The Effect of Lactobacillus plantarum ATCC 8014 and Lactobacillus acidophilus NCFM Fermentation on Antioxidant Properties of Selected in Vitro Sprout Culture of Orthosiphon aristatus (Java Tea) as a Model Study
High rosmarinic acid ( RA) productivity has been achieved by applying jasmonic acid and yeast extract elicitors to the in vitro sprout culture of Orthosiphon aritatus ( IOSC). The highest RA accumulation from three solvents was detected in IOSC after treatment with yeast extract (5 g/L). HPLC analysis clearly confirmed a drastic increase in RA subjected to yeast extract elicitation. Therefore, this yeast extract elicited IOSC was chosen for a lactic acid bacteria ( LAB) fermentation study as a model system. This selected IOSC was subjected to different types of LAB fermentations ( Lactobacillus plantarum ATCC 8014 and Lactobacillus acidophilus NCFM) for different periods of time 24, 48 and 72 h. The LAB fermentations consisted of solid state fermentations ( SSF) and liquid state fermentations ( LSF) in a Digital Control Unit ( DCU) fermenter system. The aim was to determine the effect of fermentation on the antioxidant properties of the plant extract. Results indicated that all types of LAB fermentation decreased the level of RA and total phenolics, however, a slight increase in total flavonoids and flavonols was observed in SSF samples. HPLC results confirmed that the longer the fermentation, the greater the reduction in RA content. The highest reduction was obtained in the sample of LSF inoculated with L. plantarum for a period of 72 h. The temperature of fermentation (37 °C) was predicted as contributing to the declining level in RA content. The loss in RA was concomitant with a loss of total antioxidant activity (1,1-diphenyl-2-picrylhydrazyl ( DPPH) scavenging activity, Trolox Equivalent Antioxidant Capacity ( TEAC), and Superoxide Dismutase ( SOD)-like activity). These results indicate that RA is the major contributor to the antioxidant activity of this plant.
References
[1]
Park, S.U.; Uddin, M.R.; Xu, H.; Kim, Y.K.; Lee, S.Y. Biotechnological applications for rosmarinic acid production in plant. Afr. J. Biotechnol. 2008, 7, 4959–4965.
[2]
Petersen, M.; Simmonds, M.S.J. Rosmarinic acid. Phytochemistry 2003, 62, 121–125.
[3]
Akowuah, G.A.; Ismail, Z.; Norhayati, I.; Sadikun, A. The effects of different extraction solvents of varying polarities on polyphenols of Orthosiphon stamineus and evaluation of the free radical-scavenging activity. Food Chem. 2005, 93, 311–317, doi:10.1016/j.foodchem.2004.09.028.
[4]
Fadhlina, A. The Effects of Temperature and Fermentation Time on Selected Cchemical Composition, Antioxidant and Quality of Cat Whiskers (Orthosiphon stamineus) Tea; University Sains Malaysia: Pulau Pinang, Malaysia, 2008.
[5]
Shevchenko, Y.; Smetanska, I.; Wendt, A. Sprout culture of Stevia rebaudiana Bertoni. In Stevia Science; Euprint: Heverlee, Belgium, 2010; pp. 5–26.
[6]
Cai, Z. Effects Elicitors on Secondary Metabolism of Plant Suspension Cultures of Vitis vinifera and Malus domestica and their Exudates; Berlin University of Technology: Berlin, Germany, 2012.
[7]
Sumaryono, W.; Proksch, P.; Hartmann, T.; Nimtz, M.; Wray, V. Induction of rosmarinic acid accumulation in cell suspension cultures of Orthosiphon aristatus after treatment with yeast extract. Phytochemistry 1991, 30, 3267–3271, doi:10.1016/0031-9422(91)83190-V.
[8]
Mewis, I.; Smetanska, I.; Müller, C.; Ulrichs, C. Specific poly-phenolic compounds in cell culture of Vitis vinifera L. cv. Gamay Fréaux. Appl. Biochem. Biotechnol. 2011, 164, 148–161, doi:10.1007/s12010-010-9122-x.
[9]
Dordevic, T.M.; Siler-Marinkovic, S.S.; Dimitrijevic-Brankovic, S.I. Effect of fermentation on antioxidant properties of some cereals and pseudo cereals. Food Chem. 2010, 119, 957–963, doi:10.1016/j.foodchem.2009.07.049.
[10]
Maifreni, M.; Marino, M.; Conte, L. Lactic acid fermentation of Brassica rapa: Chemical and microbial evaluation of a typical Italian product (brovada). Eur. Food Res. Technol. 2004, 218, 469–473, doi:10.1007/s00217-004-0877-6.
