Abstract
Purpose
The valorization of citrus processing waste has a great potential for transition toward a bioeconomy. Hence, the objective of this study was to characterize the phenolic composition profile recovered from the citrus solid waste and its related in vitro antioxidant and antimicrobial activities.
Methods
Solid waste residues remaining after the juice extraction process of three citrus species, C. aurantium, C. sinensis and C. reticulata were extracted with maceration with hydroethanol mix.
Results
Our findings showed that the highest levels of polymethoxyflavones were found in C. sinensis waste extracts, while O-glycosylpolymethoxylated flavonoids were highly accumulated in C. aurantium residue extracts. Luteolin 7-O glucoside, rutin, and myricetin were identified as dominant metabolites of the residue extracts from C. aurantium, C. reticulata and C. sinensis, respectively. Based on relative antioxidant capacity index (RACI) and global antioxidant score (GAS) measurements, the solid waste extracts of C. aurantium exhibited the strongest antioxidant potential. C. aurantium waste extracts were the most active against Gram-positive bacteria and F. oxysporum fungus, while, C. reticulata waste extracts were the most effective against Gram-negative bacteria and the three pathogenesis fungi: B. subtilis, C. albicans and A. flavus. C. sinensis exhibited the highest antifungal activity against A. niger.
Conclusion
Correlation analysis highlighted a positive correlation between Gram-positive bacteria and the content in glycosylated metabolites in one hand, and between Gram-negative bacteria and flavonoids in another hand.
Graphic Abstract
Similar content being viewed by others
References
Adamczak, A., Ożarowski, M., Karpiński, T.M.: Antibacterial activity of some flavonoids and organic acids widely distributed in plants. J. Clin. Med. 9(1), 109 (2019)
Baskar, A.A., Ignacimuthu, S., Michael, G.P., Al, N.K.: Cancer chemopreventive potential of luteolin-7-O-glucoside isolated from ophiorrhiza mungos Linn. Nutr. Cancer 63(1), 130–138 (2011)
Blando, F., Russo, R., Negro, C., Bellis, L.D., Frassinetti, S.: Antimicrobial and antibiofilm activity against staphylococcus aureus of opuntia ficus-indica (L.) Mill cladode polyphenolic extracts. Antioxidants 8, 1–13 (2019)
Bonesi, M., Loizzo, M.R., Leporini, M., Tenuta, M.C., Passalacqua, N.G., Tundis, R.: Comparative evaluation of petitgrain oils from six Citrus species alone and in combination as potential functional anti-radicals and antioxidant agents. Plant Biosyst. (2017). https://doi.org/10.1080/11263504.2017.1403396
Bounatirou, S., Smiti, S., Miguel, M.G., Faleiro, L., Rejeb, M.N., Neffati, M.: Chemical composition, antioxidant and antibacterial activities of the essential oils isolated from tunisian thymus capitatus. Food Chem. 105, 146–155 (2007)
Cristani, M., D’Arrigo, M., Mandalari, G., Castelli, F., Sarpietro, M.G., Micieli, D., Venuti, V., Bisignano, G., Saija, A., Trombetta, D.: Interaction of four monoterpenes contained in essential oils with model membranes: implications for their antibacterial activity. J. Agric. Food Chem. 55, 6300–6308 (2007)
Echeverría, J., Opazo, J., Mendoza, L., Urzúa, A., Wilkens, M.: Structure-Activity and Lipophilicity Relationships of Selected Antibacterial Natural Flavones and Flavanones of Chilean Flora. Molecules (Basel, Switzerland) 22(4), 608 (2017). https://doi.org/10.3390/molecules22040608
Falcinelli, B., Famiani, F., Paoletti, A., D’Egidio, S., Stagnari, F., Galieni, A., Benincasa, P.: Phenolic compounds and antioxidant activity of sprouts from seeds of citrus species. Agriculture 10, 33 (2020)
Fancello, F., Petretto, G.L., Zara, S., Sanna, M.L., Addis, R., Maldini, M., Foddai, M., Rourke, J.P., Chessa, M., Pintore, G.: Chemical characterization, antioxidant capacity and antimicrobial activity against food related microorganisms of Citrus limon var. pompia leaf essential oil. LWT-Food Sci. Technol. 69, 579–585 (2016)
