frontiers in Microbiology 10: 911. DOI: https://doi.org/10.3389/fmicb.2019.00911 DOI: https://doi.org/10.3389/fmicb.2019.00911
Patel, A., S. S. Desai, V. K. Mane, J. Enman, U. Rova, P. Christakopoulos and L. Matsakas. 2022. Futuristic food fortification with a balanced ratio of dietary ω-3/ ω-6 omega fatty acids form the prevention of lifestyle diseases. Trends in Food Science & Technology 120: 140-153. DOI: https://doi.org/10.1016/j.tifs.2022.01.006 DOI: https://doi.org/10.1016/j.tifs.2022.01.006
Padhi, E., R. Liu, M. Hernandez, R. Tsao and D. Dan. 2016. Total polyphenol content, carotenoid, tocopherol and fatty acid composition of commonly consumed Canadian pulses and their contribution to antioxidant activity. Journal of Functional Foods 38(Part B): 602-611. DOI: https://doi.org/10.1016/j.jff.2016.11.006 DOI: https://doi.org/10.1016/j.jff.2016.11.006
Porri, D., H. Biesalski, A. Limitone, L. Bertuzzo and H. Cena. 2021. Effect of magnesium supplementation of women’s health and well-being. Nutrition Food Science 23: 30-36. DOI: https://doi.org/10.1016/j.nfs.2021.03.003 DOI: https://doi.org/10.1016/j.nfs.2021.03.003
Ramirez, C., J. H. Gil, C. Marín-Loaiza, B. Rojano and D. Durango. 2018. Chemical constituents and antioxidant activity of Garcinia madruno (Kunth) Hammel. Journal of King Saud University - Science 31(4): 1283-1289. DOI: https://doi.org/10.1016/j.jksus.2018.07.017 DOI: https://doi.org/10.1016/j.jksus.2018.07.017
Reche, J., M. S. Almansa, F. Hernández, A. A. Carbonell-Barrachina, P. Legua and A. Amorós. 2019. Fatty acid profile and pulp of Spanish jujube (Ziziphus jujube Mill.) fruit. Food Chemistry 295: 247-253. DOI: https://doi.org/10.1016/j.foodchem.2019.05.147 DOI: https://doi.org/10.1016/j.foodchem.2019.05.147
Ribeiro, P. R., C. Ferraz, L. S. Guedes, D. Martins and F. G. Cruz. 2011. A new biphenyl and antimicrobial activity of extracts and compounds from Clusia burlemarxii. Fitoterapia 82(8): 1237-1240. DOI: https://doi.org/10.1016/j.fitote.2011.08.012 DOI: https://doi.org/10.1016/j.fitote.2011.08.012
Rice-Evans, C., N. J. Miller and G. Paganga. 1996. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology and Medicine 20(7): 933-956. DOI: https://doi.org/10.1016/0891-5849(95)02227-9 DOI: https://doi.org/10.1016/0891-5849(95)02227-9
Savi, A., G. C. Calegari, V. A. Queiroz Santos, E. Andrade Pereira and S. Dias Teixeira. 2020. Chemical characterization and antioxidant of polysaccharide extracted from Dioscorea bulbifera. Journal of King Saud University-Science 32(1): 636-642. DOI: https://doi.org/10.1016/j.jksus.2018.09.002 DOI: https://doi.org/10.1016/j.jksus.2018.09.002
Sayeed, R., M. Thakur and A. Gani. 2020. Celosia cristata Linn. flowers as a new source of nutraceuticals- A study on nutritional composition, chemical characterization and in-vitro antioxidant capacity. Heliyon 6(12): e05792. DOI: https://doi.org/10.1016/j.heliyon.2020.e05792 DOI: https://doi.org/10.1016/j.heliyon.2020.e05792
Silva-Gontijo, V., T. Correa de Souza, I. Aparecido-Rosa, M. Gomes-Soares, M. Aparecido da Silva, W. Villegas, C. Viegas-Junior and M. H. Dos Santos. 2012. Isolation and evaluation of the antioxidant activity of phenolic constituents of the Garcinia brasiliensis epicarp. Food Chemistry 132(3): 1230-1235. DOI: https://doi.org/10.1016/j.foodchem.2011.10.110 DOI: https://doi.org/10.1016/j.foodchem.2011.10.110
Singh, P., E. Gupta, N. Mishra and P. Mishra. 2020. Shikimic acid as intermediary model for the production of drugs effective against influenza virus. In: Egbuna, C., S. Kumar, J. C. Ifemeje, S. M. Ezzat and S. Kaliyaperumal (eds.). Phytochemicals as Lead Compounds for New Drug Discovery. Elsevier. Rockville, USA. Pp. 245-256. DOI: https://doi.org/10.1016/B978-0-12-817890-4.00016-0 DOI: https://doi.org/10.1016/B978-0-12-817890-4.00016-0