[11]
Katina, K.; Laitila, A.; Juvonen, R.; Liukkonen, K.H.; Kariluoto, S.; Piironen, V.; Landberg, R.; Aman, P.; Poutanen, K. Bran fermentation as a means to enhance technological properties and bioactivity of rye. Food Microbiol. 2007, 24, 175–186, doi:10.1016/j.fm.2006.07.012.
[12]
Katina, K.; Liukkonen, K.H.; Kaukovirta-Norja, A.; Adlercreutz, H.; Heinonen, S.M.; Lampi, A.M.; Pihlava, J.M.; Poutanen, K. Fermentation-induced changes in the nutritional value of native or germinated rye. J. Cereal Sci. 2007, 46, 348–355, doi:10.1016/j.jcs.2007.07.006.
[13]
Sun, Y.-P.; Chou, C.-C.; Yu, R.-C. Antioxidant activity of lactic-fermented Chinese cabbage. Food Chem. 2009, 115, 912–917, doi:10.1016/j.foodchem.2008.12.097.
[14]
Zhao, D.; Ding, X. Studies on the low-salt Chinese potherb mustard (Brassica juncea, Coss.) pickle. I-The effect of a homofermentative L(+)-lactic acid producer Bacillus coagulans on starter culture in the low-salt Chinese potherb mustard pickle fermentation. LWT-Food Sci. Technol. 2008, 41, 474–482, doi:10.1016/j.lwt.2007.03.023.
[15]
Liu, J.-G.; Hou, C.-W.; Lee, S.-Y.; Chuang, Y.; Lin, C.-C. Antioxidant effects and UVB protective activity of Spirulina (Arthrospira platensis) products fermented with lactic acid bacteria. Process Biochem. 2011, 46, 1405–1410, doi:10.1016/j.procbio.2011.03.010.
[16]
Martinez-Villaluenga, C.; Pe？as, E.; Sidro, B.; Ullate, M.; Frias, J.; Vidal-Valverde, C. White cabbage fermentation improves ascorbigen content, antioxidant and nitric oxide production inhibitory activity in LPS-induced macrophages. LWT-Food Sci. Technol. 2012, 46, 77–83, doi:10.1016/j.lwt.2011.10.023.
[17]
Cai, S.; Wang, O.; Wu, W.; Zhu, S.; Zhou, F.; Ji, B.; Gao, F.; Zhang, D.; Liu, J.; Cheng, Q. Comparative study of the effects of solid-state fermentation with three filamentous fungi on the Total Phenolics Content (TPC), flavonoids, and antioxidant activities of subfractions from Oats (Avena sativa L.). J. Agr. Food Chem. 2011, 60, 507–513.
[18]
Cho, K.M.; Lee, J.H.; Yun, H.D.; Ahn, B.Y.; Kim, H.; Seo, W.T. Changes of phytochemical constituents (isoflavones, flavanols, and phenolic acids) during cheonggukjang soybeans fermentation using potential probiotics Bacillus subtilis CS90. J. Food Compos. Anal. 2011, 24, 402–410, doi:10.1016/j.jfca.2010.12.015.
[19]
Ng, C.-C.; Wang, C.-Y.; Wang, Y.-P.; Tzeng, W.-S.; Shyu, Y.-T. Lactic acid bacterial fermentation on the production of functional antioxidant herbal Anoectochilus formosanus Hayata. J. Biosci. Bioeng. 2011, 111, 289–293, doi:10.1016/j.jbiosc.2010.11.011.
[20]
Wu, S.-C.; Su, Y.-S.; Cheng, H.-Y. Antioxidant properties of Lactobacillus-fermented and non-fermented Graptopetalum paraguayense E. Walther at different stages of maturity. Food Chem. 2011, 129, 804–809, doi:10.1016/j.foodchem.2011.05.025.
[21]
He, X.; Zou, Y.; Yoon, W.-B.; Park, S.-J.; Park, D.-S.; Ahn, J. Effects of probiotic fermentation on the enhancement of biological and pharmacological activities of Codonopsis lanceolata extracted by high pressure treatment. J. Biosci. Bioeng. 2011, 112, 188–193, doi:10.1016/j.jbiosc.2011.04.003.
[22]
Wang, N.-F.; Yan, Z.; Li, C.-Y.; Jiang, N.; Liu, H.-J. Antioxidant activity of peanut flour fermented with Lactic Acid Bacteria. J. Food Biochem. 2011, 35, 1514–1521, doi:10.1111/j.1745-4514.2010.00473.x.
