A comparison of fatty acid content in three species of the genus Pleurotus
Comparación del contenido de ácidos grasos en tres especies del género Pleurotus
Margarita González-Tijera1, Olivia Márquez-Fernández2, Ma. Remedios Mendoza-López3, Gerardo Mata4, Ángel Trigos2*
1 Instituto de Biotecnología y Ecología Aplicada, Universidad Veracruzana, Av. de las Culturas Veracruzanas No. 101, Col. Emiliano Zapata, C.P. 91090, Xalapa, Veracruz, México.
]]> 2 Laboratorio de Alta Tecnología de Xalapa, A. C, Universidad Veracruzana, Calle Médicos y Odontólogos No. 5. Col. Unidad del Bosque, C.P. 91010, Xalapa, Veracruz, México.3 Unidad de Servicios de Apoyo en Resolución Analítica, Universidad Veracruzana, Dr. Luis Castelazo Ayala s/n, Col. Industrial Animas, C.P. 91190, Xalapa, Veracruz, México.
4 Instituto de Ecología A.C. Km. 2.5 Carr. Antigua A Coatepec No. 351, Congregación El Haya, C.P. 91070, Xalapa, Veracruz, México.
* Autor para correspondencia:
Angel Trigos atrigos@uv.mx
Received 27 November 2013;
Accepted 23 March 2014.
]]> Abstract
A comparison was made of fatty acid profiles (FA) of Pleurotus ostreatus and P. levis grown on a barley straw substrate. The major FAs found in both species were linoleic, oleic and palmitic fatty acids. However, in the case of cultivating P. levis on a maguey bagasse-barley straw 1:1 (w/w) substrate, the major acid found was oleic acid. These results were compared with a commercial strain of Pleurotus sp. grown on wheat straw-corn bagasse, where elaidic acid was detected in P. levis and the commercial mushroom. Based on previous works it was found that the composition of the FA in mushrooms cultivation varies accordingto the substrate used.
Key words: Monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), saturated fatty acids (SFA), elaidic acid, oyster mushroom.
Resumen
Se compararon los perfiles de Acidos Grasos (AG) de Pleurotus ostreatus y P. levis cultivados en paja de cebada. Los AG mayoritarios encontrados en ambas especies fueron el linoleico, oleico y palmítico; sin embargo, al cultivar P. levis en bagazo de maguey-paja de cebada 1:1 (w/w), el AG mayoritario fue el oleico. Adicionalmente, estos resultados se compararon con una cepa comercial de Pleurotus sp. cultivada en paja de trigo-rastrojo de maíz. Por otro lado, se detectó la presencia del ácido elaídico en P. levis y el hongo comercial. Basados en trabajos previos, se comprueba que la composición de los AG en cultivos de hongos comestibles puede variar de acuerdo al sustrato empleado.
Palabras clave: Ácidos Grasos Monoinsaturados (ACMI), Ácidos Grasos Poliinsaturados (AGPI), Ácidos Grasos Saturados (AGS), ácido elaídico, setas.
Edible mushrooms have a low lipid content, varying from 1.1 to 8.3% (dry weight), with an average of 4.0% (Chang and Miles, 2004) and a high proportion of polyunsaturated fatty acids (PUFAs), which gives them added value as a healthy food, recommended for including in the diet of people with high concentration of cholesterol in blood (Chang and Buswell, 1996; Heleno et al, 2009; Kavishree et al, 2008). Furthermore, PUFAs are a key factor to the sensory evaluation of edible mushrooms (Sinanoglou et al, 2013).
Linoleic acid produces a serie of omega-6 fatty acids and it is the predecessor of volatile compounds of eight carbons, 1-octen-3-ol, 3-octanol, l-octen-3-one and 3-octanone (Combet et al, 2006), which are the components that contribute to the characteristic flavor and aroma in most edible mushroom species (Ribeiro et al, 2009). Furthermore, FA profiles provide physiological data that can be used together with their morphological characteristics and they could be used to taxonomically classify a large number of mushroom strains (Jabaji-Hare, 1988; Lechevalier and Lechevalier, 1988). Therefore, a detailed analysis of lipids and fatty acids (FA) is useful in evaluating mushrooms for nutritional and nutraceutical characteristics and also for taxonomical classification (Kavishree et al., 2008). The study of edible native strains such as Pleurotus levis (Berk. & M. A. Curtis) Singer could offer new market alternatives based on their morphological, organoleptic and nutritional characteristics among others. Therefore, the aim of this study was to determine and compare the fatty acid profile between Pleurotus ostreatus and P. levis. Additionally, the nutritional value of these mushrooms was also evaluated.
