Pleurotus Mushrooms Content in Glucans and Ergosterol Assessed by ATR-FTIR Spectroscopy and Multivariate Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Biological Material
2.2. Cultivation of Pleurotus Species
2.3. Determination of Glucan and Ergosterol Content
2.4. Attenuated Total Reflection—Fourier Transform Infrared (ATR-FTIR) Analysis
2.5. Multivariate Analysis
3. Results and Discussion
3.1. Glucan and Ergosterol Contents of Pleurotus Species
3.2. Qualitative Analysis of Pleurotus Mushrooms Based on ATR-FTIR Spectroscopy
3.2.1. Spectral Comparison of P. ostreatus and P. eryngii Mushrooms Cultivated on Different Substrates
3.2.2. Comparative Evaluation of Pleurotus Species
3.3. Principal Component Analysis (PCA)
3.4. Prediction of Mushrooms Glucans Content
3.5. Prediction of Mushrooms Ergosterol Content
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Royse, D.J.; Baars, J.; Tan, Q. Current overview of mushroom production in the world. In Edible and Medicinal Mushrooms; Diego, C.Z., Pardo-Giménez, A., Eds.; Wiley Online Library location: Hoboken, NJ, USA, 2017; pp. 5–13. [Google Scholar]
- Koutrotsios, G.; Larou, E.; Mountzouris, K.C.; Zervakis, G.I. Detoxification of olive mill wastewater and bioconversion of olive crop residues into high-value-added biomass by the choice edible mushroom Hericium erinaceus. Biotechnol. Appl. Biochem. 2016, 180, 195–209. [Google Scholar] [CrossRef]
- Koutrotsios, G.; Mountzouris, K.C.; Chatzipavlidis, I.; Zervakis, G.I. Bioconversion of lignocellulosic residues by Agrocybe cylindracea and Pleurotus ostreatus mushroom fungi–Assessment of their effect on the final product and spent substrate properties. Food Chem. 2014, 161, 127–135. [Google Scholar] [CrossRef] [PubMed]
- Julian, A.V.; Reyes, R.G.; Eguchi, F. Agro-industrial waste conversion into medicinal mushroom cultivation. In Encyclopedia of Environmental Health, 2nd ed.; Nriagu, J., Ed.; Elsevier: Oxford, UK, 2019; pp. 13–20. [Google Scholar]
- Zervakis, G.I.; Koutrotsios, G. Solid-state fermentation of plant residues and agro-industrial wastes for the production of medicinal mushrooms. In Medicinal Plants and Fungi: Recent Advances in Research and Development; Agrawal, D.C., Tsay, H.-S., Shyur, L.-F., Wu, Y.-C., Wang, S.-Y., Eds.; Springer: Singapore, 2017; pp. 365–396. [Google Scholar]
- Mediterranean Plant Specialist Group. The Top 50 Mediterranean Island Plants UPDATE 2017. Available online: http://top50.iucn-mpsg.org/species/39 (accessed on 23 March 2020).
- Gargano, M.L.; van Griensven, L.J.L.D.; Isikhuemhen, O.S.; Lindequist, U.; Venturella, G.; Wasser, S.P.; Zervakis, G.I. Medicinal mushrooms: Valuable biological resources of high exploitation potential. Plant Biosyst. Int. J. Deal. All Asp. Plant Biol. 2017, 151, 548–565. [Google Scholar] [CrossRef]
- Synytsya, A.; Míčková, K.; Synytsya, A.; Jablonský, I.; Spěváček, J.; Erban, V.; Kováříková, E.; Čopíková, J. Glucans from fruit bodies of cultivated mushrooms Pleurotus ostreatus and Pleurotus eryngii: Structure and potential prebiotic activity. Carbohydr. Polym. 2009, 76, 548–556. [Google Scholar] [CrossRef]
- Sari, M.; Prange, A.; Lelley, J.I.; Hambitzer, R. Screening of beta-glucan contents in commercially cultivated and wild growing mushrooms. Food Chem. 2017, 216, 45–51. [Google Scholar] [CrossRef] [PubMed]
- Koutrotsios, G.; Patsou, M.; Mitsou, E.K.; Bekiaris, G.; Kotsou, M.; Tarantilis, P.A.; Pletsa, V.; Kyriacou, A.; Zervakis, G.I. Valorization of olive by-products as substrates for the cultivation of Ganoderma lucidum and Pleurotus ostreatus mushrooms with enhanced functional and prebiotic properties. Catalysts 2019, 9, 537. [Google Scholar] [CrossRef] [Green Version]