Ganeshpurkar, A., Saluja, A.K.: The pharmacological potential of rutin. Saudi Pharm. J. 25(2), 149–164 (2017)
Gao, X., Ohlander, M., Jeppsson, N., Björk, L., Trajkovski, V.: Changes in antioxidant effects and their relationship to phytonutrients in fruits of sea buckthorn (Hippophaer hamnoides L.) during maturation. J. Agric. Food Chem. 48, 1485–1490 (2000)
Gómez-Mejía, E., Rosales-Conrado, N., León-González, M.E., Madrid, Y.: Citrus peels waste as a source of value-added compounds: extraction and quantification of bioactive polyphenols. Food Chem. 295, 289–299 (2019)
Hafsa, J., Smach, M.A., Ben Khedher, M.R., Charfeddine, B., Limem, K., Majdoub, H., Rouatbi, S.: Physical, antioxidant and antimicrobial properties of chitosan films containing eucalyptus globulus essential oil. LWT Food Sci. Technol. 68, 356–364 (2016)
Hanato, T., Kagawa, H., Yasuhara, T., Okuda, T.: Two new flavonoids and other constituents in licorice root: their relative astringency and radical scavenging effects. Chem. Pharm. Bull. 36(6), 2090–2097 (1988)
Lamine, M., Rahali, F.Z., Hamdaoui, G., Selmi, S., Mliki, A., Gargouri, M.: Associating chemical analysis to molecular markers for the valorization of citrus aurantium leaves: a useful starting point for marker-assisted selection. Euphytica 213, 1–14 (2017)
Lamine, M., Rahali, F.Z., Hammami, M., Mliki, A.: Correlative metabolite profiling approach to understand antioxidant and antimicrobial activities from citrus essential oils. Int. J. Food Sci. Technol. (2019). https://doi.org/10.1111/ijfs.14173
Leeuw, R.W., Kevers, C., Pincemail, J., Defraigne, J.O., Dommes, J.: Antioxidant capacity and phenolic composition of red wines from various grape varieties: specificity of Pinot Noir. J. Food Compos. Anal. 36, 40–50 (2014)
Leporini, M., Tundis, R., Sicari, V., et al.: Impact of extraction processes on phytochemicals content and biological activity of citrus × clementina hort Ex tan leaves: new opportunity for under-utilized food by-products. Food Res. Int. 127, 108742 (2020). https://doi.org/10.1016/j.foodres.2019.108742
Li, S.M., Lo, C.Y., Ho, C.T.: Hydroxylated polymethoxyfavones and methylated favonoids in sweet orange (Citrus sinensis) peel. J Agr. Food Chem. 54(12), 4176–4185 (2006)
Loizzo, M.R., Tundis, R., Bonesi, M., Di Sanzo, G., Verardi, A., Lopresto, C.G., et al.: Chemical profile and antioxidant properties of extracts and essential oils from Citrus × limon (L.) BURM. cv femminello comune. Chem. Biodivers. 13, 571–581 (2016)
Loizzo, M.R., Leporini, M., Sicari, V., Falco, T., Pellicanò, M.T., Tundis, R.: Investigating the in vitro hypoglycaemic and antioxidant properties of Citrus × clementina Hort. juice. Eur. Food Res. Technol. 244, 523–534 (2018)
Loizzo, M.R., Sicari, V., Tundis, R., Leporini, M., Falco, T., Calabrò, V.: The influence of ultrafiltration of Citrus limon L. Burm. cv femminello comune juice on its chemical composition and antioxidant, and hypoglycaemic properties. Antioxidants 8, 23 (2019)
Lv, X., Zhao, S., Ning, Z., Zeng, H., Shu, Y., Tao, O., et al.: Citrus fruits as a treasure trove of active natural metabolites that potentially provide benefits for human health. Chem. Cent. J. 9, 68 (2015)
Mahato, N., Sharma, K., Sinha, M., Cho, M.H.: Citrus waste derived nutra-/ pharmaceuticals for health benefits: current trends and future perspectives. J. Funct. Foods 40, 307–316 (2018)
Martillanes, S., Rocha-Pimienta J., Cabrera-Bañegil M., Martín-Vertedor D., Delgado-Adámez J., 2017 Application of phenolic compounds for food preservation: food additive and active packaging, Phenolic Compounds - Biological Activity, Marcos Soto-Hernandez, Mariana Palma-Tenango and Maria del Rosario Garcia-Mateos, IntechOpen, DOI: 10.5772/66885
Oikeh, E.I., Oviasogie, F.E., Omoregie, E.S.: Quantitative phytochemical analysis and antimicrobial activities of fresh and dry ethanol extracts of Citrus sinensis (L.) Osbeck (sweet Orange) peels. Clin. Phytosci. 6, 46 (2020a)
