Antimicrobial Potential and Phytochemical Content of Six Diverse Sources of Quinoa Seeds (Chenopodium quinoa Willd.)
Author(s)
Margarita Miranda1,
José Delatorre-Herrera2,
Antonio Vega-Gálvez1,3,
Evelyn Jorquera1,
Issis Quispe-Fuentes1,
Enrique A. Martínez23*
Affiliation(s)
1 Department of Food Engineering, Universidad de La Serena, La Serena, Chile. 2 Department of Agriculture of Desert and Biotechnology, Facultad de Recursos Naturales Renovables, Universidad Arturo Prat, Iquique, Chile. 3 Centro de Estudios Avanzados en Zonas áridas (CEAZA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo and La Serena, Chile.
1 Department of Food Engineering, Universidad de La Serena, La Serena, Chile. 2 Department of Agriculture of Desert and Biotechnology, Facultad de Recursos Naturales Renovables, Universidad Arturo Prat, Iquique, Chile. 3 Centro de Estudios Avanzados en Zonas áridas (CEAZA), Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo and La Serena, Chile.
ABSTRACT
Antimicrobial potential of quinoa seeds from six diverse seeds, grown in three distinctive geo-graphical zones of Chile, was correlated with their total phenolic content (TPC), total flavonoid content (TFC) and total saponin content (TSC). The six seeds were Ancovinto, Cancosa, Cahuil, Faro, Regalona and Villarrica. A significant influence of quinoa source on chemical composition of seeds was observed. Extracts of all quinoa samples showed antimicrobial activity in the range of 8.3 - 14.8 mm inhibition zone for E. coli and 8.5 - 15.0 mm inhibition zone for S. aureus. Cancosa seeds had the highest antimicrobial action. The TPC and TFC ranged from 3.71 to 16.55 mg GA/100 g d.m. and 7.77 to 14.37 mg QE/100 g d.m., respectively. TSC varied from 1.78 to 3.08 g/100 g d.m. A cor-relation between TFC and antimicrobial activity was found. In conclusion, the six types of quinoa seeds were identified as potential sources of antioxidant compounds and antimicrobial activity.
Antimicrobial potential of quinoa seeds from six diverse seeds, grown in three distinctive geo-graphical zones of Chile, was correlated with their total phenolic content (TPC), total flavonoid content (TFC) and total saponin content (TSC). The six seeds were Ancovinto, Cancosa, Cahuil, Faro, Regalona and Villarrica. A significant influence of quinoa source on chemical composition of seeds was observed. Extracts of all quinoa samples showed antimicrobial activity in the range of 8.3 - 14.8 mm inhibition zone for E. coli and 8.5 - 15.0 mm inhibition zone for S. aureus. Cancosa seeds had the highest antimicrobial action. The TPC and TFC ranged from 3.71 to 16.55 mg GA/100 g d.m. and 7.77 to 14.37 mg QE/100 g d.m., respectively. TSC varied from 1.78 to 3.08 g/100 g d.m. A cor-relation between TFC and antimicrobial activity was found. In conclusion, the six types of quinoa seeds were identified as potential sources of antioxidant compounds and antimicrobial activity.
Cite this paper
Miranda, M. , Delatorre-Herrera, J. , Vega-Gálvez, A. , Jorquera, E. , Quispe-Fuentes, I. and Martínez, E. (2014) Antimicrobial Potential and Phytochemical Content of Six Diverse Sources of Quinoa Seeds (Chenopodium quinoa Willd.). Agricultural Sciences, 5, 1015-1024. doi: 10.4236/as.2014.511110.
Miranda, M. , Delatorre-Herrera, J. , Vega-Gálvez, A. , Jorquera, E. , Quispe-Fuentes, I. and Martínez, E. (2014) Antimicrobial Potential and Phytochemical Content of Six Diverse Sources of Quinoa Seeds (Chenopodium quinoa Willd.). Agricultural Sciences, 5, 1015-1024. doi: 10.4236/as.2014.511110.