- De Silva, D.D.; Rapior, S.; Fons, F.; Bahkali, A.H.; Hyde, K.D. Medicinal mushrooms in supportive cancer therapies: An approach to anti-cancer effects and putative mechanisms of action. Fungal Divers. 2012, 55, 1–35. [Google Scholar] [CrossRef]
- Jasinghe, V.J.; Perera, C.O.; Sablani, S.S. Kinetics of the conversion of ergosterol in edible mushrooms. J. Food Eng. 2007, 79, 864–869. [Google Scholar] [CrossRef]
- Koutrotsios, G.; Kalogeropoulos, N.; Kaliora, A.C.; Zervakis, G.I. Toward an increased functionality in oyster (Pleurotus) mushrooms produced on grape marc or olive mill wastes serving as sources of bioactive compounds. J. Agric. Food Chem. 2018, 66, 5971–5983. [Google Scholar] [CrossRef]
- Koutrotsios, G.; Kalogeropoulos, N.; Stathopoulos, P.; Kaliora, A.C.; Zervakis, G.I. Bioactive compouds and antioxidant activity exhibit high intraspecific variability in Pleurotus ostreatus mushrooms and correlate well with cultivation performance parameters. World J. Microbiol. Biotechnol. 2017, 33, 98. [Google Scholar] [CrossRef]
- Hoa, H.T.; Wang, C.L.; Wang, C.H. The effects of different substrates on the growth, yield, and nutritional composition of two oyster mushrooms (Pleurotus ostreatus and Pleurotus cystidiosus). Mycobiology 2015, 43, 423–434. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ntougias, S.; Gaitis, F.; Katsaris, P.; Skoulika, S.; Iliopoulos, N.; Zervakis, G.I. The effects of olives harvest period and production year on olive mill wastewater properties—Evaluation of Pleurotus strains as bioindicators of the effluent’s toxicity. Chemosphere 2013, 92, 399–405. [Google Scholar] [CrossRef] [PubMed]
- Tournour, H.H.; Segundo, M.A.; Magalhães, L.M.; Barreiros, L.; Queiroz, J.; Cunha, L.M. Valorization of grape pomace: Extraction of bioactive phenolics with antioxidant properties. Ind. Crop. Prod. 2015, 74, 397–406. [Google Scholar] [CrossRef]
- Romero, C.; Medina, E.; Mateo, M.A.; Brenes, M. New by-products rich in bioactive substances from the olive oil mill processing. J. Sci. Food Agric. 2018, 98, 225–230. [Google Scholar] [CrossRef] [Green Version]
- Teixeira, A.; Baenas, N.; Dominguez-Perles, R.; Barros, A.; Rosa, E.; Moreno, D.A.; Garcia-Viguera, C. Natural bioactive compounds from winery by-products as health promoters: A review. Int. J. Mol. Sci. 2014, 15, 15638–15678. [Google Scholar] [CrossRef] [Green Version]
- Cullen, P.J.; O’Donnell, C.P.; Fagan, C.C. Benefits and challenges of adopting PAT for the food industry. In Process Analytical Technology for the Food Industry; O’Donnell, C.P., Fagan, C., Cullen, P.J., Eds.; Springer: New York, NY, USA, 2014; pp. 1–5. [Google Scholar]
- Roussel, S.; Preys, S.; Chauchard, F.; Lallemand, J. Multivariate data analysis (chemometrics). In Process Analytical Technology for the Food Industry; O’Donnell, C.P., Fagan, C., Cullen, P.J., Eds.; Springer: New York, NY, USA, 2014; pp. 7–59. [Google Scholar]
- Venetsanou, A.; Anastasaki, E.; Gardeli, C.; Tarantilis, P.A.; Pappas, C.S. Estimation of antioxidant activity of different mixed herbal infusions using attenuated total reflectance Fourier transform infrared spectroscopy and chemometrics. Emir. J. Food Agric. 2017, 29, 149–155. [Google Scholar] [CrossRef] [Green Version]
- Sousa, N.; Moreira, M.J.; Saraiva, C.; De Almeida, J.M.M.M. Applying Fourier transform mid infrared spectroscopy to detect the adulteration of Salmo salar with Oncorhynchus mykiss. Foods 2018, 7, 55. [Google Scholar] [CrossRef] [Green Version]