StatSoft and TIBCO Software Group Inc. 2002. Statistica version 7. Hamburg, Germany. https://www.tibco.com/data-science-and-streaming
Thaipong, K., U. Boonprakob, K. Crosby, L. Cisneros-Zevallos and D. H. Byrne. 2006. Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extract. Journal of Food Composition and Analysis 19(6-7): 669-675. DOI: https://doi.org/10.1016/j.jfca.2006.01.003 DOI: https://doi.org/10.1016/j.jfca.2006.01.003
Tome, A. C., E. Teixeira-Marsico, F. Alves-da Silva, L. Kato, Pimenta-do Nascimento and M. L. Guerra-Monteiro. 2019. Achachairu (Garcinia humilis): chemical characterization, antioxidant activity and mineral profile. Journal of Food Measurement and Characterization 13: 213-221. DOI: https://doi.org/10.1007/s11694-018-9934-x DOI: https://doi.org/10.1007/s11694-018-9934-x
Wang, W., R. Chen and J. Wang. 2017. Procyanidin B2 ameliorates carrageenan-induced chronic nonbacterial prostatitis in rats via anti-inflammatory and activation of the Nrf2 pathway. Biochemical and Biophysical Research Communications 493(1): 794-799. DOI: https://doi.org/10.1016/j.bbrc.2017.08.089 DOI: https://doi.org/10.1016/j.bbrc.2017.08.089
Zheng, D., C. Lv, X. Sun, J. Wang and Z. Zhao. 2019. Preparation of a supersaturable self-microemulsion as drug delivery system form ellagic acid and evaluation of its antioxidant activities. Journal of Drug Delivery Science and Technology 53: 101209. DOI: https://doi.org/10.1016/j.jddst.2019.101209 DOI: https://doi.org/10.1016/j.jddst.2019.101209
Zengin, G., Z. Aumeeruddy-Elelfi, A. Mollica, M. Abdullah-Yilmaz and M. F. Mahomoodally. 2018. In vitro and in silico perspectives on biological and phytochemical profile of three halophyte species - A source of innovative phytopharmaceuticals from nature. Phytomedicine 38: 35-44. DOI: http://doi.org/10.1016/j.phymed.2017.10.017 DOI: https://doi.org/10.1016/j.phymed.2017.10.017
Published
How to Cite
-
Abstract3079
-
PDF619
-
XML (Español)13
-
EPUB193
Issue
Section
License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Authors who publish in this journal accept the following conditions:
In accordance with copyright legislation, Acta Botanica Mexicana recognizes and respects the moral rights of authors, as well as the ownership of the patrimonial right, which will be assigned to the journal for its dissemination in open access. Acta Botanica Mexicana does not charge authors for sending and processing articles for publication.
All the texts published by Acta Botanica Mexicana - without exception- are distributed under the Creative Commons 4.0 Attribution-Non Commercial License (CC BY-NC 4.0 International), which allows third parties to use what is published whenever they mention the authorship of the work and the first publication in this journal.
The authors can make other independent and additional contractual agreements for the non-exclusive distribution of the version of the article published in Acta Botanica Mexicana (for example, include it in an institutional repository or publish it in a book) as long as they clearly indicate that the work was published for the first time in Acta Botanica Mexicana
As a consequence, the copyeditors will request you, together with the galley review, to issue your Letter-Transfer of Ownership of Copyright form of the first publication duly completed and signed by the author(s). This letter should be sent by email in pdf file to the email: acta.botanica@inecol.mx (Letter-Transfer of Ownership of Copyright).