References
[1] Kabuki, T., Nakajima, H., Arai, M., et al. (2000) Characterization of Novel Antimicrobial Compounds from Mango (Mangifera indica L.) Kernel Seeds. Food Chemistry, 71, 61-66.
http://dx.doi.org/10.1016/S0308-8146(00)00126-6 [2] Wangensteen, H., Samuelsen, A.B. and Malterud, K.E. (2004) Antioxidant Activity in Extracts from Coriander. Food Chemistry, 88, 293-297.
http://dx.doi.org/10.1016/j.foodchem.2004.01.047 [3] Borchardt, J.R., Wyse, D.L., Sheaffer, et al. (2009) Antioxidant and Antimicrobial Activity of Seed from Plants of the Mississippi River Basin. Journal of Medicinal Plants Research, 3, 707-718. [4] Quan, C., Yao, H. and Hou, C. (2013) Certification and Uncertainty Evaluation of Flavonoids Certified Reference Materials. Agricultural Sciences, 4, 89-96.
http://dx.doi.org/10.4236/as.2013.49B016 [5] Cai, Y., Luo, Q., Sun, M., et al. (2004) Antioxidant Activity and Phenolic Compounds of 112 Traditional Chinese Medicinal Plants Associated with Anticancer. Life Sciences, 74, 2157-2184.
http://dx.doi.org/10.1016/j.lfs.2003.09.047 [6] Komutarin, T., Azadi, S., Butterworth, L., et al. (2004) Extract of the Seed Coat of Tamarindus indica Inhibits Nitric Oxide Production by Murine Macrophages in Vitro and in Vivo. Food and Chemical Toxicology, 42, 649-658.
http://dx.doi.org/10.1016/j.fct.2003.12.001 [7] Comai, S., Bertazzo, A., Bailoni, L., et al. (2007) The Content of Proteic and Nonproteic (Free and Protein-Bound) Tryptophan in Quinoa and Cereal Flours. Food Chemistry, 100, 1350-1355.
http://dx.doi.org/10.1016/j.foodchem.2005.10.072 [8] Gely, MC. and Santalla, E. (2007) Moisture Diffusivity in Quinoa (Chenopodium quinoa Willd.) Seeds: Effect of Air Temperature and Initial Moisture Content of Seeds. Journal of Food Enginnering, 78, 1029-1033.
http://dx.doi.org/10.1016/j.jfoodeng.2005.12.015 [9] Ruiz, K.B, Biondi, S., Oses, R., et al. (2013) Quinoa, Its Biodiversity and Crop Sustainability as Key Contributions towards World Food Security in the Face of Climate Change. Agronomy for Sustainable Development, 34, 349-359.
http://dx.doi.org/10.1007/s13593-013-0195-0 [10] Juneja, V.K., Dwivedi, H.P. and Yan, X. (2012) Novel Natural Food Antimicrobials. Annual Review of Food Science and Technology, 3, 381-403.
http://dx.doi.org/10.1146/annurev-food-022811-101241 [11] Wright, K.H., Pike, O.A., Fairbanks, D.J. and Huber, C.S. (2002) Composition of Atriplex hortensis, Sweet and Bitter Chenopodium quinoa Seeds. Journal of Food Science, 67, 1383-1385. [12] Alvarez-Jubete, L., Wijngaard, H., Arendt, E.K. and Gallagher, E. (2010) Polyphenol Composition and in Vitro Antioxidant Activity of Amaranth, Quinoa, Buckwheat and Wheat as Affected by Sprouting and Baking. Food Chemistry, 119, 770-778.
http://dx.doi.org/10.1016/j.foodchem.2009.07.032 [13] Hassan, S.M., Haq, A.U., Byrd, J.A., Berhowd, M.A., Cartwrightb, A.L. and Bailey, C.A. (2010) Haemolytic and Antimicrobial Activities of Saponin-Rich Extracts from Guar Meal. Food Chemistry, 119, 600-605.
http://dx.doi.org/10.1016/j.foodchem.2009.06.066 [14] Deba, F., Xuan, T.D., Yasuda, M. and Tawata, S. (2008) Chemical Composition and Antioxidant, Antibacterial and Antifungal Activities of the Essential Oils from Bidens pilosa Linn. var. Radiata. Food Control, 19, 346-352.