- Rodriguez-Saona, L.E.; Allendorf, M.E. Use of FTIR for rapid authentication and detection of adulteration of food. Annu. Rev. Food Sci. Technol. 2011, 2, 467–483. [Google Scholar] [CrossRef]
- Erwanto, Y.; Muttaqien, A.T.; Sugiyono; Sismindari; Rohman, A. Use of Fourier transform infrared (FTIR) spectroscopy and chemometrics for analysis of lard adulteration in “Rambak” crackers. Int. J. Food Prop. 2016, 19, 2718–2725. [Google Scholar] [CrossRef] [Green Version]
- Fagan, C.C. Infrared spectroscopy. In Process Analytical Technology for the Food Industry; O’Donnell, C.P., Fagan, C., Cullen, P.J., Eds.; Springer: New York, NY, USA, 2014; pp. 73–101. [Google Scholar]
- Lecellier, A.; Mounier, J.; Gaydou, V.; Castrec, L.; Barbier, G.; Ablain, W.; Manfait, M.; Toubas, D.; Sockalingum, G.D. Differentiation and identification of filamentous fungi by high-throughput FTIR spectroscopic analysis of mycelia. Int. J. Food Microbiol. 2014, 168, 32–41. [Google Scholar] [CrossRef]
- Santos, C.; Fraga, M.E.; Kozakiewicz, Z.; Lima, N. Fourier transform infrared as a powerful technique for the identification and characterization of filamentous fungi and yeasts. Res. Microbiol. 2010, 161, 168–175. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zervakis, G.I.; Bekiaris, G.; Tarantilis, P.; Pappas, C.S. Rapid strain classification and taxa delimitation within the edible mushroom genus Pleurotus through the use of diffuse reflectance infrared Fourier transform (DRIFT) spectroscopy. Fungal Biol. 2012, 116, 715–728. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.Y.; Li, J.Q.; Liu, H.G.; Wang, Y.Z. Attenuated total reflection-Fourier transform infrared spectroscopy (ATR-FTIR) combined with chemometrics methods for the classification of Lingzhi species. Molecules 2019, 24, 2210. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yao, S.; Li, J.; Li, T.; Liu, H.; Wang, Y. Discrimination of Boletaceae mushrooms based on data fusion of FT-IR and ICP–AES combined with SVM. Int. J. Food Prop. 2018, 21, 255–266. [Google Scholar] [CrossRef]
- Chen, Y.; Xie, M.Y.; Yan, Y.; Zhu, S.B.; Nie, S.P.; Li, C.; Wang, Y.X.; Gong, X.F. Discrimination of Ganoderma lucidum according to geographical origin with near infrared diffuse reflectance spectroscopy and pattern recognition techniques. Anal. Chim. Acta 2008, 618, 121–130. [Google Scholar] [CrossRef]
- O’Gorman, A.; Downey, G.; Gowen, A.A.; Barry-Ryan, C.; Frias, J.M. Use of Fourier transform infrared spectroscopy and chemometric data analysis to evaluate damage and age in mushrooms (Agaricus bisporus) grown in Ireland. J. Agric. Food Chem. 2010, 58, 7770–7776. [Google Scholar] [CrossRef] [Green Version]
- Sapozhnikova, Y.; Byrdwell, W.C.; Lobato, A.; Romig, B. Effects of UV-B radiation levels on concentrations of phytosterols, ergothioneine and polyphenolic compounds in mushroom powders used as dietary supplements. J. Agric. Food Chem. 2014, 62, 3034–3042. [Google Scholar] [CrossRef]
- Phillips, K.M.; Ruggio, D.M.; Horst, R.L.; Minor, B.; Simon, R.R.; Feeney, M.J.; Byrdwell, W.C.; Haytowitz, D.B. Vitamin D and sterol composition of 10 types of mushrooms from retail suppliers in the United States. J. Agric. Food Chem. 2011, 59, 7841–7853. [Google Scholar] [CrossRef]
- Teichmann, A.; Dutta, P.C.; Staffas, A.; Jägerstad, M. Sterol and vitamin D2 concentrations in cultivated and wild grown mushrooms: Effects of UV irradiation. Lwt Food Sci. Technol. 2007, 40, 815–822. [Google Scholar] [CrossRef]