]]> In this study, three strains of Pleurotus genus were used: P. ostreatus (IE-137), P. levis (IE-771) as well as a commercial Pleurotus strain. The first two are stored at the Ceparium of the Institute of Ecology (IE) in Xalapa, Mexico, and were grown on barley straw (S) following the general methodology of Gaitán-Hernández et al. (2006). The third mushroom (Pleurotus sp.) used was "Hongos San Miguel" and was purchased in a local commercial store grown on wheat straw-corn bagasse. Additionally, P. levis was also cultivated in a mixture (M) of barley straw-maguey bagasse 1:1 (w/w).Approximately 500 g of sporophores and stipe of each mushroom were lyophilized (LABCONCO lyophilizer model 77530). Once dry, they were reduced to a fine powder using a food processor (Moulinex). For lipid extraction, about 4 g of each sample were weighed and extracted for 20 h in a Soxhlet apparatus with 200 mL of redistilled hexane (AOAC). Three extractions were performed for each mushroom species, removing the solvent by distillation under reduced pressure.
Fatty acids were hydrolyzed and methylated with borontrifluoride 14% in metanol (BF3-MeOH, Sigma-Aldrich) and the derivatives were extracted using hexane (Yilmaz et al., 2006; Pedneault et al., 2007; Ribeiro et al., 2009).The methyl esters were identified and quantified using a gas Chromatograph coupled to a mass spectrometer (Agilent Technologies 6890N). Gas chromatography was carried out using He as carrier gas at a flow of lmL/min at a pressure of 24.87 psi. To identify volatile derivatives, the mass spectra obtained for each methyl ester were compared to the database (HP Chemstation-NIST 05 Mass spectral search program, version 2.Od). A comparison using a standard of fatty acid methyl ester (F.A.M.E mix, C8:C22, catalog No. 18920-1AMP, Sigma-Aldrich), analyzed under the same conditions, was also made. Means and standard deviations of the values of the major fatty acids were obtained as percentages. The data obtained were processed using an analysis of variance (ANOVA) with post hoc Tukey test at 0.05% to determine significant differences amongthe means, using the Statistica 7.0 software.
Results showed that linoleic acid was the main fatty acid found in Pleurotus ostreatus as in P. levis grown on S substrate (Table 1), followed by oleic and palmitic FAs and the same result was found for the commercial mushroom grown on wheat straw-corn bagasse, this results agree with Reis et al. (2012) who reported the same profile for Pleurotus FAs. However, when P. levis grown on M was analyzed, the major FA encountered was oleic, followed by linoleic and palmitic FAs (Table 1). It has been reported that, when compared with plants, animals, bacteria and yeasts, fungi have a less diversity of FAs, usually containing six or seven at the most (Stahl and Klug, 1996). In the majority of the studies reported for wild and cultivated edible mushrooms, the main FA found is linoleic (CI 8: 2) followed by oleic (CI 8: 1) and palmitic (C16: 0) (Barros et al., 2008; Diez and Alvarez, 2001; Gutiérrez et al., 2002; Jing et al., 2012). Moreover, in the present work the presence of elaidic acid (CI 8:1 trans-9) was detected in a very small amount m Pleurotus levis grown on both substrates, S and M. On the other hand Pleurotus sp. contains 5 % of this isomer of oleic acid (Table 1). Elaidic acid was first reported in wild edible mushrooms from Canada by Pedneault et al., (2008). This is a "trans" acid that is usually found in aliments such as milk fat, animal tissue of ruminants and occasionally in oil seeds. Furthermore, the decapentanoic acid content (CI5: 0) is statistically different in the three species of Pleurotus. In this regard Ergönul et al., (2012) report that the odd numbered FAs were detected in trace amounts in edible mushrooms in Turkey, in contrast to edible mushrooms in northwest Spain as Tricholoma portentosum and T. terreum, where FAs have not been identified with an odd number (Diez and Alvarez, 2001). This is relevant because the FA may contain valuable taxonomic and physiological information (Pedneault et al., 2008) and in particular a minimum quantity of FAs can prove to be distinctive of certain species (Stahl and Klug, 1996). However, in some studies in Basidiomycetes, it has not been possible to identify a minimum quantity of FAs due to inadequate methodologies used in their extraction (Brondz et al., 2004). From a nutritional standpoint, the ratios PUFA/SFA of the mushrooms studied had values above 0.45, indicating that they are healthy foods since it has been reported that ratios greater than or equal to 0.45 have a strong hypocholesterolemic effect (Chang and Huang, 1998; Takahashi and Carvalho, 2010). It is worth noticing that P. ostreatus presented the best value for this ratio and for P. levis is the first time that this parameter was evaluated.
