Pretreatment of Grape Stalks by Fungi: Effect on Bioactive Compounds, Fiber Composition, Saccharification Kinetics and Monosaccharides Ratio
Abstract
:1. Introduction
2. Materials and Methods
2.1. Grape Stalks and Fungal Strains
2.2. Fungal Solid State Fermentation of Grape Stalks
2.3. Antioxidant Activities
2.4. Determination of Total Polyphenols and Lignocellulose Composition
2.5. Enzyme Assays
2.6. Scanning Electron Microscopy (SEM)
2.7. Enzymatic Hydrolysis of Holocellulose
2.8. Quantification of Soluble Sugars and HPLC Analysis
2.9. Data Processing and Statistical Analysis
3. Results and Discussion
3.1. Antioxidant Activities
3.2. Pretreatment: Lignocellulose Composition, Enzymatic Activities and PCA Analysis
3.3. Enzymatic Saccharification
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Oh, I.; Yoo, W.J.; Yoo, Y. Impact and Interactions of Policies for Mitigation of Air Pollutants and Greenhouse Gas Emissions in Korea. Int. J. Environ. Res. Public Health 2019, 16, 1161. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, Y.; Chiu, Y.H.; Lin, T.Y. Research on New and Traditional Energy Sources in OECD Countries. Int. J. Environ. Res. Public Health 2019, 16, 1122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Oh, Y.K.; Hwang, K.R.; Kim, C.; Kim, J.R.; Lee, J.S. Recent developments and key barriers to advanced biofuels: A short review. Bioresour. Technol. 2018, 257, 320–333. [Google Scholar] [CrossRef] [PubMed]
- International Renewable Energy Agency (IRENA). Renewable Energy Prospects for the European Union (REmap Analysis Conducted by the International Renewable Energy Agency in Co-Operation with the European Commission); International Renewable Energy Agency: Brussels, Belgium, 2018. [Google Scholar]
- Sindhu, R.; Binod, P.; Pandey, A. Biological pretreatment of lignocellulosic biomass—An overview. Bioresour. Technol. 2016, 199, 76–82. [Google Scholar] [CrossRef]
- Nicolini, L.; Volpe, C.; Pezzotti, A.; Carilli, A. Changes in in-vitro digestibility of orange peels and distillery grape stalks after solid-state fermentation by higher fungi. Bioresour. Technol. 1993, 45, 17–20. [Google Scholar] [CrossRef]
- Moldes, D.; Lorenzo, M.; Sanromán, M.A. Different proportions of laccase isoenzymes produced by submerged cultures of Trametes versicolor grown on lignocellulosic wastes. Biotechnol. Lett. 2004, 26, 327–330. [Google Scholar] [CrossRef]
- Levin, L.; Diorio, L.; Grassi, E.; Forchiassin, F. Grape stalks as substrate for white rot fungi, lignocellulolytic enzyme production and dye decolorization. Rev. Argent. Microbiol. 2012, 44, 105–112. [Google Scholar]
- Wan, C.; Li, Y. Fungal pretreatment of lignocellulosic biomass. Biotechnol. Adv. 2012, 30, 1447–1457. [Google Scholar] [CrossRef]
- Isikgor, F.H.; Becer, C.R. Lignocellulosic biomass: A sustainable platform for the production of bio-based chemicals and polymers. Polym. Chem. 2015, 6, 4497–4559. [Google Scholar] [CrossRef] [Green Version]
- Bhutto, A.W.; Qureshi, K.; Harija, K.; Abro, R.; Abbas, T.; Bazmi, A.A.; Karim, S.; Yu, G. Insight into progress in pre-treatment of lignocellulosic biomass. Energy 2017, 122, 724–745. [Google Scholar] [CrossRef]
- Zabed, H.M.; Akter, S.; Yun, J.; Zhang, G.; Awad, F.N.; Qi, X.; Sahu, J.N. Recent advances in biological pretreatment of microalgae and lignocellulosic biomass for biofuel production. Renew. Sustain. Energy Rev. 2019, 105, 105–128. [Google Scholar] [CrossRef]
