Generic placeholder image

Current Bioactive Compounds

Editor-in-Chief

ISSN (Print): 1573-4072
ISSN (Online): 1875-6646

Research Article

Nutraceutical, Antioxidant, Antimicrobial Properties of Pyropia vietnamensis (Tanaka et Pham-Hong Ho) J.E. Sutherl. et Monotilla

Author(s): Saurabh Bhatia*, Arun K. Sharma, Celia B. Vargas De La Cruz, Bhupal Chaugule and Ahmed Al-Harrasi

Volume 17, Issue 2, 2021

Published on: 27 February, 2020

Page: [151 - 164] Pages: 14

DOI: 10.2174/1573407216666200227094935

Price: $65

Abstract

Background: Pyropia genus is one of the most nutritionally rich marine algae which contain various bioactive compounds. Among Indian Pyropia species, Pyropia vietnamensis (P. vietnamensis), which was earlier known as Porphyra vietnamensis has recently documented with various reports. The present work is designed to evaluate the radical scavenging, nutraceutical and microbicidal properties of Pyropia vietnamensis.

Methods: P. vietnamensis was collected from the coastal region of Maharashtra, namely Harihareshwar. Dried algal material was extracted with different solvents. Nutritional parameters such as fatty acids, minerals, dietary fibers, vitamins, lipids, ash content and protein were measured as per the standard protocol (WHO guidelines). Folin-Ciocalteu and aluminum chloride colorimetric procedures were used to estimate total phenolic content and total flavonoid content. Free radical scavenging activity was assessed using 2,2-diphenyl-1-picrylhydrazyl, nitric oxide and superoxide anion (O2¯) assays. Antimicrobial activity was investigated by in vitro microdilution procedure to estimate minimum inhibitory concentration and minimum bacterial concentration, against Gram-- positive bacterium (Staphylococcus aureus) and Gram-negative bacteria (Klebsiella pneumoniae, Escherichia coli, and Proteus vulgaris).

Results: Nutritional analysis revealed that Pyropia vietnamensis contained a considerable amount of dietary fiber, protein, carbohydrate, methyl palmitate, magnesium, sulphur and sodium. Total phenolic content and total flavonoid content of methanolic fractions (913±21.7, 128±11.7) were more than an aqueous fraction (841±21.2, 3.7±11.1). Aqueous and ethyl acetate fractions showed significant antioxidant activity against 2,2-diphenyl-1-picrylhydrazyl (65.5±1.2 μg/mL, 68.3±1.6 μg/mL), nitric oxide (71.5±3.5 μg/mL, 52.3±1.9 μg/mL), and O2¯ (50.6±1.02 μg/mL, 62.1±1.03μg/mL) free radicals. Aqueous, methanolic and ethyl acetate fractions had the highest total antibacterial activity with minimum inhibitory concentration as 110–490 μg/mL and minimum bacterial concentration as 248–689 μg/mL against one Gram-positive and three Gram-negative microorganisms.

Conclusion: Aqueous, ethyl acetate, and methanolic fractions of Pyropia vietnamensis exhibited good antimicrobial spectrum and antioxidant activity. This could be useful in preventing various oxidative stresses and pathogenic microbial strains.

Keywords: Pyropia vietnamensis, minerals, nutritional, antioxidant, red, alga, antimicrobial.