Figure 1 shows the proportions of saturated and unsaturated FAs in both Pleurotus species grown on barley straw as well as the commercial mushroom and P. levis cultivated on maguey bagasse- barley straw. When comparing P. levis and P. ostreatus grown on P, the proportion of SEA, MUFA and PUFA showed similar behavior, the main FA being linoleic FA, followed by MUFA and SFA to a lesser extent. Nevertheless, when comparing the composition of FA of P. levis on Ρ and M, unlike the mushrooms grown on P, the majority of FAs on M were monounsaturated which shows that a change in the composition of the substrate can generate a change in the profiles of FAs (Erwin, 1973). Both P. ostreatus and the commercial mushroom showed the highest values of PUFA, and the lowest proportion of SFA was found only in the commercial mushroom. In all cases, the predominant FAs were unsaturated, which is consistent with those reported for other edible species like Russula delica, Boletus, edulis, Cantharellus cibarius, Amanita caesarea among others (Heleno et al., 2009; Ribeiro et al., 2009). The studied strains proved to be excellent food, due to their low saturated fat content and they can be consumed by people whit high blood cholesterol levels. This study opens the possibility for further research based on the characteristics of the strains and the type of substrate used in mushroom cultivation, with the aim of improving nutritional quality relating to FAs and obtain commercial mushrooms with higher coefficients of PUFA/SFA.
Acknowledgements
Authors thank the Consejo Nacional de Ciencia y Tecnología (CONACyT) for the postgraduate scholarship awarded to the first author (fellow No. 223892) and financial support (CB: 181820), Susana Sanchez (Unidad de Servicios de Apoyo en Resolución Analítica), Janette Sandoval and Luis Juarez (Laboratorio de Alta Tecnologia de Xalapa) of Universidad Veracruzana, Xalapa, México, for their technical help.
References
]]>AOAC, 1990. Official method of analysis, 15th ed. Association of Official Analytical Chemist, Inc, Arlington. [ Links ]
Barros, L., T. Cruz, P. Baptista, L.M. Estevinho, I.C.F.R. Ferreira, 2008. Wild and commercial mushrooms as source of nutrients and nutraceuticals. Food and Chemical Toxicology 46:2742-2747. [ Links ]
Brondz, I., K. Fteiland, D. Ekeberg, 2004. Multivariate analysis of fatty acids in spores of higher basidiomycetes: a new method for chemotaxonomical classification of fungi. Journal of Chromatography 800:303-307. [ Links ]
Chang, N.W., P.C. Huang, 1998. Effects of the ratio of polyunsaturated and monounsaturated fatty acids to saturated fatty acids on rat plasma and liver lipid concentrations. Lipids 33:481-487. [ Links ]
Chang, S.T., J. A. Buswell, 1996. Mushroom nutriceuticals. World Journal of Microbiology and Biotechnology 12:473-476. [ Links ]
]]>Chang, S.T., P.G. Miles, 2004. Mushrooms: cultivation, nutritional value, medicinal effect, and environmental impact. CRC Press, Boca Ratón, 453 p. [ Links ]
Combet, E.,J. Henderson,D.C. Eastwood, K.S. Burton, 2006. Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317-326. [ Links ]
Diez-Alvarez, V.A., A. Alvarez, 2001. Compositional and nutritional studies on two wild edible mushrooms from northwest Spain. Food Chemistry 75:417-422. [ Links ]
Ergönul, P. G., B. Ergönul, F. Kalyoncu, I. Akata, 2012. Fatty acid compositions of five wild edible mushroom species collected from Turkey. International Journal of Pharmacology 8:463-466. [ Links ]