- Savitzky, A.; Golay, M.J.E. Smoothing and differentiation of data by simplified least squares procedures. Anal. Chem. 1964, 36, 1627–1639. [Google Scholar] [CrossRef]
- Vinutha, H.P.; Poornima, B.; Sagar, B.M. Detection of Outliers Using Interquartile Range Technique from Intrusion Dataset; Springer: Singapore, 2018; pp. 511–518. [Google Scholar]
- Hotelling, H. The generalization of Student’s ratio. Inst. Math. Stat. 1931, 360–378. [Google Scholar] [CrossRef]
- Martens, H.; Martens, M. Modified Jack-knife estimation of parameter uncertainty in bilinear modelling by partial least squares regression (PLSR). Food Qual. Prefer. 2000, 11, 5–16. [Google Scholar] [CrossRef]
- Olivieri, A.C. The classical least-squares model. In Introduction to Multivariate Calibration: A Practical Approach; Springer International Publishing: Cham, Germany, 2018; pp. 19–38. [Google Scholar]
- Movasaghi, Z.; Rehman, S.; Rehman, I.U. Fourier transform infrared (FTIR) spectroscopy of biological tissues. Appl. Spectrosc. Rev. 2008, 43, 134–179. [Google Scholar] [CrossRef]
- Oliveira, R.N.; Mancini, M.C.; Oliveira, F.C.S.D.; Passos, T.M.; Quilty, B.; Thiré, R.M.D.S.M.; McGuinness, G.B. FTIR analysis and quantification of phenols and flavonoids of five commercially available plants extracts used in wound healing. Matéria 2016, 21, 767–779. [Google Scholar] [CrossRef] [Green Version]
- Socrates, G. Infrared and Raman Characteristic Group Frequencies: Tables and Charts, 3rd ed.; John Wily & Sons Ltd.: Chichester, UK, 2001. [Google Scholar]
- Moţ, A.C.; Silaghi-Dumitrescu, R.; Sârbu, C. Rapid and effective evaluation of the antioxidant capacity of propolis extracts using DPPH bleaching kinetic profiles, FT-IR and UV–vis spectroscopic data. J. Food Compos. Anal. 2011, 24, 516–522. [Google Scholar] [CrossRef]
- Zervakis, G.I.; Ntougias, S.; Gargano, M.L.; Besi, M.I.; Polemis, E.; Typas, M.A.; Venturella, G. A reappraisal of the Pleurotus eryngii complex–New species and taxonomic combinations based on the application of a polyphasic approach, and an identification key to Pleurotus taxa associated with Apiaceae plants. Fungal Biol. 2014, 118, 814–834. [Google Scholar] [CrossRef]
- Coates, J. Interpretation of infrared spectra: A practical approach interpretation of infrared spectra. In Encyclopedia of Analytical Chemistry; Meyers, R.A., Ed.; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2000; pp. 10815–10837. [Google Scholar]
- Bro, R.; Rinnan, Å.; Faber, N.M. Standard error of prediction for multilinear PLS: 2. Practical implementation in fluorescence spectroscopy. Chemom. Intell. Lab. Syst. 2005, 75, 69–76. [Google Scholar] [CrossRef]
- Olivieri, A.C. Chemometrics and multivariate calibration. In Introduction to Multivariate Calibration: A Practical Approach; Springer International Publishing: Cham, Germanty, 2018; pp. 1–17. [Google Scholar]
- Fazio, A.; La Torre, C.; Caroleo, M.C.; Caputo, P.; Plastina, P.; Cione, E. Isolation and purification of glucans from an italian cultivar of Ziziphus jujuba Mill. and in vitro effect on skin repair. Molecules 2020, 25, 968. [Google Scholar] [CrossRef] [Green Version]
- Ciolacu, D.; Ciolacu, F.; Popa, V.I. Amorphous cellulose-structure and characterization. Cellul. Chem. Technol. 2011, 45, 13–21. [Google Scholar]
- Ma, Y.; He, H.; Wu, J.; Wang, C.; Chao, K.; Huang, Q. Assessment of polysaccharides from mycelia of genus Ganoderma by mid-infrared and near-infrared spectroscopy. Sci. Rep. 2018, 8, 10. [Google Scholar] [CrossRef]