Graphical Abstract

[1]
Pérez, A.A.; Farías, S.S.; Strobl, A.M.; Pérez, L.B.; López, C.M.; Piñeiro, A.; Roses, O.; Fajardo, M.A. Levels of essential and toxic elements in Porphyra columbina and Ulva sp. from San Jorge Gulf, Patagonia Argentina. Sci. Total Environ., 2007, 376(1-3), 51-59.
[http://dx.doi.org/10.1016/j.scitotenv.2006.11.013] [PMID: 17337287]
[2]
Rupe’rez, P. Mineral content of edible marine seaweeds. Food Chem., 2002, 79, 23-26.
[http://dx.doi.org/10.1016/S0308-8146(02)00171-1]
[3]
Rupe’rez, P.; Saura-Calixto, F. Dietary fiber and physicochemical properties of edible Spanish seaweeds. Eur. Food Res. Technol., 2001, 212, 349-354.
[http://dx.doi.org/10.1007/s002170000264]
[4]
Urbano, G.; Gon˜, I.I. Bioavailability of nutrients in rats fed on edible seaweeds, Nori (Porphyra tenera) and Wakame (Undaria pinnatifida), as a source of dietary fiber. Food Chem., 2002, 76, 281-286.
[http://dx.doi.org/10.1016/S0308-8146(01)00273-4]
[5]
Rao, P.; Mantri, V.; Ganesan, K. Mineral composition of edible seaweed Porphyra vietnamensis. Food Chem., 2007, 102, 215-218.
[http://dx.doi.org/10.1016/j.foodchem.2006.05.009]
[6]
Kumar, M.; Kumari, P.; Trivedi, N.; Shukla, M.K.; Gupta, V.; Reddy, C.R.K.; Jha, B. Minerals, PUFAs and antioxidant properties of some tropical seaweeds from Saurashtra coast of India. J. Appl. Phycol., 2011, 23, 797-810.
[http://dx.doi.org/10.1007/s10811-010-9578-7]
[7]
Mohamed, S.; Hashim, S.N.; Rahman, H.A. Seaweeds: A sustainable functional food for complementary and alternative therapy. Trends Food Sci. Technol., 2012, 23, 83-96.
[http://dx.doi.org/10.1016/j.tifs.2011.09.001]
[8]
Bhatia, S.; Namdeo, A.G.; Nanda, S. Factors effecting the gelling and emulsifying properties of a natural polymer. Systematic reviews in pharmacy, 2010, 1, 86-92. b
[9]
Bhatia, S.; Garg, A.; Sharma, K.; Kumar, S.; Sharma, A.; Purohit, A.P. Mycosporine and mycosporine-like amino acids: A paramount tool against ultra violet irradiation. Pharmacogn. Rev., 2011, 5(10), 138-146.
[http://dx.doi.org/10.4103/0973-7847.91107] [PMID: 22279371]
[10]
Bhatia, S.; Rathee, P.; Sharma, K.; Chaugule, B.B.; Kar, N.; Bera, T. Immuno-modulation effect of sulphated polysaccharide (porphyran) from Porphyra vietnamensis. Int. J. Biol. Macromol., 2013, 57, 50-56.
[http://dx.doi.org/10.1016/j.ijbiomac.2013.03.012] [PMID: 23500431]
[11]
Bhatia, S.; Sharma, A.; Sharma, K.; Kavale, M.; Chaugule, B.B.; Dhalwal, K. Novel Algal Polysaccharides from Marine Source: Porphyran. Pharmacogn. Rev., 2008, 2, 271-276.
[12]
Bhatia, S.; Sharma, K.; Namdeo, A.G.; Chaugule, B.B.; Kavale, M.; Nanda, S. Broad-spectrum sun-protective action of Porphyra-334 derived from Porphyra vietnamensis. Pharmacognosy Res., 2010, 2(1), 45-49.
[http://dx.doi.org/10.4103/0974-8490.60578] [PMID: 21808539]
[13]
Bhatia, S. Significance of algal polymer in designing amphotericin B nanoparticles. Scientific World J., 2014, 2014, 21.
[http://dx.doi.org/10.1155/2014/564573]
[14]
Bhatia, S.; Sharma, K.; Nagpal, K.; Bera, T. Investigation of the factors influencing the molecular weight of porphyran and its associated antifungal activity. Bioactive Carbohydrates and Dietary Fibre., 2015, 5, 153-168.