- Den, W.; Sharma, V.K.; Lee, M.; Nadadur, G.; Varma, R.S. Lignocellulosic biomass transformations via greener oxidative pretreatment processes: Access to energy and value-added chemicals. Front. Chem. 2018, 6, 141. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kumar, M.N.; Ravikumar, R.; Thenmozhi, S.; Kumar, M.R.; Shankar, M.K. Choice of pretreatment technology for sustainable production of bioethanol from lignocellulosic biomass: Bottle necks and recommendations. Waste Biomass Valoriz. 2019, 10, 1693–1709. [Google Scholar] [CrossRef]
- Baruah, J.; Nath, B.; Sharma, R.; Kumar, S.; Deka, R.; Baruah, D.; Kalita, E. Recent trends in the pretreatment of lignocellulosic biomass for value-added products. Front. Energy Res. 2018, 6, 141. [Google Scholar] [CrossRef]
- Ruiz-Dueñas, F.J.; Morales, M.; García, E.; Miki, Y.; Martínez, M.J.; Martínez, A.T. Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J. Exp. Bot. 2009, 60, 441–452. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, Y.; Yu, X.; Sun, Y.; Wang, G.; Chen, H.; Chen, G. Evaluation of screened lignin-degrading fungi for the biological pretreatment of corn stover. Sci. Rep. 2018, 8, 5385. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dinis, M.J.; Bezerra, R.M.F.; Nunes, F.; Dias, A.A.; Guedes, C.V.; Ferreira, L.M.; Cone, J.W.; Marques, G.S.; Barros, A.R.; Rodrigues, M.A. Modification of wheat straw lignin by solid state fermentation with white-rot fungi. Bioresour. Technol. 2009, 100, 4829–4835. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Moreno, S.; Scheyer, T.; Romano, C.S.; Vojnov, A.A. Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radic. Res. 2006, 40, 223–231. [Google Scholar] [CrossRef]
- Ozgen, M.; Reese, R.N.; Tulio, A.Z.; Scheerens, J.C.; Miller, A.R. Modified 2,2’-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid (ABTS) method to measure antioxidant capacity of selected small fruits and comparison to ferric reducing antioxidant power (FRAP) and 2, 2’-diphenyl-1-picrylhydrazyl (DPPH) methods. J. Agric. Food Chem. 2006, 54, 1151–1157. [Google Scholar] [CrossRef]
- Re, R.; Pellegrini, N.; Proteggente, A.; Pannala, A.; Yang, M.; Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic. Biol. Med. 1999, 26, 1231–1237. [Google Scholar] [CrossRef]
- Fernandes, J.M.C.; Sousa, R.M.O.; Fraga, I.; Sampaio, A.; Amaral, C.; Bezerra, R.M.F.; Dias, A.A. Fungal biodegradation and multi-level toxicity assessment of vinasse from distillation of winemaking by-products. Chemosphere 2020, 238, 124572. [Google Scholar] [CrossRef] [PubMed]
- Association of Official Analytical Chemists. Official Methods of Analysis, 15th ed.; Association of Official Analytical Chemists: Arlington, VA, USA, 1990. [Google Scholar]
- Robertson, J.B.; Van Soest, P.J. The detergent system of analysis and its application in human foods. In The Analysis of Dietary Fiber in Food; James, W.P.T., Theander, O., Eds.; Marcel Dekker: New York, NY, USA, 1981; pp. 123–158. [Google Scholar]
- Bezerra, R.M.F.; Dias, A.A. Discrimination among eight modified Michaelis–Menten kinetics models of cellulose hydrolysis with a large range of substrate/enzyme ratios: Inhibition by cellobiose. Appl. Biochem. Biotechnol. 2004, 112, 173–184. [Google Scholar] [CrossRef]
- Miller, G.L. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 1959, 31, 426–428. [Google Scholar] [CrossRef]
- Isah, T. Stress and defense responses in plant secondary metabolites production. Biol. Res. 2019, 52, 39. [Google Scholar] [CrossRef] [Green Version]
- Anastasiadi, M.; Pratsinis, H.; Kletsas, D.; Skaltsounis, A.-L.; Haroutounian, S.A. Grape stem extracts: Polyphenolic content and assessment of their in vitro antioxidant properties. LWT Food Sci. Technol. 2012, 48, 316–322. [Google Scholar] [CrossRef]