Oikeh, E.I., Oviasogie, F.E., Omoregie, E.S.: Evaluation of antimicrobial efficacy of ethanol extracts of fresh citrus sinensis (sweet orange) seeds against selected bacterial strains. J. Appl. Sci. Environ. Manage. 24(2), 249–252 (2020b). https://doi.org/10.4314/jasem.v24i2.9
Orhan, F., Çeker, S., Anar, M., et al.: Protective effects of three luteolin derivatives on aflatoxin B1-induced genotoxicity on human blood cells. Med. Chem. Res. 25, 2567–2577 (2016)
Osorio-Esquivel, O., Moreno, A.O., Alvarez, V.B., Dorantes-Alvarez, L., Giusti, M.M.: Phenolics, betacyanins and antioxidant activity in opuntia joconostle fruits. Food Res. Int. 44(7), 2160–2168 (2011)
Pellegrini, N., Re, R., Yang, M., Rice-Evans, C.A.: Screening of dietary carotenoids and carotenoid-rich fruit extracts for antioxidant activities applying 2,2’-azinobis (3-ethylenebenzothiazoline-6-sulfonic acid) radical cation decolorization. Meth. Enzymol. 299, 379–389 (1999)
Ríos, J.L., Recio, M.C.: Medicinal plants and antimicrobial activity. J. Ethnopharm. 100, 80–84 (2005)
Satari, B., Karimi, K.: Citrus processing wastes: Environmental impacts, recent advances, and future perspectives in total valorization. Resour. Conserv. Recycl. 129, 153–167 (2018)
Schelz, Z., Molnar, J., Hohmann, J.: Antimicrobial and antiplasmid activities of essential oils. Fitoterapia 77(4), 279–285 (2006). https://doi.org/10.1016/j.fitote.2006.03.013
Semwal, D.K., Semwal, R.B., Combrinck, S., Viljoen, A.: Myricetin: a dietary molecule with diverse biological activities. Nutrients 8(2), 90 (2016)
Song, Y.S., Mu, P.C.: Luteolin and luteolin-7-O-glucoside strengthen antioxidative potential through the modulation of Nrf2/MAPK mediated HO-1 signaling cascade in RAW 264.7 cells. Food Chem. Toxicol. 65, 70–75 (2014)
Sun, T., Tanumihardjo, S.A.: An integrated approach to evaluate food antioxidant capacity. J. Food Sci. 72, 159–165 (2007)
Tundis, R., Bonesi, M., Sicari, V., Pellicanò, T.M., Tenuta, M.C., Leporini, M., et al.: Poncirus trifoliata (L.) Raf.: chemical composition, antioxidant properties and hypoglycaemic activity via the inhibition of α-amylase and α-glucosidase enzymes. J. Funct. Foods 25, 477–485 (2016)
Tung, Y.C., Chou, Y.C., Hung, W.L., Cheng, A.C., Yu, R.C., Ho, C.T., Pan, M.H.: Polymethoxyflavones: chemistry and molecular mechanisms for cancer prevention and treatment. Curr. Pharmacol. Rep. 5(2), 98–113 (2019)
Veldhuizen, E.J., Tjeerdsma-van Bokhoven, J.L., Zweijtzer, C., Burt, S.A., Haagsman, H.P.: Structural requirements for the antimicrobial activity of carvacrol. J. Agr. Food Chem. 54, 1874–1879 (2006)
Wang, S., Yang, C., Tu, H., et al.: Characterization and metabolic diversity of flavonoids in Citrus Species. Sci. Rep. 7, 10549 (2017)
Wang, S., Tu, H., Wan, J., Chen, W., Liu, X., Luo, J., Xu, J., Zhang, H.: Spatio-temporal distribution and natural variation of metabolites in citrus fruits. Food Chem. 199, 8–17 (2016)
Willcox, J.K., Ash, S.L., Catignani, G.L.: Antioxidants and prevention of chronic disease. Crit. Rev. Food Sci. Nutr. 44, 275–295 (2004)
Xi, W., Lu, J., Qun, J., Jiao, B.: Characterization of phenolic profile and antioxidant capacity of different fruit part from lemon (Citrus limon Burm) cultivars. J. Food Sci. Technol. 54(5), 1108–1118 (2017)
Xia, J., Wishart, D.S.: Web-based inference of biological patterns, functions and pathways from metabolomic data using metaboanalyst. Nat. Protoc. 6(6), 743–760 (2011)
Zema, D.A., Calabrò, P., Fòlino, A., Tamburino, V., Zappia, G., Zimbone, S.M.: Valorisation of citrus processing waste: a review. Waste Manage. 80, 252–273 (2018)
Acknowledgements
This work was supported by the Tunisian Ministry of Higher Education and Scientific Research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lamine, M., Gargouri, M., Rahali, F.Z. et al. Recovering and Characterizing Phenolic Compounds From Citrus By-Product: A Way Towards Agriculture of Subsistence and Sustainable Bioeconomy. Waste Biomass Valor 12, 4721–4731 (2021). https://doi.org/10.1007/s12649-020-01306-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-020-01306-9