[http://dx.doi.org/10.1016/j.bcdf.2015.03.005]
[15]
Bhatia, S.; Sharma, K.; Sharma, A.; Nagpal, K.; Bera, T. Anti-inflammatory, analgesic and antiulcer properties of Porphyra vietnamensis. Avicenna J. Phytomed., 2015, 5(1), 69-77.
[PMID: 25767759]
[16]
Bhatia, S. Structural characterization and pharmaceutical properties of porphyran. Asian. J. Pharm. (Cairo), 2015, 9, 2.
[17]
Bhatia, S.; Sardana, S.; Naved, T.; Sharma, A. Effects of Porphyra vietnamensis extract on TNBS-induced colitis in rats. Int. J. Pharm. Sci. Res., 2019, 10, 1000-1010.
[18]
Bhatia, S.; Sharma, K.; Sharma, A.; Namdeo, A.G.; Chaugule, B.B. Anti-oxidant potential of Indian porphyra. Pharmacologyonline, 2011, 1, 248-257.
[19]
Bhatia, S.; Sardana, S.; Senwar, K.R.; Dhillon, A.; Sharma, A.; Naved, T. In vitro antioxidant and antinociceptive properties of Porphyra vietnamensis. BioMedicine., 2019, 9, 1(3)
[20]
Bhatia, S.; Sardana, S.; Sharma, A.; Vargas De La Cruz, C.B.; Chaugule, B.; Khodaie, L. Development of broad spectrum mycosporine loaded sunscreen formulation from Ulva fasciata delile. Biomedicine (Taipei), 2019, 9(3), 17.
[http://dx.doi.org/10.1051/bmdcn/2019090317] [PMID: 31453798]
[21]
Sutherland, J.E.; Lindstrom, S.C.; Nelson, W.A.; Brodie, J.; Lynch, M.D.J. Hwang, Havang M.S., Choi, H-G., Miyata, M., Kikuchi, N., Oliveira, M.C., Farr, T., Neefus, C., Mols-Mortensen, A., Milstein, D.; Müller, K.M. A new look at an ancient order: Generic revision of the Bangiales (Rhodophyta). J. Phycol., 2011, 47, 1131-1151.
[http://dx.doi.org/10.1111/j.1529-8817.2011.01052.x] [PMID: 27020195]
[22]
Zuccarello, J. What are you eating? It may be Nori, but it is probably not Porphyra anymore. J. Phycol., 2011, 47(5), 967-968.
[http://dx.doi.org/10.1111/j.1529-8817.2011.01064.x] [PMID: 27020177]
[23]
Milstein, D.; Medeiros, A.S.; Oliveira, E.C.; Oliveira, M.C. Native or introduced? A re-evaluation of Pyropia species (Bangiales, Rhodophyta) from Brazil based on molecular analyses. Eur. J. Phycol., 2015, 50, 37-45.
[http://dx.doi.org/10.1080/09670262.2014.982202]
[24]
Tanaka, T.; Ho, P.H. Notes of some marine algae from Viet-Nam - I. Mem. Fac. Fish. Kagoshima Univ., 1962, 11, 24-40.
[25]
Desikachary, T.V.; Krishnamurthy, V.; Balakrishnan, M.S. Rhodophyta. Madras Science Foundation, 1990, I, 279.
[26]
Lowry, O.H.; Rosebrough, N.J.; Farr, A.L.; Randall, R.J. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193(1), 265-275.
[PMID: 14907713]
[27]
Hedge, J.E.; Hofreiter, B.T. Carbohydrate chemistry 17. Whistler, R.L. and Be Miller, J. N., Eds., Academic Press, New York 1962.
[28]
AOAC. Official method of Analysis. 17th Ed. The Association of Official Analytical Chemists, Gaithersburg, MD, USA. Methods 925, 10, 65, 17, 2000.
[29]
AOAC. Official method of Analysis. 18th Ed. Association of Officiating Analytical Chemists, Washington DC, Method 935, 14 and 992, 24, 2005.
[30]
Bligh, E.G.; Dyer, W.J. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol., 1959, 37(8), 911-917.
[http://dx.doi.org/10.1139/o59-099] [PMID: 13671378]
[31]
de La Cruz Garcia, C.; López Hernandez, J.; Simal Lozano, J. Gas chromatographic determination of the fatty-acid content of heat-treated green beans. J. Chromatogr. A, 2000, 891(2), 367-370.
