Evaluation of antioxidant activity of the fermented product from the biotransformation of R-(+)-limonene in solid-state fermentation of orange waste by Diaporthe sp.
Mário César Jucoski Bier, Adriane Bianchi Pedroni Medeiros, Norbert De Kimpe, Carlos Ricardo Soccol
Abstract
Through solid-state fermentation, the endophytic fungus Diaporthe sp. biotransformed the compound R-(+)-limonene, a great quantity of which is present in orange waste. The fermented orange waste was evaluated to determine its antioxidant potential. Mass spectrometry identified several biotransformation products, which were quantified by gas chromatography. The fermentation process yielded compounds such as limonene-1,2-diol, α-terpineol, (−)-carvone, α-tocopherol, dihydrocarveol and valencene, most of which have already been associated with antioxidant activity. The highest concentration of limonene-1,2-diol produced was 3.02 g/kg of dry substrate and 0.72 g/kg of α-terpineol. The DPPH, ORAC and CUPRAC methods were employed to analyze the antioxidant activity comparing the orange waste and the fermented orange waste. According to the results obtained using the DPPH method, the fermented media extract represented 20.17% of antioxidant activity, compared to 12.1% of the orange waste extract, while from the ORAC method analysis the results were 24,011.39 μmolTE/g, obtained from the fermented extract in comparison to 5226.45 μmolTE/g from the orange waste. The results from the CUPRAC method analysis were 538.05 mg TE/g of dry extract, from the fermented extract in comparison to 168.27 TE/g of dry extract, from the orange waste. These results prove that the fermentation process increased the antioxidant potential of the orange waste.
Keywords
References
Adams et al., 2003
A. Adams, J.C.R. Demyttenaere, N. De Kimpe
Biotransformation of (R)-(+)- and (S)-(−)-limonene to α-terpineol by Penicillium digitatum – Investigation of the culture conditions
Food Chemistry, 80 (2003), pp. 525-534
Apak et al., 2007
R. Apak, K. Güçlü, B. Demirata, M. Özyürek, S.E. Çelik, B. Bektaşoğlu, et al.
Comparative evaluation of various total antioxidant capacity assays applied to phenolic compounds with the CUPRAC assay
Molecules, 12 (2007), pp. 1496-1547
Arce et al., 2007
A. Arce, A. Pobudkowskal, O. Rodríguez, O. Soto
Citrus essential oil terpenless by extraction using 1-ethyl-3-methylimidazolium ethylsulfate ionic liquid: Effect of the temperature
Chemical Engineering Journal, 133 (2007), pp. 213-218, 10.1016/j.cej.2007.01.035
Assefa et al., 2016
A.D. Assefa, E.Y. Ko, S.H. Moon, Y.-S. Keum
Antioxidant and antiplatelet activities of flavonoid-rich fractions of three citrus fruits from Korea
3 Biotech, 6 (2016), pp. 1-10
Bacanli et al., 2015
M. Bacanli, A.A. Basaran, N. Basaran
The antioxidant and antigenotoxic properties of citrus phenolics limonene and naringin
Food and Chemical Toxicology, 81 (2015), pp. 160-170
Badee et al., 2011
A.Z.M. Badee, S.A. Helmy, N.F.S. Morsy