http://dx.doi.org/10.1016/j.foodcont.2007.04.011 [15] AOAC (1990) Official Method of Analysis. 15th Edition, Association of Official Analytical Chemists, Washington DC. [16] Khoobchandani, M., Ojeswi, B.K., Ganesh, N., Srivastava, M.M., Gabbanini, S., Matera, R., et al. (2010) Antimicrobial Properties and Analytical Profile of Traditional Eruca sativa Seed Oil: Comparison with Various Aerial and Root Plant Extracts. Food Chemistry, 120, 217-224.
http://dx.doi.org/10.1016/j.foodchem.2009.10.011 [17] Chuah, A.M., Lee, Y.C., Yamaguchi, T., Takamura, H., Yin, L.J. and Matoba, T. (2008) Effect of Cooking on the Antioxidant Properties of Coloured Peppers. Food Chemistry, 111, 20-28.
http://dx.doi.org/10.1016/j.foodchem.2008.03.022 [18] Jia, Z., Tang, M. and Wu, J. (1999) The Determination of Flavonoid Contents in Mulberry and Their Scavenging Effects on Superoxide Radicals. Food Chemistry, 64, 555-559.
http://dx.doi.org/10.1016/S0308-8146(98)00102-2 [19] Liu, S.C., Lin, J.T., Wang, C.K., Chen, H.Y. and Yang D.J., (2009) Antioxidant Properties of Various Solvent Extracts from Lychee (Litchi chinenesis Sonn.) Flowers. Food Chemistry, 114, 577-581.
http://dx.doi.org/10.1016/j.foodchem.2008.09.088 [20] Madl, T., Sterk, H., Mittelbach, M. and Rechberger, G.N. (2006) Tandem Mass Spectrometric Analysis of a Complex Triterpene Saponin Mixture of Chenopodium quinoa. Journal of the American Society for Mass Spectrometry, 17, 795-806.
http://dx.doi.org/10.1016/j.jasms.2006.02.013 [21] Martín, R.S. and Briones, R. (2000) Quality Control of Commercial Quillaza (Quillaja saponaria Molina) Extracts by Reverse Phase HPLC. Journal of the Science of Food and Agriculture, 80, 2063-2068. [22] Repo-Carrasco-Valencia, R., Hellströmb, J.K., Pihlavac, J.M. and Mattila, P.H. (2010) Flavonoids and Other Phenolic Compounds in Andean Indigenous Grains: Quinoa (Chenopodium quinoa), Kañiwa (Chenopodium pallidicaule) and Kiwicha (Amaranthus caudatus). Food Chemistry, 120, 128-133.
http://dx.doi.org/10.1016/j.foodchem.2009.09.087 [23] Miranda, M., Vega-Gálvez, A., Quispe-Fuentes, I., Rodríguez, M.J., Maureira, H. and Martínez, E.A. (2012) Nutritional Aspects of Six Quinoa (Chenopodium quinoa Willd.) Seeds from Three Geographical Areas of Chile. Chilean Journal of Agricultural Research, 72, 175-181.
http://dx.doi.org/10.4067/S0718-58392012000200002 [24] Jancurová, M., Minarovicová, L. and Dandár, A. (2009) Quinoa-A Review. Czech Journal of Food Science, 27, 71-79. [25] Oliveira, I., Sousa, A., Ferreira, I., Bento, A., Estevinho, L. and Pereira, J.A. (2008) Total Phenols, Antioxidant Potential and Antimicrobial Avtivity of Walnut (Juglans regia L.) Green Husks. Food and Chemical Toxicology, 46, 2326-2331.
http://dx.doi.org/10.1016/j.fct.2008.03.017 [26] Al-Zoreky, N.S. (2009) Antimicrobial Activity of Pomegranate (Punica granatum L.) Fruit Peels. International Journal of Food Microbiology, 134, 244-248.