[23]
Alberto, M.R.; Farías, M.E.; Manca de Nadra, M.C. Effect of gallic acid and catechin on Lactobacillus hilgardii 5w growth and metabolism of organic compounds. J. Agr. Food Chem. 2001, 49, 4359–4363, doi:10.1021/jf0101915.
[24]
Sunny-Roberts, E.O. Application of Disaccarides Pre-Treatment in Improving Tolerances of Lactobacillus rhamnosus Strains to Environmental Stresses or during Vacuum- and Spray Drying Processes; Berlin University of Technology: Berlin, Germany, 2009.
[25]
Mohdaly, A.A.; Sarhan, M.A.; Smetanska, I.; Mahmoud, A. Antioxidant properties of various solvent extracts of potato peel, sugar beet pulp and sesame cake. J. Sci. Food Agr. 2010, 90, 218–226, doi:10.1002/jsfa.3796.
[26]
Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biol. Med. 1999, 26, 1231–1237, doi:10.1016/S0891-5849(98)00315-3.
[27]
Debnath, T.; Park, P.-J.; Deb Nath, N.C.; Samad, N.B.; Park, H.W.; Lim, B.O. Antioxidant activity of Gardenia jasminoides Ellis fruit extracts. Food Chem. 2011, 128, 697–703, doi:10.1016/j.foodchem.2011.03.090.
Lee, I.H.; Hung, Y.-H.; Chou, C.-C. Solid-state fermentation with fungi to enhance the antioxidative activity, total phenolic and anthocyanin contents of black bean. Int. J. Food Microbiol. 2008, 121, 150–156, doi:10.1016/j.ijfoodmicro.2007.09.008.
[30]
Azlim Almey, A.A.; Ahmed Jalal Khan, C.; Syed Zahir, I.; Mustapha Suleiman, K.; Aisyah, M.R.; Kamarul Rahim, K. Total phenolic content and primary antioxidant activity of methanolic and ethanolic extracts of aromatic plants’ leaves. Int. Food Res. J. 2010, 17, 1077–1084.
[31]
Ogata, A.; Tsuruga, A.; Matsuno, M.; Mizukami, H. Elicitor-induced rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures: Activities of rosmarinic acid synthase and the final two cytochrome P450-catalyzed hydroxylations. Plant Biotechnol. 2004, 21, 393–396, doi:10.5511/plantbiotechnology.21.393.
[32]
Kim, H.K.; Oh, S.-R.; Lee, H.-K.; Huh, H. Benzothiadiazole enhances the elicitation of rosmarinic acid production in a suspension culture of Agastache rugosa O. Kuntze. Biotechnol. Lett. 2001, 23, 55–60, doi:10.1023/A:1026738409671.
[33]
Mizukami, H.; Ogawa, T.; Ohashi, H.; Ellis, B.E. Induction of rosmarinic acid biosynthesis in Lithospermum erythrorhizon cell suspension cultures by yeast extract. Plant Cell Rep. 1992, 11, 480–483.
[34]
G？nzle, M.G.; Ehmann, M.; Hammes, W.P. Modeling of growth of Lactobacillus sanfranciscensis and Candida milleri in response to process parameters of sourdough fermentation. Appl. Environ. Microbiol. 1998, 64, 2616–2623.
[35]
Cuppers, H.G.A.M.; Smelt, J.P.P.M. Time to turbidity measurement as a tool for modeling spoilage by Lactobacillus. J. Ind. Microbiol. Biotechnol. 1993, 12, 168–171.
[36]
Chen, C.-P.; Lin, C.-C.; Tsuneo, N. Screening of Taiwanese crude drugs for antibacterial activity against Streptococcus mutans. J. Ethnopharmacol. 1989, 27, 285–295, doi:10.1016/0378-8741(89)90003-2.
[37]
Puupponen-Pimi？, R.; Nohynek, L.; Meier, C.; K？hk？nen, M.; Heinonen, M.; Hopia, A.; Oksman-Caldentey, K.M. Antimicrobial properties of phenolic compounds from berries. J. Appl. Microbiol. 2001, 90, 494–507, doi:10.1046/j.1365-2672.2001.01271.x.
[38]
Doblado, R.; Zielinski, H.; Piskula, M.; Kozlowska, H.; Munoz, R.; Frias, J.; Vidal-Valverde, C. Effect of processing on the antioxidant vitamins and antioxidant capacity of Vigna sinensis Var. Carilla. J. Agr. Food Chem. 2005, 53, 1215–1222, doi:10.1021/jf0492971.