[http://dx.doi.org/10.1016/S0021-9673(00)00674-9] [PMID: 11043798]
[32]
Kavale, M.G.; Kazi, M.A.; Sreenadhan, N.; Murgan, P. Nutritional profiling of Pyropia acanthophora var. robusta (Bangiales, Rhodophyta) from Indian waters. J. Appl. Phycol., 2017, 29, 2013-2020.
[http://dx.doi.org/10.1007/s10811-017-1096-4]
[33]
McHugh, D.J. A guide to the seaweed industry. Rome, FAO. FAO Fisheries Technical Paper No. 441, 2003.
[34]
Kendel, M.; Wielgosz-Collin, G.; Bertrand, S.; Roussakis, C.; Bourgougnon, N.; Bedoux, G. Lipid composition, fatty acids and sterols in the seaweeds Ulva armoricana, and Solieria chordalis from Brittany (France): An analysis from nutritional, chemotaxonomic, and antiproliferative activity perspectives. Mar. Drugs, 2015, 13(9), 5606-5628.
[http://dx.doi.org/10.3390/md13095606] [PMID: 26404323]
[35]
Nishide, E.; Ohno, M.; Anzai, H.; Uchida, N. Extraction of porphyran from Porphyra yezoiensis Ueda F. Narawaensis Miura. Nippon Suisan Gakkaishi, 1998, 54, 2189-2194.
[http://dx.doi.org/10.2331/suisan.54.2189]
[36]
Ishihara, K.; Oyamada, C.; Matsushima, R.; Murata, M.; Muraoka, T. Inhibitory effect of porphyran, prepared from dried “Nori”, on contact hypersensitivity in mice. Biosci. Biotechnol. Biochem., 2005, 69(10), 1824-1830.
[http://dx.doi.org/10.1271/bbb.69.1824] [PMID: 16244430]
[37]
Henry, G.E.; Momin, R.A.; Nair, M.G.; Dewitt, D.L. Antioxidant and cyclooxygenase activities of fatty acids found in food. J. Agric. Food Chem., 2002, 50(8), 2231-2234.
[http://dx.doi.org/10.1021/jf0114381] [PMID: 11929276]
[38]
Huang, H.L.; Wang, B.G. Antioxidant capacity and lipophilic content of seaweeds collected from the Qingdao coastline. J. Agric. Food Chem., 2004, 52(16), 4993-4997.
[http://dx.doi.org/10.1021/jf049575w] [PMID: 15291465]
[39]
Djeridane, A.; Youffi, M.; Nadjemi, B. Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chem., 2006, 97, 654-660.
[http://dx.doi.org/10.1016/j.foodchem.2005.04.028]
[40]
Zhishen, J.; Mengcheng, T.; Wu, J. The determination of flavonoid content in mulberry and their scavenging effects on superoxide radicals. Food Chem., 1999, 64, 555-559.
[http://dx.doi.org/10.1016/S0308-8146(98)00102-2]
[41]
Yen, G.C.; Duh, P.D.; Tsai, C.L. The relationship between antioxidant activity and maturity of peanut hulls. J. Agric. Food Chem., 1993, 41, 67-70.
[http://dx.doi.org/10.1021/jf00025a015]
[42]
Jao, C.H.; Ko, W.C. 1,1-Diphenyl-2-picrylhydrazyl (DPPH) radical scavenging by protein hydrolyzates from tuna cooking juice. Fish. Sci., 2002, 68, 430-435.
[http://dx.doi.org/10.1046/j.1444-2906.2002.00442.x]
[43]
Green, L.C.; Wagner, D.A.; Glogowski, J.; Skipper, P.L.; Wishnok, J.S.; Tannenbaum, S.R. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem., 1982, 126(1), 131-138.
[http://dx.doi.org/10.1016/0003-2697(82)90118-X] [PMID: 7181105]
[44]
Liu, F.; Ooi, V.E.C.; Chang, S.T. Free radical scavenging activities of mushroom polysaccharide extracts. Life Sci., 1997, 60(10), 763-771.
[http://dx.doi.org/10.1016/S0024-3205(97)00004-0] [PMID: 9064481]
[45]