- Barros, A.; Gironés-Vilaplana, A.; Teixeira, A.; Collado-González, J.; Moreno, D.A.; Gil-Izquierdo, A.; Rosa, E.; Domínguez-Perles, R. Evaluation of grape (Vitis vinifera L.) stems from portuguese varieties as a resource of (poly) phenolic compounds: A comparative study. Food Res. Int. 2014, 65, 375–384. [Google Scholar] [CrossRef]
- García-Torreiro, M.; López-Abelairas, M.; Lu-Chau, T.; Lema, J. Fungal pretreatment of agricultural residues for bioethanol production. Ind. Crops Prod. 2016, 89, 486–492. [Google Scholar] [CrossRef]
- Sousa, D.; Venâncio, A.; Belo, I.; Salgado, J.M. Mediterranean agro-industrial wastes as valuable substrates for lignocellulolytic enzymes and protein production by solid-state fermentation. J. Sci. Food Agric. 2018, 98, 5248–5256. [Google Scholar] [CrossRef]
- Ping, L.; Brosse, N.; Sannigrahi, P.; Ragauskas, A. Evaluation of grape stalks as a bioresource. Ind. Crops Prod. 2011, 33, 200–204. [Google Scholar] [CrossRef]
- Spigno, G.; Maggi, L.; Amendola, D.; Dragoni, M.; De Faveri, D.M. Influence of cultivar on the lignocellulosic fractionation of grape stalks. Ind. Crops Prod. 2013, 46, 283–289. [Google Scholar] [CrossRef]
- Yu, H.; Du, W.; Zhang, J.; Ma, F.; Zhang, X.; Zhong, W. Fungal treatment of cornstalks enhances the delignification and xylan loss during mild alkaline pretreatment and enzymatic digestibility of glucan. Bioresour. Technol. 2010, 101, 6728–6734. [Google Scholar] [CrossRef] [PubMed]
- Isroi; Millati, R.; Syamsiah, S.; Niklasson, C.; Cahyanto, M.N.; Ludquist, K.; Taherzadeh, M.J. Biological pretreatment of lignocelluloses with white-rot fungi and its applications: A review. BioResources 2011, 6, 5224–5259. [Google Scholar]
- Pinto, P.A.; Dias, A.A.; Fraga, I.; Marques, G.; Rodrigues, M.A.; Colaço, J.; Sampaio, A.; Bezerra, R.M.F. Influence of ligninolytic enzymes on straw saccharification during fungal pretreatment. Bioresour. Technol. 2012, 111, 261–267. [Google Scholar] [CrossRef] [PubMed]
- Hofrichter, M.; Vares, T.; Kalsi, M.; Galkin, S.; Scheibner, K.; Fritsche, W.; Hatakka, A. Production of manganese peroxidase and organic acids and mineralization of 14C-labelled lignin (14C-DHP) during solid-state fermentation of wheat straw with the white rot fungus Nematoloma Frowardii. Appl. Environ. Microbiol. 1999, 65, 1864–1870. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pino, M.S.; Rodríguez-Jasso, R.M.; Michelin, M.; Flores-Gallegos, A.C.; Morales-Rodriguez, R.; Teixeira, J.A.; Ruiz, H.A. Bioreactor design for enzymatic hydrolysis of biomass under the biorefinery concept. Chem. Eng. J. 2018, 347, 119–136. [Google Scholar] [CrossRef] [Green Version]
- Salvachúa, D.; Prieto, A.; López-Abelairas, M.; Lu-Chau, T.; Martínez, A.T.; Martínez, M.J. Fungal pretreatment: An alternative in second-generation ethanol from wheat straw. Bioresour. Technol. 2011, 102, 7500–7506. [Google Scholar] [CrossRef] [Green Version]
- Janusz, G.; Pawlik, A.; Sulej, J.; Świderska-Burek, U.; Jarosz-Wilkołazka, A.; Paszczyński, A. Lignin degradation: Microorganisms, enzymes involved, genomes analysis and evolution. FEMS Microbiol. Rev. 2017, 41, 941–962. [Google Scholar] [CrossRef] [Green Version]
- Saha, B.C.; Qureshi, N.; Kennedy, G.J.; Cotta, M.A. Biological pretreatment of corn stover with white-rot fungus for improved enzymatic hydrolysis. Int. Biodeterior. Biodegrad. 2016, 109, 29–35. [Google Scholar] [CrossRef] [Green Version]
- Kumar, B.; Bhardwaj, N.; Agrawal, K.; Chaturvedi, V.; Verma, P. Current perspective on pretreatment technologies using lignocellulosic biomass: An emerging biorefinery concept. Fuel Process. Technol. 2020, 199, 106244. [Google Scholar] [CrossRef]