[39]
Fang, Z.; Hu, Y.; Liu, D.; Chen, J.; Ye, X. Changes of phenolic acids and antioxidant activities during potherb mustard (Brassica juncea, Coss.) pickling. Food Chem. 2008, 108, 811–817, doi:10.1016/j.foodchem.2007.11.033.
[40]
Othman, N.B.; Roblain, D.; Chammen, N.; Thonart, P.; Hamdi, M. Antioxidant phenolic compounds loss during the fermentation of Chétoui olives. Food Chem. 2009, 116, 662–669, doi:10.1016/j.foodchem.2009.02.084.
[41]
Juan, M.-Y.; Chou, C.-C. Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food Microbiol. 2010, 27, 586–591, doi:10.1016/j.fm.2009.11.002.
[42]
Chandrasekara, A.; Shahidi, F. Bioaccessibility and antioxidant potential of millet grain phenolics as affected by simulated in vitro digestion and microbial fermentation. J. Funct. Foods 2012, 4, 226–237, doi:10.1016/j.jff.2011.11.001.
[43]
Singh, H.B.; Singh, B.N.; Singh, S.P.; Nautiyal, C.S. Solid-state cultivation of Trichoderma harzianum NBRI-1055 for modulating natural antioxidants in soybean seed matrix. Bioresource Technol. 2010, 101, 6444–6453, doi:10.1016/j.biortech.2010.03.057.
[44]
Cho, K.M.; Hong, S.Y.; Math, R.K.; Lee, J.H.; Kambiranda, D.M.; Kim, J.M.; Islam, S.M.A.; Yun, M.G.; Cho, J.J.; Lim, W.J.; Yun, H.D. Biotransformation of phenolics (isoflavones, flavanols and phenolic acids) during the fermentation of cheonggukjang by Bacillus pumilus HY1. Food Chem. 2009, 114, 413–419, doi:10.1016/j.foodchem.2008.09.056.
[45]
Rodriguez, H.; Curiel, J.A.; Landete, J.M.; de las Rivas, B.; de Felipe, F.L.; Gomez-Cordoves, C.; Mancheno, J.M.; Munoz, R. Food phenolics and lactic acid bacteria. Int. J. Food Microbiol. 2009, 132, 79–90, doi:10.1016/j.ijfoodmicro.2009.03.025.
[46]
Fernandez-Orozco, R.; Frias, J.; Mu？oz, R.; Zielinski, H.; Piskula, M.; Kozlowska, H.; Vidal-Valverde, C. Effect of fermentation conditions on the antioxidant compounds and antioxidant capacity of Lupinus angustifolius cv. zapaton. Eur. Food Res. Technol. 2008, 227, 979–988, doi:10.1007/s00217-007-0809-3.
[47]
Frias, J.; Miranda, M.L.; Doblado, R.; Vidal-Valverde, C. Effect of germination and fermentation on the antioxidant vitamin content and antioxidant capacity of Lupinus albus L. var. Multolupa. Food Chem. 2005, 92, 211–220, doi:10.1016/j.foodchem.2004.06.049.
[48]
Torres, A.; Frias, J.; Granito, M.; Vidal-Valverde, C. Fermented pigeon pea (Cajanus cajan) ingredients in pasta products. J. Agr. Food Chem. 2006, 54, 6685–6691, doi:10.1021/jf0606095.
[49]
Fernandez-Orozco, R.; Frias, J.; Mu？oz, R.; Zielinski, H.; Piskula, M.K.; Kozlowska, H.; Vidal-Valverde, C. Fermentation as a bio-process to obtain functional soybean flours. J. Agr. Food Chem. 2007, 55, 8972–8979, doi:10.1021/jf071823b.
[50]
Chang, C.T.; Hsu, C.K.; Chou, S.T.; Chen, Y.C.; Huang, F.S.; Chung, Y.C. Effect of fermentation time on the antioxidant activities of tempeh prepared from fermented soybean using Rhizopus oligosporus. Int. J. Food Sci. Technol. 2009, 44, 799–806, doi:10.1111/j.1365-2621.2009.01907.x.
[51]
Landete, J.M.; Rodríguez, H.; De Las Rivas, B.; Mu？oz, R. High-added-value antioxidants obtained from the degradation of wine phenolics by Lactobacillus plantarum. J. Food Protect. 2007, 70, 2670–2675.
[52]
Jamal, P.; Idris, Z.M.; Alam, M.Z. Effects of physicochemical parameters on the production of phenolic acids from palm oil mill effluent under liquid-state fermentation by Aspergillus niger IBS-103ZA. Food Chem. 2011, 124, 1595–1602, doi:10.1016/j.foodchem.2010.08.022.