Utilisation of orange peel in the production of α-terpineol by Penicillium digitatum (NRRL 1202)
Food Chemistry, 126 (2011), pp. 849-854
Bier et al., 2011
M.C.J. Bier, S. Poletto, V.T. Soccol, C.R. Soccol, A.B.P. Medeiros
Isolation and screening of microorganisms with potential for biotransformation of terpenic substrates
Brazilian Archives of Biology and Technology, 54 (2011), pp. 1019-1026
Bier et al., 2016
M.C.J. Bier, A.B.P. Medeiros, J.S. De Oliveira, L.C. Côcco, J.L. Costa, C.R. Soccol
Liquefied gas extraction: A new method for the recovery of terpenoids from agroindustrial and forest wastes
The Journal of Supercritical Fluids, 110 (2016), pp. 97-102
Burdock, 2010
G.A. Burdock
Fenaroli's handbook of flavor ingredients
CRC Press, Boca Raton (2010), p. 2159
Carvalho and Fonseca, 2006
C.C.R. Carvalho, M.M.R. Fonseca
Biotransformation of terpenes
Biotechnology Advances, 24 (2006), pp. 134-142
Chen et al., 2012
Z.T. Chen, H.L. Chu, C.C. Chyau, C.C. Chu, P.D. Duh
Protective effects of sweet orange (Citrus sinensis) peel and their bioactive compounds on oxidative stress
Food Chemistry, 135 (2012), pp. 2119-2127
Crizel et al., 2013
T.M. Crizel, A. Jablonski, A.O. Rios, R. Rech, S.H. Flôres
Dietary fiber from orange byproducts as a potential fat replacer
LWT – Food Science Technology, 53 (2013), pp. 9-14, 10.1016/j.lwt.2013.02.002
Demyttenaere et al., 2001
J.C.R. Demyttenaere, K.V. Belleghem, N. De Kimpe
Biotransformation of (R)-(+)- and (S)-(−)-limonene by fungi and the use of solid phase microextraction for screening
Phytochemistry, 57 (2001), pp. 199-208
Demyttenaere and De Kimpe, 2001
J.C.R. Demyttenaere, N. De Kimpe
Biotransformation of terpenes by fungi: Study of the pathways involved
Journal of Molecular Catalysis B-Enzymatic, 11 (2001), pp. 265-270
El-Akhal et al., 2015
F. El-Akhal, A.E.O. Lalami, R. Guemmouh
Larvicidal activity of essential oils of Citrus sinensis and Citrus aurantium (Rutaceae) cultivated in Morocco against the malaria vector Anopheles labranchiae (Diptera: Culicidae)
Asian Pacific Journal of Tropical Disease, 5 (2015), pp. 458-462
Gosslau et al., 2014
A. Gosslau, K.Y. Chen, C. Ho, S. Li
Anti-inflammatory effects of characterized orange peel extracts enriched with bioactive polymethoxyflavones
Food Science and Human Wellness, 3 (2014), pp. 26-35
IAL, 2008
IAL
Normas Analíticas do Instituto Adolfo Lutz
Instituto Adolfo Lutz, São Paulo (2008), p. 1020
Jayaprakasha et al., 2008
G.K. Jayaprakasha, B. Girennavar, B.S. Patil
Antioxidant capacity of pummelo and navel oranges: Extraction efficiency of solvents in sequence
LWT – Food Science and Technology, 41 (2008), pp. 376-384
Kaur and Kaur, 2015
J. Kaur, G. Kaur
An insight into the role of citrus bioactives in modulation of colon cancer
Journal of Functional Foods, 13 (2015), pp. 239-261
Liu et al., 2012
K. Liu, Q. Chen, Y. Liu, X. Zhou, X. Wang
Isolation and biological activities of decanal, linalool, valencene, and octanal from sweet orange oil