- Chen, Y.; Xie, M.; Zhang, H.; Wang, Y.; Nie, S.; Li, C. Quantification of total polysaccharides and triterpenoids in Ganoderma lucidum and Ganoderma atrum by near infrared spectroscopy and chemometrics. Food Chem. 2012, 135, 268–275. [Google Scholar] [CrossRef]
- Engelsen, S.B. Near infrared spectroscopy—A unique window of opportunities. Nir. News 2016, 27, 14–17. [Google Scholar] [CrossRef]
- Ríos-Reina, R.; García-González, D.L.; Callejón, R.M.; Amigo, J.M. NIR spectroscopy and chemometrics for the typification of Spanish wine vinegars with a protected designation of origin. Food Control 2018, 89, 108–116. [Google Scholar] [CrossRef]
- Gracia, M.-B.; Armstrong, P.R.; Rongkui, H.; Mark, S. Quantification of betaglucans, lipid and protein contents in whole oat groats (Avena sativa L.) using near infrared reflectance spectroscopy. J. Near Infrared Spectrosc. 2017, 25, 172–179. [Google Scholar] [CrossRef]
- Brown, C.; Martin, A.P.; Grof, C.P.L. The application of Fourier transform mid-infrared (FTIR) spectroscopy to identify variation in cell wall composition of Setaria italica ecotypes. J. Integr. Agric. 2017, 16, 1256–1267. [Google Scholar] [CrossRef]
- Li, Y.; Zhang, J.; Liu, F.; Xu, F.; Wang, Y.; Zhang, J.-Y. Prediction of total polysaccharides content in P. notoginseng using FTIR combined with SVR. Spectrosc. Spectr. Anal. 2018, 38, 1696–1701. [Google Scholar] [CrossRef]
- Esquerre, C.; Gowen, A.A.; O’Donnell, C.P.; Downey, G. Initial studies on the quantitation of bruise damage and freshness in mushrooms using visible-near-infrared spectroscopy. J. Agric. Food Chem. 2009, 57, 1903–1907. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Zhang, J.; Li, T.; Liu, H.; Li, J.; Wang, Y. Geographical traceability of wild Boletus edulis based on data fusion of FT-MIR and ICP-AES coupled with data mining methods (SVM). Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2017, 177, 20–27. [Google Scholar] [CrossRef]
- Li, Y.; Wang, Y. Synergistic strategy for the geographical traceability of wild Boletus tomentipes by means of data fusion analysis. Microchem. J. 2018, 140, 38–46. [Google Scholar] [CrossRef]
- Shapaval, V.; Brandenburg, J.; Blomqvist, J.; Tafintseva, V.; Passoth, V.; Sandgren, M.; Kohler, A. Biochemical profiling, prediction of total lipid content and fatty acid profile in oleaginous yeasts by FTIR spectroscopy. Biotechnol. Biofuels 2019, 12, 140. [Google Scholar] [CrossRef] [Green Version]
- Bouzidi, N.; Daghbouche, Y.; El Hattab, M.; Aliche, Z.; Culioli, G.; Piovetti, L.; Garrigues, S.; de la Guardia, M. Determination of total sterols in brown algae by Fourier transform infrared spectroscopy. Anal. Chim. Acta 2008, 616, 185–189. [Google Scholar] [CrossRef] [PubMed]
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Bekiaris, G.; Tagkouli, D.; Koutrotsios, G.; Kalogeropoulos, N.; Zervakis, G.I. Pleurotus Mushrooms Content in Glucans and Ergosterol Assessed by ATR-FTIR Spectroscopy and Multivariate Analysis. Foods 2020, 9, 535. https://doi.org/10.3390/foods9040535
Bekiaris G, Tagkouli D, Koutrotsios G, Kalogeropoulos N, Zervakis GI. Pleurotus Mushrooms Content in Glucans and Ergosterol Assessed by ATR-FTIR Spectroscopy and Multivariate Analysis. Foods. 2020; 9(4):535. https://doi.org/10.3390/foods9040535
Chicago/Turabian StyleBekiaris, Georgios, Dimitra Tagkouli, Georgios Koutrotsios, Nick Kalogeropoulos, and Georgios I. Zervakis. 2020. "Pleurotus Mushrooms Content in Glucans and Ergosterol Assessed by ATR-FTIR Spectroscopy and Multivariate Analysis" Foods 9, no. 4: 535. https://doi.org/10.3390/foods9040535