http://dx.doi.org/10.1016/j.ijfoodmicro.2009.07.002 [27] Zeng, W.C., Jia, L.R., Zhang, Y., Cen, J.Q., Chen, X., Gao, H., et al. (2011) Antibrowning and Antimicrobial Activities of the Water-Soluble Extract from Pine Needles of Cedrus deodara. Journal of Food Science, 76, C318-C123. [28] Keskin, D. and Toroglu, S. (2011) Studies on Antimicrobial Activities of Solvent Extracts of Different Species. Journal of Environmental Biology, 32, 251-256. [29] Miranda, M., Vega-Gálvez, A., López, J., Parada, G., Sanders, M., Aranda, M., et al. (2010) Impact of Air-Drying Temperature on Nutritional Properties, Total Phenolic Content and Antioxidant Capacity of Quinoa Seeds (Chenopodium quinoa Willd.). Industrial Crops and Products, 32, 258-263. http://dx.doi.org/10.1016/j.indcrop.2010.04.019 [30] Shan, B., Cai, Y.Z., Brooks, J. and Corke, H. (2007) The in Vitro Antibacterial Activity of Dietary Species and Medicinal Herb Extracts. International Journal of Food Microbiology, 117, 112-119.
http://dx.doi.org/10.1016/j.ijfoodmicro.2007.03.003 [31] Kalogeropoulos, N., Konteles, S.J., Troullidou, E., Mourtzinos, I. and Karathanos, V.T. (2009) Chemical Composition, Antioxidant Activity and Antimicrobial Properties of Propolis Extracts from Greece and Cyprus. Food Chemistry, 116, 452-461.
http://dx.doi.org/10.1016/j.foodchem.2009.02.060 [32] Fuentes, F., Martínez, E. A., Hinrichsen, P., Jellen, E.N. and Maughan, P.J. (2009) Assessment of Genetic Diversity Patterns in Chilean Quinoa (Chenopodium quinoa Willd.) Germplasm Using Multiplex Flourescent Microsatellites Markers. Conservation Genetics, 10, 369-377.
http://dx.doi.org/10.1007/s10592-008-9604-3
[1] Kabuki, T., Nakajima, H., Arai, M., et al. (2000) Characterization of Novel Antimicrobial Compounds from Mango (Mangifera indica L.) Kernel Seeds. Food Chemistry, 71, 61-66.
http://dx.doi.org/10.1016/S0308-8146(00)00126-6 [2] Wangensteen, H., Samuelsen, A.B. and Malterud, K.E. (2004) Antioxidant Activity in Extracts from Coriander. Food Chemistry, 88, 293-297.
http://dx.doi.org/10.1016/j.foodchem.2004.01.047 [3] Borchardt, J.R., Wyse, D.L., Sheaffer, et al. (2009) Antioxidant and Antimicrobial Activity of Seed from Plants of the Mississippi River Basin. Journal of Medicinal Plants Research, 3, 707-718. [4] Quan, C., Yao, H. and Hou, C. (2013) Certification and Uncertainty Evaluation of Flavonoids Certified Reference Materials. Agricultural Sciences, 4, 89-96.
http://dx.doi.org/10.4236/as.2013.49B016 [5] Cai, Y., Luo, Q., Sun, M., et al. (2004) Antioxidant Activity and Phenolic Compounds of 112 Traditional Chinese Medicinal Plants Associated with Anticancer. Life Sciences, 74, 2157-2184.
http://dx.doi.org/10.1016/j.lfs.2003.09.047 [6] Komutarin, T., Azadi, S., Butterworth, L., et al. (2004) Extract of the Seed Coat of Tamarindus indica Inhibits Nitric Oxide Production by Murine Macrophages in Vitro and in Vivo. Food and Chemical Toxicology, 42, 649-658.
http://dx.doi.org/10.1016/j.fct.2003.12.001 [7] Comai, S., Bertazzo, A., Bailoni, L., et al. (2007) The Content of Proteic and Nonproteic (Free and Protein-Bound) Tryptophan in Quinoa and Cereal Flours. Food Chemistry, 100, 1350-1355.