- Rodríguez-Chueca, J.; Alonso, E.; Singh, D.N. Photocatalytic mechanisms for peroxymonosulfate activation through the removal of methylene blue: A case study. Int. J. Environ. Res. Public Health 2019, 16, 198. [Google Scholar] [CrossRef] [Green Version]
- Lucas, M.S.; Dias, A.A.; Bezerra, R.M.; Peres, J.A. Gallic acid photochemical oxidation as a model compound of winery wastewaters. J. Environ. Sci. Health Part A Tox. Hazard. Subst. Environ. Eng. 2008, 43, 1288–1295. [Google Scholar] [CrossRef] [PubMed]
- Surendran, A.; Siddiqui, Y.; Saud, H.M.; Ali, N.S.; Manickam, S. Inhibition and kinetic studies of cellulose and hemicellulose degrading enzymes of Ganoderma boninense by naturally occurring phenolic compounds. J. Appl. Microbiol. 2018, 124, 1544–1555. [Google Scholar] [CrossRef] [PubMed]
- Gusakov, V.A.; Sinitsyn, P.A.; Manenkova, A.J.; Protas, V.O. Enzymatic saccharification of industrial and agricultural lignocellulosic wastes—Main features of the process. Appl. Biochem. Biotechnol. 1992, 34, 625. [Google Scholar] [CrossRef]
- Tian, S.-Q.; Ma, S.; Wang, X.-W.; Zhang, Z.-N. Fractal kinetic analysis of the enzymatic saccharification of CO2 laser pretreated corn stover. Carbohydr. Polym. 2013, 98, 618–623. [Google Scholar] [CrossRef] [PubMed]
CP | NDF | ADF | ADL | HC | Cellulose | ADL Removal (%) | |
---|---|---|---|---|---|---|---|
Control | 5.61 | 86.40 ab | 74.17 bc | 30.96 a | 12.23 ab | 43.21 e | - |
I. lacteus | 4.65 | 88.17 a | 75.08 bc | 30.07 abc | 13.09 a | 45.01 bcd | 2.9 |
G. resinaceum | 4.37 | 85.50 bc | 74.85 bc | 28.52 d | 10.65 abc | 46.34 ab | 7.9 |
B. adusta | 5.11 | 87.02 ab | 77.48 a | 29.91 abc | 9.54 bc | 47.57 a | 3.4 |
P. rufa | 5.29 | 83.73 c | 75.09 b | 29.56 cd | 8.64 c | 45.53 bc | 4.5 |
T. versicolor | 5.29 | 85.11 bc | 75.21 b | 30.88 ab | 9.90 abc | 44.33 cde | 0.3 |
Trametes sp. | 4.50 | 86.43 ab | 73.39 c | 29.67 bcd | 13.04 a | 43.72 de | 4.2 |
p-value | 0.106 | <0.001 | <0.001 | <0.001 | 0.001 | <0.001 | - |
Sugars Yield (mg g−1) | k(1) (d−1) | R2 | Productivity (mg g−1 h−1) | |
---|---|---|---|---|
Control | 75.9 ± 0.4 f | 0.150 ± 0.010 | 0.867 | 1.0 |
I. lacteus | 94.8 ± 1.0 e | 0.315 ± 0.006 | 0.943 | 1.3 |
G. resinaceum | 147.7 ± 2.2 b | 0.224 ± 0.008 | 0.804 | 2.1 |
B. adusta | 138.7 ± 1.0 c | 0.234 ± 0.004 | 0.844 | 1.9 |
P. rufa | 199.6 ± 1.8 a | 0.447 ± 0.003 | 0.944 | 2.8 |
T. versicolor | 145.5 ± 0.9 b | 0.254 ± 0.008 | 0.733 | 2.0 |
Trametes sp. | 120.1 ± 0.6 d | 0.213 ± 0.002 | 0.812 | 1.7 |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Fernandes, J.M.C.; Fraga, I.; Sousa, R.M.O.F.; Rodrigues, M.A.M.; Sampaio, A.; Bezerra, R.M.F.; Dias, A.A. Pretreatment of Grape Stalks by Fungi: Effect on Bioactive Compounds, Fiber Composition, Saccharification Kinetics and Monosaccharides Ratio. Int. J. Environ. Res. Public Health 2020, 17, 5900. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph17165900
Fernandes JMC, Fraga I, Sousa RMOF, Rodrigues MAM, Sampaio A, Bezerra RMF, Dias AA. Pretreatment of Grape Stalks by Fungi: Effect on Bioactive Compounds, Fiber Composition, Saccharification Kinetics and Monosaccharides Ratio. International Journal of Environmental Research and Public Health. 2020; 17(16):5900. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph17165900
Chicago/Turabian StyleFernandes, Joana M.C., Irene Fraga, Rose M.O.F. Sousa, Miguel A.M. Rodrigues, Ana Sampaio, Rui M.F. Bezerra, and Albino A. Dias. 2020. "Pretreatment of Grape Stalks by Fungi: Effect on Bioactive Compounds, Fiber Composition, Saccharification Kinetics and Monosaccharides Ratio" International Journal of Environmental Research and Public Health 17, no. 16: 5900. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph17165900