Journal of Food Science, 77 (2012), pp. 1156-1161
Lu et al., 2012
Y. Lu, S. Zhao, J. Zhang, H. Zhang, Z. Xie, G. Cai, et al.
Effect of orange peel essential oil on oxidative stress in AOM animals
International Journal of Biological Macromolecules, 50 (2012), pp. 1144-1150
Malhotra et al., 2009
S. Malhotra, S. Suri, R. Tuli
Antioxidant activity of citrus cultivars and chemical composition of Citrus karna essential oil
Planta Medica, 75 (2009), pp. 62-64
Mantzouridou et al., 2015
F.T. Mantzouridou, A. Paraskevopoulou, S. Lalou
Yeast flavour production by solid state fermentation of orange peel waste
Biochemical Engineering Journal, 101 (2015), pp. 1-8
Maróstica Júnior and Pastore, 2007a
M.R. Maróstica Júnior, G.M. Pastore
Production of R-(+)-α-terpineol by the biotransformation of limonene from orange essential oil, using cassava waste water as medium
Food Chemistry, 101 (2007), pp. 345-350
Maróstica Júnior and Pastore, 2007b
M.R. Maróstica Júnior, G.M. Pastore
Biotransformation of limonene: A review of the main metabolic pathways
Química Nova, 30 (2007), pp. 382-387
Molina et al., 2013
G. Molina, D.M. Pinheiro, M.R. Pimentel, R. Dos Sanros, G.M. Pastore
Monoterpene bioconversion for the production of aroma compounds by fungi isolated from Brazilian fruits
Food Science and Biotechnology, 22 (2013), pp. 999-1006
Murthy et al., 2012
K.N.C. Murthy, G.K. Jayaprakasha, B.S. Patil
D-limonene rich volatile oil from blood oranges inhibits angiogenesis, metastasis and cell death in human colon cancer cell
Life Science, 91 (2012), pp. 429-439
NIST, 2014
NIST, National Institute of Standards and Technology
Mass Spectral Library and Search Software v.2.2 (NIST 2014/EPA/NIH)
(2014), p. 72
Gaithersburg, MD
Pandey, 2003
A. Pandey
Solid state fermentation
Biochemical Engineering Journal, 13 (2003), pp. 81-88
Pourbafrani et al., 2010
M. Pourbafrani, G. Forgács, I.S. Horváth, C. Niklasson, M.J. Taherzadeh
Production of biofuels, limonene and pectin from citrus wastes
Bioresource Technology, 101 (2010), pp. 4246-4250
Qadri et al., 2015
M. Qadri, R. Deshidi, B.A. Shah, K. Bindu, R.A. Vishwakarma, S. Riyaz-Ul-Hassan
An endophyte of Picrorhiza kurroa Royle ex. Benth, producing menthol, phenylethyl alcohol and 3-hydroxypropionic acid, and other volatile organic compounds
World Journal of Microbiology and Biotechnology, 31 (2015), pp. 1647-1654
Santi et al., 2010
G. Santi, S. Crognale, A. D’Annibale, M. Petruccioli, M. Ruzzi, R. Valentini, et al.
Orange peel pretreatment in a novel lab-scale direct steam-injection apparatus for ethanol production
Biomass and Bioenergy, 61 (2010), pp. 146-156
Sarrou et al., 2013
E. Sarrou, P. Chatzopoulou, K. Dimassi-Theriou, L. Therios
Volatile constituents and antioxidant activity of peel, flowers and leaf oils of Citrus aurantium L. growing in Greece
Molecules, 18 (2013), pp. 10639-10647
Soccol et al., 2014
C.R. Soccol, A.B.P. Medeiros, M.C.J. Bier
Bioprocesso para a produção de derivados de terpenos por Diaporthe sp. e Rhodotorula mucilaginosa
Brazilian Patent (2014)
INPI BR 102014029813.
Song et al., 2010
F.L. Song, R.Y. Gan, Y. Zhang, Q. Xiao, L. Kuang, H.B. Li
Total phenolic contents and antioxidant capacities of selected Chinese medicinal plants
International Journal of Molecular Sciences, 11 (2010), pp. 2362-2372
USDA, 2018
USDA, United States Department of Agriculture
Citrus: World markets and trade
Foreign Agricultural Service, Washington (2018), p. 13
Velázquez-Nuñez et al., 2013
M.J. Velázquez-Nuñez, R. Avila-Sosa, E. Palou, A. López-Malo
Antifungal activity of orange (Citrus sinensis var. Valencia) peel essential oil applied by direct addition or vapor contact
Food Control, 31 (2013), pp. 1-4
Wang and Dai, 2011
Y. Wang, C.C. Dai
Endophytes: A potential resource for biosynthesis, biotransformation, and biodegradation
Annals of Microbiology, 61 (2011), pp. 207-215
Yang et al., 2013
F.C. Yang, T.W. Ma, Y.H. Lee
Reuse of citrus peel to enhance the formation of bioactive metabolite-triterpenoid in solid-state fermentation of A. cinnamomea
Biochemical Engineering Journal, 78 (2013), pp. 59-66
Zulueta et al., 2007
A. Zulueta, M.J. Esteve, A. Frígola
ORAC and TEAC assays comparison to measure the antioxidant capacity of food products
Food Chemistry, 114 (2007), pp. 310-316