http://dx.doi.org/10.1016/j.foodchem.2005.10.072 [8] Gely, MC. and Santalla, E. (2007) Moisture Diffusivity in Quinoa (Chenopodium quinoa Willd.) Seeds: Effect of Air Temperature and Initial Moisture Content of Seeds. Journal of Food Enginnering, 78, 1029-1033.
http://dx.doi.org/10.1016/j.jfoodeng.2005.12.015 [9] Ruiz, K.B, Biondi, S., Oses, R., et al. (2013) Quinoa, Its Biodiversity and Crop Sustainability as Key Contributions towards World Food Security in the Face of Climate Change. Agronomy for Sustainable Development, 34, 349-359.
http://dx.doi.org/10.1007/s13593-013-0195-0 [10] Juneja, V.K., Dwivedi, H.P. and Yan, X. (2012) Novel Natural Food Antimicrobials. Annual Review of Food Science and Technology, 3, 381-403.
http://dx.doi.org/10.1146/annurev-food-022811-101241 [11] Wright, K.H., Pike, O.A., Fairbanks, D.J. and Huber, C.S. (2002) Composition of Atriplex hortensis, Sweet and Bitter Chenopodium quinoa Seeds. Journal of Food Science, 67, 1383-1385. [12] Alvarez-Jubete, L., Wijngaard, H., Arendt, E.K. and Gallagher, E. (2010) Polyphenol Composition and in Vitro Antioxidant Activity of Amaranth, Quinoa, Buckwheat and Wheat as Affected by Sprouting and Baking. Food Chemistry, 119, 770-778.
http://dx.doi.org/10.1016/j.foodchem.2009.07.032 [13] Hassan, S.M., Haq, A.U., Byrd, J.A., Berhowd, M.A., Cartwrightb, A.L. and Bailey, C.A. (2010) Haemolytic and Antimicrobial Activities of Saponin-Rich Extracts from Guar Meal. Food Chemistry, 119, 600-605.
http://dx.doi.org/10.1016/j.foodchem.2009.06.066 [14] Deba, F., Xuan, T.D., Yasuda, M. and Tawata, S. (2008) Chemical Composition and Antioxidant, Antibacterial and Antifungal Activities of the Essential Oils from Bidens pilosa Linn. var. Radiata. Food Control, 19, 346-352.
http://dx.doi.org/10.1016/j.foodcont.2007.04.011 [15] AOAC (1990) Official Method of Analysis. 15th Edition, Association of Official Analytical Chemists, Washington DC. [16] Khoobchandani, M., Ojeswi, B.K., Ganesh, N., Srivastava, M.M., Gabbanini, S., Matera, R., et al. (2010) Antimicrobial Properties and Analytical Profile of Traditional Eruca sativa Seed Oil: Comparison with Various Aerial and Root Plant Extracts. Food Chemistry, 120, 217-224.
http://dx.doi.org/10.1016/j.foodchem.2009.10.011 [17] Chuah, A.M., Lee, Y.C., Yamaguchi, T., Takamura, H., Yin, L.J. and Matoba, T. (2008) Effect of Cooking on the Antioxidant Properties of Coloured Peppers. Food Chemistry, 111, 20-28.
http://dx.doi.org/10.1016/j.foodchem.2008.03.022 [18] Jia, Z., Tang, M. and Wu, J. (1999) The Determination of Flavonoid Contents in Mulberry and Their Scavenging Effects on Superoxide Radicals. Food Chemistry, 64, 555-559.
http://dx.doi.org/10.1016/S0308-8146(98)00102-2 [19] Liu, S.C., Lin, J.T., Wang, C.K., Chen, H.Y. and Yang D.J., (2009) Antioxidant Properties of Various Solvent Extracts from Lychee (Litchi chinenesis Sonn.) Flowers. Food Chemistry, 114, 577-581.
http://dx.doi.org/10.1016/j.foodchem.2008.09.088 [20] Madl, T., Sterk, H., Mittelbach, M. and Rechberger, G.N. (2006) Tandem Mass Spectrometric Analysis of a Complex Triterpene Saponin Mixture of Chenopodium quinoa. Journal of the American Society for Mass Spectrometry, 17, 795-806.