Oktay, M.; Gulcin, I.; Kufrevioglu, O.I. Determination of in vitro antioxidant activity of fennel (Foeniculum vulgare) seed extracts. Lebensmittel Wissenchaft und Technol., 2003, 36, 263-271.
[http://dx.doi.org/10.1016/S0023-6438(02)00226-8]
[46]
Oki, T.; Masuda, M.; Furuta, S.; Nishiba, Y.; Terahara, N.; Suda, I. Involvement of anthocyanins and other phenolic compounds in radical scavenging activity of purple fleshed sweet potato cultivars. Food Chem. Toxicol., 2002, 67, 1752-1756.
[47]
Lu, Y.; Foo, Y.L. Antioxidant and free radical scavenging activities of selected medicinal herbs. J. Life Sci., 2000, 66, 725-735.
[http://dx.doi.org/10.1016/S0024-3205(99)00643-8]
[48]
Braca, A.; De Tommasi, N.; Di Bari, L.; Pizza, C.; Politi, M.; Morelli, I. Antioxidant principles from Bauhinia tarapotensis. J. Nat. Prod., 2001, 64(7), 892-895.
[http://dx.doi.org/10.1021/np0100845] [PMID: 11473417]
[49]
Siriwardhana, N.; Lee, K.W.; Kim, S.H.; Ha, J.W.; Jeon, Y.J. Antioxidant activity of Hizikia fusiformis on reactive oxygen species scavenging and lipid peroxidation inhibition. Food Sci. Technol. Int., 2003, 9, 339-346.
[http://dx.doi.org/10.1177/1082013203039014]
[50]
Shariff, N.; Sudarshana, M.S.; Umesha, S.; Hariprasad, P. Antimicrobial activity of Rauvolfia tetraphylla and Physalis minima leaf and callus extracts. Afr. J. Biotechnol., 2006, 5, 946-950.
[51]
Pacifici, R.E.; Davies, K.J. Protein, lipid and DNA repair systems in oxidative stress: the free-radical theory of aging revisited. Gerontology, 1991, 37(1-3), 166-180.
[http://dx.doi.org/10.1159/000213257] [PMID: 2055497]
[52]
Dahl, M.; Richardson, M. Photogeneration of superoxide anion in serum of bovine milk and in model systems containing riboflavin and amino acids. J. Dairy Sci., 1978, 61, 400-407.
[http://dx.doi.org/10.3168/jds.S0022-0302(78)83613-3]
[53]
Kavale, M.; Anisoddin, M.; Mudassar, K.; Kazi, A.; Bagal, P.U.; Behera, D.P. Food value of Pyropia vietnamensis (Bangiales, Rhodophyta) from India. Indian J. Geo-Mar. Sci., 2017, 46(12)
[54]
Jung, S.M.; Kang, S.G.; Son, J.S.; Jeon, J.H.; Lee, H.J.; Shin, H.W. Temporal and spatial variations in the proximate composition, amino acid, and mineral content of Pyropia yezoensis. J. Appl. Phycol., 2016, 28, 3459-3467.
[http://dx.doi.org/10.1007/s10811-016-0862-z]
[55]
Hwang, E.S.; Ki, K.N.; Chung, H.Y. Proximate composition, amino Acid, mineral, and heavy metal content of dried laver. Prev. Nutr. Food Sci., 2013, 18(2), 139-144.
[http://dx.doi.org/10.3746/pnf.2013.18.2.139] [PMID: 24471123]
[56]
Taboada, M.C.; Millán, R.; Miguez, M.I. Nutritional value of the marine algae wakame (Undaria pinnatifida) and nori (Porphyra purpurea) as food supplements. J. Appl. Phycol., 2013, 25, 1271-1276.
[http://dx.doi.org/10.1007/s10811-012-9951-9]
[57]
Sánchez-Machado, D.I.; López-Cervantes, C.; López-Hernandez, J.; Paseiro Losada, P. Fatty acids, total lipids, protein and ash contents of processed edible seaweeds. Food Chem., 2004, 85, 439-444.
[http://dx.doi.org/10.1016/j.foodchem.2003.08.001]
[58]
Patarra, R.F.; Paiva, L.; Neto, A.I.; Lima, E.; Baptista, J. Nutritional value of selected macroalgae. J. Appl. Phycol., 2011, 23, 205-208.