[53]
Hegde, S.; Kavitha, S.; Varadaraj, M.C.; Muralikrishna, G. Degradation of cereal bran polysaccharide-phenolic acid complexes by Aspergillus niger CFR 1105. Food Chem. 2006, 96, 14–19, doi:10.1016/j.foodchem.2005.01.050.
[54]
Justesen, U.; Arrigoni, E.; Larsen, B.R.; Amado, R. Degradation of flavonoid glycosides and aglycones during in vitro fermentation with human faecal flora. LWT-Food Sci. Technol. 2000, 33, 424–430, doi:10.1006/fstl.2000.0681.
[55]
Podsedek, A.; Sosnowska, D.; Redzynia, M.; Anders, B. Antioxidant capacity and content of Brassica oleracea dietary antioxidants. Int. J. Food Sci. Technol. 2006, 41, 49–58, doi:10.1111/j.1365-2621.2006.01260.x.
[56]
Sumaryono, W.; Proksch, P.; Wray, V.; Witte, L.; Hartmann, T. Qualitative and quantitative analysis of the phenolic constituents from Orthosiphon aristatus. Planta Med. 1991, 57, 176–180, doi:10.1055/s-2006-960060.
[57]
Gil-Mu？oz, R.; Gómez-Plaza, E.; Martínez, A.; López-Roca, J.M. Evolution of phenolic compounds during wine fermentation and post-fermentation: Influence of grape temperature. J. Food Compos. Anal. 1999, 12, 259–272, doi:10.1006/jfca.1999.0834.
[58]
Ju, H.K.; Cho, E.J.; Jang, M.H.; Lee, Y.Y.; Hong, S.S.; Park, J.H.; Kwon, S.W. Characterization of increased phenolic compounds from fermented Bokbunja (Rubus coreanus Miq.) and related antioxidant activity. J. Pharmaceut. Biomed. Anal. 2009, 49, 820–827, doi:10.1016/j.jpba.2008.12.024.
[59]
Hernández, T.; Estrella, I.; Carlavilla, D.; Martín-álvarez, P.J.; Moreno-Arribas, M.V. Phenolic compounds in red wine subjected to industrial malolactic fermentation and ageing on lees. Anal. Chim. Acta 2006, 563, 116–125, doi:10.1016/j.aca.2005.10.061.
[60]
Rodríguez, H.; Landete, J.M.; Rivas, B.D.L.; Mu？oz, R. Metabolism of food phenolic acids by Lactobacillus plantarum CECT 748T. Food Chem. 2008, 107, 1393–1398, doi:10.1016/j.foodchem.2007.09.067.
[61]
Curiel, J.A.; Rodríguez, H.; Landete, J.M.; de las Rivas, B.; Mu？oz, R. Ability of Lactobacillus brevis strains to degrade food phenolic acids. Food Chem. 2010, 120, 225–229, doi:10.1016/j.foodchem.2009.10.012.
[62]
Fletcher, R.S.; Slimmon, T.; McAuley, C.Y.; Kott, L.S. Heat stress reduces the accumulation of rosmarinic acid and the total antioxidant capacity in spearmint (Mentha spicata L). J. Sci. Food Agr. 2005, 85, 2429–2436, doi:10.1002/jsfa.2270.
[63]
Ariffin, F.; Heong Chew, S.; Bhupinder, K.; Karim, A.A.; Huda, N. Antioxidant capacity and phenolic composition of fermented Centella asiatica herbal teas. J. Sci. Food Agr. 2011, 91, 2731–2739, doi:10.1002/jsfa.4454.
[64]
Coinu, R.; Carta, S.; Urgeghe, P.P.; Mulinacci, N.; Pinelli, P.; Franconi, F.; Romani, A. Dose-effect study on the antioxidant properties of leaves and outer bracts of extracts obtained from Violetto di Toscana artichoke. Food Chem. 2007, 101, 524–531, doi:10.1016/j.foodchem.2006.02.009.
[65]
Soobrattee, M.A.; Neergheen, V.S.; Luximon-Ramma, A.; Aruoma, O.I.; Bahorun, T. Phenolics as potential antioxidant therapeutic agents: Mechanism and actions. Mutat. Res. Fund. Mol. Mech. Mutagen. 2005, 579, 200–213, doi:10.1016/j.mrfmmm.2005.03.023.
[66]
Tepe, B. Antioxidant potentials and rosmarinic acid levels of the methanolic extracts of Salvia virgata (Jacq), Salvia staminea (Montbret & Aucher ex Bentham) and Salvia verbenaca (L.) from Turkey. Bioresource Technol. 2008, 99, 1584–1588, doi:10.1016/j.biortech.2007.04.008.