Erwin J., 1973. Comparative biochemistry of fatty acids in eukaryotic microorganisms. In: Erwin J.A. (ed.), Lipids and biomembranes of eukaryotic microorganisms. Academic Press, New York, pp. 41-143. [ Links ]
]]>Gaitán-Hernández R., D. Salmones, R. Pérez-Merlo, G. Mata, 2006. Manual práctico del cultivo de setas: aislamiento, siembra y producción, Instituto de Ecología, Xalapa, 56 p. [ Links ]
Gaitán-Hernández R., D. Salmones, R. Pérez-Merlo, G. Mata, 2009. Evaluación de la eficiencia biológica de cepas de Pleurotus pulmonarius en paja de cebada fermentada. Revista Mexicana de Micologia 30:63-71. [ Links ]
Gutiérrez, Α., J.C. del Río, M.J. Martínez-ífiigo, J. Martínez, A.T. Martínez, 2002. Production of new unsaturated lipids during wood decay by ligninolytic basidiomycetes.Applied and Environmental Microbiology 68:1344-1350. [ Links ]
Heleno, S.A., L. Barros, M.J. Sousa, A. Martins, I.C.F.R. Ferreira, 2009. Study and characterization of selected nutrients in wild mushrooms from Portugal by gas chromatography and high performance liquid chromatography. Microchemical Journal 93:195-199. [ Links ]
Jabaji-Hare, S., 1988. Lipid and fatty acid profiles of some vesicular-arbuscular mycorrhizal fungi: contribution to taxonomy. Mycologia 80:622-629. [ Links ]
]]>Jing N., J. Shi, G. Li, Z. Sun, J. You, 2012. Determination of fatty acids from mushrooms using high performance liquid chromatography with fluorescence detection and on line mass spectrometry. Food Research International 48:155-163. [ Links ]
Kavishree, S., J. Hemavathy, B.R. Lokesh, M.N. Shashirekha, S. Rajarathnam, 2008. Fat and fatty acids of Indian edible mushrooms. Food Chemistry 106:597-602. [ Links ]
Lechevalier, H., M.P. Lechevalier. 1988. Chemotaxonomic use of lipids: an overview. In: Ratledge, C., S.G. Wilkinson (eds.), Microbial lipids Vol. 1. Academic Press, London, pp. 869—902. [ Links ]
Pedneault, K., P. Angers, A. Gosselin, R.J. Tweddell, 2008. Fatty acid profiles of polar and neutral lipids of ten species of higher basidiomycetes indigenous to eastern Canada. Mycological Research 112:1428—1434. [ Links ]
Reis, F.S., L. Barros, A. Martins, I.C.F.R. Ferreira, 2012. Chemical composition and nutritional value of the most widely appreciated cultivated mushrooms: an inter-species comparative study. Food and Chemical Toxicology 50:191-197. [ Links ]
]]>Ribeiro, Β., P. Guedes de Pinho, P.B. Andrade, P. Baptista, P.Valentão, 2009. Fatty acid composition of wild edible mushrooms species: a comparative study. Microchemical Journal 93:29-35. [ Links ]
Sinanoglou, V.J., I.F. Strati, S.M. Bratakos, C. Proestos, P. Zoumpoulakis, S. Miniadis-Meimaroglou, 2013. On the combined application of iatroscan TLC-FID and GC-FID to identify total, neutral, and polar lipids and their fatty acids extracted from foods. ISRN Chromatography, article ID 859024,8 p. [ Links ]
Stahl, P.D., M.J. Klug, 1996.Characterization and differentiation of filamentous fungi based on fatty acid composition. Applied and Environmental Microbiology 62:4136-4146. [ Links ]
Takahashi, J.A., S.A. Carvalho, 2010. Nutritional potential of biomass and metabolites from filamentous fungi. In: Méndez-Vila, A. (ed.), Current Research Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, Formatex, Badajoz, pp. 1126-1135. [ Links ]
Yilmaz, N., M. Solmaz, I. Türkekul, M. Elmastas, 2006. Fatty acid composition in some wild edible mushrooms growing in the middle Black Sea region of Turkey Food Chemistry 99:168-174. [ Links ]
]]>