http://dx.doi.org/10.1016/j.jasms.2006.02.013 [21] Martín, R.S. and Briones, R. (2000) Quality Control of Commercial Quillaza (Quillaja saponaria Molina) Extracts by Reverse Phase HPLC. Journal of the Science of Food and Agriculture, 80, 2063-2068. [22] Repo-Carrasco-Valencia, R., Hellströmb, J.K., Pihlavac, J.M. and Mattila, P.H. (2010) Flavonoids and Other Phenolic Compounds in Andean Indigenous Grains: Quinoa (Chenopodium quinoa), Kañiwa (Chenopodium pallidicaule) and Kiwicha (Amaranthus caudatus). Food Chemistry, 120, 128-133.
http://dx.doi.org/10.1016/j.foodchem.2009.09.087 [23] Miranda, M., Vega-Gálvez, A., Quispe-Fuentes, I., Rodríguez, M.J., Maureira, H. and Martínez, E.A. (2012) Nutritional Aspects of Six Quinoa (Chenopodium quinoa Willd.) Seeds from Three Geographical Areas of Chile. Chilean Journal of Agricultural Research, 72, 175-181.
http://dx.doi.org/10.4067/S0718-58392012000200002 [24] Jancurová, M., Minarovicová, L. and Dandár, A. (2009) Quinoa-A Review. Czech Journal of Food Science, 27, 71-79. [25] Oliveira, I., Sousa, A., Ferreira, I., Bento, A., Estevinho, L. and Pereira, J.A. (2008) Total Phenols, Antioxidant Potential and Antimicrobial Avtivity of Walnut (Juglans regia L.) Green Husks. Food and Chemical Toxicology, 46, 2326-2331.
http://dx.doi.org/10.1016/j.fct.2008.03.017 [26] Al-Zoreky, N.S. (2009) Antimicrobial Activity of Pomegranate (Punica granatum L.) Fruit Peels. International Journal of Food Microbiology, 134, 244-248.
http://dx.doi.org/10.1016/j.ijfoodmicro.2009.07.002 [27] Zeng, W.C., Jia, L.R., Zhang, Y., Cen, J.Q., Chen, X., Gao, H., et al. (2011) Antibrowning and Antimicrobial Activities of the Water-Soluble Extract from Pine Needles of Cedrus deodara. Journal of Food Science, 76, C318-C123. [28] Keskin, D. and Toroglu, S. (2011) Studies on Antimicrobial Activities of Solvent Extracts of Different Species. Journal of Environmental Biology, 32, 251-256. [29] Miranda, M., Vega-Gálvez, A., López, J., Parada, G., Sanders, M., Aranda, M., et al. (2010) Impact of Air-Drying Temperature on Nutritional Properties, Total Phenolic Content and Antioxidant Capacity of Quinoa Seeds (Chenopodium quinoa Willd.). Industrial Crops and Products, 32, 258-263. http://dx.doi.org/10.1016/j.indcrop.2010.04.019 [30] Shan, B., Cai, Y.Z., Brooks, J. and Corke, H. (2007) The in Vitro Antibacterial Activity of Dietary Species and Medicinal Herb Extracts. International Journal of Food Microbiology, 117, 112-119.
http://dx.doi.org/10.1016/j.ijfoodmicro.2007.03.003 [31] Kalogeropoulos, N., Konteles, S.J., Troullidou, E., Mourtzinos, I. and Karathanos, V.T. (2009) Chemical Composition, Antioxidant Activity and Antimicrobial Properties of Propolis Extracts from Greece and Cyprus. Food Chemistry, 116, 452-461.
http://dx.doi.org/10.1016/j.foodchem.2009.02.060 [32] Fuentes, F., Martínez, E. A., Hinrichsen, P., Jellen, E.N. and Maughan, P.J. (2009) Assessment of Genetic Diversity Patterns in Chilean Quinoa (Chenopodium quinoa Willd.) Germplasm Using Multiplex Flourescent Microsatellites Markers. Conservation Genetics, 10, 369-377.
http://dx.doi.org/10.1007/s10592-008-9604-3