[http://dx.doi.org/10.1007/s10811-010-9556-0]
[59]
Galland-Irmouli, A.V.; Fleurence, J.; Lamghari, R.; Luçon, M.; Rouxel, C.; Barbaroux, O.; Bronowicki, J.P.; Villaume, C.; Guéant, J.L. Nutritional value of proteins from edible seaweed Palmaria palmata (dulse). J. Nutr. Biochem., 1999, 10(6), 353-359.
[http://dx.doi.org/10.1016/S0955-2863(99)00014-5] [PMID: 15539310]
[60]
Toyosaki, T.; Iwabuchi, M. New antioxidant protein in seaweed (Porphyra yezoensis Ueda). Int. J. Food Sci. Nutr., 2009, 60(2)(Suppl. 2), 46-56.
[http://dx.doi.org/10.1080/09637480802345591] [PMID: 19212859]
[61]
Dawczynski, C.; Schubert, R.; Jahreis, G. Amino acids, fatty acids and dietary fibers in edible seaweed products. Food Chem., 2007, 103, 891-899.
[http://dx.doi.org/10.1016/j.foodchem.2006.09.041]
[62]
Shin, D-M.; An, Se-Ra. Seasonal variation in the dietary fiber, amino acid and fatty acid contents of Porphyra yezoensis. In: Korean J Fish Aquat Sci; , 2013; 46, pp. 337-342.
[63]
Jiménez-Escrig, A.; Sánchez-Muniz, F.J. Dietary fibre from edible seaweeds: Chemical structure, physicochemical properties and effects on cholesterol metabolism. Nutr. Res., 2000, 20, 585-598.
[http://dx.doi.org/10.1016/S0271-5317(00)00149-4]
[64]
Lahaye, M. Marine algae as sources of fibers: Determination of soluble and insoluble dietary fibre contents in some ‘sea vegetables’. J. Sci. Food Agric., 1991, 54, 587-594.
[http://dx.doi.org/10.1002/jsfa.2740540410]
[65]
Cian, R.E.; Fajardo, M.A.; Alaiz, M.; Vioque, J.; González, R.J.; Drago, S.R. Chemical composition, nutritional and antioxidant properties of the red edible seaweed Porphyra columbina. Int. J. Food Sci. Nutr., 2014, 65(3), 299-305.
[http://dx.doi.org/10.3109/09637486.2013.854746] [PMID: 24219228]
[66]
Kumari, P.; Bijo, A.J.; Mantri, V.A.; Reddy, C.R.K.; Jha, B. Fatty acid profiling of tropical marine macroalgae: An analysis from chemotaxonomic and nutritional perspectives. Phytochemistry, 2013, 86, 44-56.
[http://dx.doi.org/10.1016/j.phytochem.2012.10.015] [PMID: 23168246]
[67]
Fleurence, J. Seaweed proteins: Biochemical, nutritional aspects and potential uses. Trends Food Sci. Technol., 1999, 10, 25-28.
[http://dx.doi.org/10.1016/S0924-2244(99)00015-1]
[68]
Maghraby, D.M.E.; Fakhry, M.E. Lipid content and fatty acid composition of Mediterranean macro-algae as dynamic factors for biodiesel production. Oceanologia, 2015, 57, 86-92.
[http://dx.doi.org/10.1016/j.oceano.2014.08.001]
[69]
Khairy, H.M.; El-Shafay, S.M. Seasonal variation in the biochemical composition of some common seaweed species from the coast of Abu Qir Bay, Alexandria, Egypt. Oceanologia, 2013, 55, 435-452.
[http://dx.doi.org/10.5697/oc.55-2.435]
[70]
Jiao, K.; Gao, J.; Zhou, T.; Yu, J.; Song, H.; Wei, Y.; Gao, X. Isolation and purification of a novel antimicrobial peptide from Porphyra yezoensis. J. Food Biochem., 2019, 43(7)e12864
[http://dx.doi.org/10.1111/jfbc.12864] [PMID: 31353731]
[71]
Mendes, M.; Pereira, R.; Sousa Pinto, I.; Carvalho, A.P.; Gomes, A.M. Antimicrobial activity and lipid profile of seaweed extracts from the North Portuguese Coast. Int. Food Res. J., 2013, 20, 3337-3345.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy