- Email: [email protected]
Biodegradation kinetics of oil palm empty fruit bunches by white rot fungi
International Biodeterioration & Biodegradation 91 (2014) 24e28
Contents lists available at ScienceDirect
International Biodeterioration & Biodegradation journal homepage: www.elsevier.com/locate/ibiod
Short communication
Biodegradation kinetics of oil palm empty fruit bunches by white rot fungi Yineth Piñeros-Castro a, *, Mario Velásquez-Lozano b a b
Engineering Department, Natural Sciences and Engineering Faculty, Universidad Jorge Tadeo Lozano, Cra 4 22-61, Bogotá, Colombia Chemical and Environmental Engineering Department, Universidad Nacional de Colombia, Bogotá, Colombia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 January 2014 Received in revised form 7 March 2014 Accepted 9 March 2014 Available online
The biodegradation of lignin, cellulose and hemicellulose from oil palm empty fruit bunches by white rot fungi Phanerochaete chrysosporium and Pleurotus ostreatus was investigated. The results showed higher mass loss and polysaccharide degradation when the biological treatment was carried out with P. chrysosporium. Biodegradation curves were modelled by a Weibull kinetic model and the kinetic parameters were obtained for each one of the components. Even though the lignin degradation rates were similar for both fungi, the biodegradation of this component reached 50% with P. ostreatus, a higher value than the 41% reached with P. chrysosporium after harvesting for four weeks. Higher polysacharides biodegradation rates were observed for P. chrysosporium compared to P. ostreatus. Consequently, the P. ostreatus pretreatment can be considered adequate for the delignification of palm residues without considerably affecting the cellulose fraction, which is important for the production of fermentable sugars. Ó 2014 Elsevier Ltd. All rights reserved.
Keywords: Biodegradation kinetics Oil palm empty fruit bunch Biological pretreatment White rot fungi Lignocelullolosic biodegradation
1. Introduction Colombia is the world’s fifth producer of palm oil and the first in Latin America. Palmiculture is one of the most promising agricultural activities and considered an important source for national development. 4.6 million tons of oil palm fruits were processed in 2012 (Torres et al., 2013) and generated Mt (Million tonnes) of lignocellulosic materials. In 2007, the worldwide annual production of oil palm biomass reached 184.6 Mt (Kelly-Yong et al., 2007). Lignocellulosic materials are the main source of renewable materials on the surface of the earth. For this reason, their biological degradation has gained interest for investigation, especially for the production of bioenergy and bioproducts (Singh and Chen, 2008). Lignocelluloses are degraded by many microorganisms and, particularly with high efficiencies by white rot fungi. These fungi exhibit an oxidative enzymatic system and a lignolytic extracellular system, and consequently are the most efficient for lignin degradation (Sánchez, 2009). White rot fungi including Phanerochaete chyrsosporium, Ceriporia lacerata, Cyathus stercoreus, Ceriporiopsis subvermispora, Pycnoporus cinnabarinus and Pleurotus ostreatus have been studied for the degradation of different
* Corresponding author. Tel.: þ57 1 2427030 ext 1444. E-mail addresses: [email protected], [email protected] (Y. Piñeros-Castro). http://dx.doi.org/10.1016/j.ibiod.2014.03.009 0964-8305/Ó 2014 Elsevier Ltd. All rights reserved.
lignocellulosic biomasses showing high delignification efficiencies (Shi et al., 2008; Kumar et al., 2009). The study of the biodegradation kinetics of the lignocellulosic materials is important considering the fungal treatment breaks the lignin-carbohydrate complex. This improves the availability of cellulose to the hydrolytic enzymes (Taniguchi et al., 2005; Zhang et al., 2007; Shi et al., 2009; Yu et al., 2009), which is considered a requirement for the production of fermentable sugars (Gupta et al., 2011). So far, no studies on the kinetics biodegradation of oil palm residues by white rot fungi have been reported. In the present work, the process of biodegradation of lignin, cellulose and hemicellulose by the fungi P. chysosporium and P. ostreatus in solid state fermentation was studied. In the present work, the experimental data for the biodegradation of lignin, cellulose and hemicellulose were described by Weibull kinetic model. It is potentially interesting for the kinetic description of chemical, microbial or enzymatic degradation. One of the advantages of this model is its flexibility when adjusting the experimental data (van Boekel, 2002) using two parameters: the reaction rate constant (a) and the shape factor (b) (Cunha et al., 1998). The distribution has been used with satisfactory results when investigating shelf life (Schmidt and Bouma, 1992; Duyvesteyn et al., 2001), microbial deactivation curves (Peleg, 2000; Unluturk et al., 2010), vitamins and antioxidants degradation (Oms-Oliu et al., 2009; Zheng and Lu, 2011), osmotic dehydration (Corzo and Bracho, 2008), amongst others. It has also been
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
evaluated in degradation kinetics of monosaccharides under supercritical conditions (Khajavi et al., 2005). During the literature review, no reports in the use of the Weibull model for biodegradation of lignocellulosic materials were found. In general, a kinetics model is important to study the effect of the culture conditions on the biomass biodegradation.
25
2.5. Statistical analysis All experiments and measurements were made by triplicates and the mean values were used for calculations and data analysis. The ANOVA (p ¼ 0.05) and the means difference tests (Tukey test) were carried out using Statgraphics 5.0 (Statistical Graphics Corp USA).
2. Materials and methods 3. Results and discussion 2.1. Feedstock 3.1. Weight loss percentage The oil palm empty fruit bunches were supplied by the farmhouse Hacienda La Cabaña in Cumaral, Meta, Colombia. The material was washed, dried and chopped (3 cm approx.). The characterization of the material included the determination of cellulose, hemicellulose and lignin using the methodology described by the National Renewable Energy Laboratory NREL (Sluiter et al., 2008). The structural carbohydrate composition was determined based on monomeric sugars content measured after an acid hydrolysis with 72% H2SO4 at 30 C for 60 min and 4% H2SO4 at 121 C for 1 h. This hydrolysis liquid was analyzed by high performance liquid chromatography (HPLC) with refractive index detector, in an AMINEX HPX-87H sugars analysis column (Bio-RAD) operating at 60 C with 5 mM H2SO4 as a mobile-phase (0.6 ml/ min). Acid-soluble lignin was determined by UV adsorption and insoluble lignin by gravimetric method.
The weight loss percentage of the palm residues caused by the biological treatment is showed in Table 1. During first week, the weight loss was similar between both fungi. However, a higher weight loss was observed for bunches treated with the fungus P. chrysosporium during the following two weeks. The results are similar to those obtained by Camarero et al. (1994), who reported that P. chrysosporium causes higher weight losses when compared to Pleurotus eryngii in the biodegradation of wheat residues. This can be attributed to the simultaneous attack to lignin and polysaccharides by P. chrysosporium, whereas P. eryngii preferentially degrades lignin and xylans while slightly affecting the cellulose. The observed values are within the ranges reported for white rot fungi degradation of eucalyptus and grasses (Akin et al., 1995) as well as rubberwood (Pandey and Nagveni, 2007).
2.2. Strains, culture preparation and solid substrate
3.2. Biodegradation of palm residues
Two fungi from the white rot were used: the Phanerochaete chrysosporium CECT 2798 and the P. ostreatus CECT 20311 from the Spanish Type Culture Collection. The strains were kept using potato dextrose agar (PDA) as medium, and were cultivated for six days at 30 C to prepare the inoculants. For P. chrysosporium, spores were suspended in sterile distilled water (1.4 108 spores/mL) and 2 mL were added to each experimental unit. For P. ostreatus, 4 cm2 of the agar surface were scraped for each experimental unit. Polyetylene bags were used as experimental units. 10 g of lignocellulosic material were added (dry basis), and humidity was adjusted to 67% (w/w) using saline supplement (Kirk medium) (Kirk et al., 1986). Subsequently, the units were sterilized for 20 min at 121 C and the inoculant was added after cool down. The experimental units were incubated at 30 C for four weeks.
Experimental data obtained for the degradation of the different components present in the palm residues is presented in Fig. 1. Both P. ostreatus and P. chrysosporium fungi degraded the lignin to a similar extent, but also degraded the polysaccharides at the evaluated conditions. The fungus P. ostreatus can be considered as selective for delignification, since the degradation of cellulose starts only after the third week of treatment. In contrast, P. chrysosporium simultaneously removes lignin and structural carbohydrates, homogeneously degrading the material as has been reported for rubber in previous studies (Pandey and Nagveni, 2007). Other authors have also reported the results of the biodegradation of rice (Oriza sativa L.) and corn residues (Zea maize L.) by P. chrysosporium, which degraded cellulose and hemicellulose indiscriminately (Karunanandaa and Varga, 1996). Table 2 summarizes the characterization results for the palm residues after the third week of treatment. Data reported in other scientific studies using the same fungi is also presented for comparison. The wide range of variation observed for the biodegradation of lignin reflects differences in the complexity of this molecule depending on the feedstock (Agosin et al., 1985). With regard to the degradation of polysaccharides, the behavior observed for the palm residues has a similar tendency to that reported for wheat straw (Salvachúa et al., 2011), where higher degradation was observed for P. chrysosporium. It has been reported that the lignin degradation by P. chrysosporium reached 70% for olive residues (Tomati et al., 1995),
2.3. Biomass biodegradation The progress of the oil palm empty fruit bunches pretreated with P. ostreatus and P. chrysosporium was monitored for 4 weeks. Each week, three random samples were removed and washed. Weight loss was calculated as the percentage of total solids lost after each week. Lignin content and polysaccharide composition (cellulose and hemicellulose) of biopretreated palm biomass were determined as described in section 2.2.1. The weight loss and the kinetic parameters of the Weibull model (a and b) were set as response variables. 2.4. Methods for Weibull model parameters estimation Weibull model kinetic parameters were obtained by adjusting experimental data of lignin, cellulose and hemicellulose degraded fraction. Such procedure was carried out by minimizing the square of the experimental error using the LevenbergeMarquardt algorithm (Bates and Watts, 2008) available in the SciDavis software v.0.2.4. (http://scidavis.sourceforge.net/).
Table 1 Weight loss percentage observed during the biological treatment (wt %). Week
P. chrysosporium
0 1 2 3 4
0.00 3.24 23.24 27.48 33.43
0.00 0.03 0.61 3.08 2.24
P. ostreatus 0.00 3.33 6.63 14.63 42.69
0.00 0.03 0.27 0.57 2.37
26
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
Fig. 1. Biodegradation of the main components of the residue. - Cellulose, lignin, Ahemicellulose.
30% for wheat residues (Tuomela et al., 2000) and 15% for eucalyptus (del Ri’o and Gutiérrez, 2001). Reports using P. ostreatus showed the lignin degradation reached 1% for eucalyptus and 2.67% for bamboo (Zhang et al., 2007). However, the results in the present study showed higher delignification percentages with P. ostreatus compared to P. chrysosporium. 3.3. Palm residue degradation kinetics The experimental data obtained for the biodegradation of lignin, cellulose and hemicellulose were adjusted applying the Weibull kinetic model. The model is described in Eq. (1), where ni represents the fractional quantity of component X, which varies between the initial value Xo and the equilibrium value Xe. The time required to reach the equilibrium is represented by f(t), which is the Weibull distribution function (Cunha et al., 1998).
Za nðtÞ ¼
f ðtÞdt ¼ 1 FðtÞ ¼ 1 expðatÞb
(1)
t
Eq. (2) is the expression used to calculate the fraction of degraded lignin (L (t)) in the present work.
Lðt Þ ¼
Lo Lt ¼ expðat Þb Lo Le
(2)
where Lo, Lt and Le represent the initial lignin fraction, the lignin fraction at time t, and the lignin content at equilibrium (t ¼ a), respectively. (a) represents the kinetic rate constant and (b) is the Weibull shape parameter. Likewise, the accumulated fractions of degraded cellulose C(t) and degraded hemicellulose H(t) were calculated. The accumulated fractions of degraded lignin, cellulose and hemicellulose for oil palm residues are presented in Fig. 2, where it can be observed that the data accurately fits the proposed model (relative mean difference <0.1, correlation coefficient r2 > 0,97). The values obtained for the Weibull parameters, the rate constant (a) and the shape parameter (b), are presented in Fig. 3. The values for the rate constant (a) and the shape factor (b) of the different components as were found to between 0.066 and
Table 2 Composition and biodegradation of biologically pretreated feedstocks using white rot fungi. Characteristic
Lignocellullosic material Oil palm empty fruit bunch
Lignin (%) Cellulose (%) Hemicellulose (%) Lignin biodegradation (%) Cellulose biodegradation (%) Hemicellulose biodegradation (%) a b c d e f
Wheat straw (Camarero et al., 1994)
Wheat straw (Salvachúa et al., 2011)
Control
P.ca
P.ob
Control
P.cc
P.ed
Control
25.17 49.95 18.91
20.24 53.73 19.81 42.09 28.24 27.70
14.25 54.23 18.43 51.91 7.63 13.77
15.9 40.7 20.5
14.4 24.6 14.7 45.0 63 50
10.2 42.8 14.6 47.0 14 43
24,0 36.9 23.0
Phanerochaete chrysosporium CECT 2798, 3 weeks at 30 C. Pleurotus ostreatus CECT 20311, 3 weeks at 30 C. Phanerochaete chrysosporium ATCC 24725, 30 days. Pleurotus eryngii, 60 days. Phanerochaete chrysosporium, 3 weeks at 30 C. Pleurotus ostreatus, 3 weeks at 30 C.
P.ce
P.of
0.0 35 70
27 22 52
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
27
The relation between the parameter (b) and the mass transfer in drying processes has been reported before (Corzo and Bracho, 2008), showing that lower values are obtained when the water loss is fast. A similar relation has been established for the degradation of components with antioxidant activity in watermelon (Oms-Oliu et al., 2009), where higher biodegradation rates resulted in lower (b) values. A similar relation was expected for the lignin biodegradation and lower (b) values would then suggest higher rates of lignin removal. A higher lignin degradation rate was observed for P. ostreatus for which 50% of the lignin was removed after 4 weeks, higher than the 41% observed for P. chysosporium. However, the kinetic parameters were similar for both fungi. Regarding the biodegradation of cellulose and hemicellulose, Fig. 1 shows higher polysaccharide degradation ability for P. chrysosporium than for P. ostreatus. Significant differences were observed in the calculated kinetic parameters (p < 0.05) presented in Fig. 3. The lowest values for (a) were obtained with P. ostreatus, demonstrating that the affinity for polysaccharides is lower for this strain than for P. chrysosporium. Concerning the parameter (b), the values for P. chrysosporium were lower for cellulose as well as for hemicellulose. This means this fungus exhibits a higher polysaccharides degradation rates than P. ostreatus. Fig. 2B shows there is no significant difference in the degradation of cellulose between the two fungi after the fourth week when an average biodegradation of 40% is reached. The lowest values for (b) were observed for hemicellulose, followed by cellulose and lignin, for the biodegradation carried out with P. chrysosporium (Fig. 3). It has been reported that the enzymes feruloyl and p-coumaroyl esterases present in this strain play an important role in the biodegradation of the cellular walls of grasses (Kuhad et al., 1997) and react synergically with xylanases to break the bond with the lignin (Fillingham et al., 1999). The degradation rate of the fractions of palm residues was studied in the present work resulting in higher degradation rates for hemicellulose than for lignin. This means it is necessary to remove the hemicellulose to
Fig. 2. Experimental data and Weibull model adjustment for the degraded fraction of lignin. - P. ostreatus , P. chrysosporium. A. Lignin, B.Cellulose, C. Hemicellulose.
0.632 (weeks1) for (a) and between 1.96 and 6.79 for (b). The shape factor values were higher than one, which indicates the Weibull function increases due to the increase of the degree of biodegradation with time. The (a) parameter, related to the resistance to biodegradation, did not exhibit significant differences between both fungi for lignin (p > 0.05) evidencing their similar affinity for this component.
Fig. 3. Kinetic parameters of the Weibull model (a) and (b) for the degradation of lignin ,, cellulose and hemicellulose .
28
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
achieve an efficient removal of lignin. However, other authors report higher degradation rates for lignin compared to the degradation rate of cellulose when treating wheat residues with P. chrysosporium (Huang et al., 2008). This opposite behavior could be explained by the complex structure of the lignocellulosic matrix of the oil palm residues. With regard to the results obtained with P. ostreatus after three weeks, the lowest values for the parameter (b) were observed for lignin, followed by hemicellulose and then cellulose, corroborating the higher affinity of this strain for lignin than for polysaccharides. The results agree with those reported for the degradation of wheat straw by P. ostreatus (Camarero et al., 1994) and by other white rot fungi like Euc-1 and Irpex lacteus (Dias et al., 2010). As can be observed in Table 2, the biological treatment using P. ostreatus for the degradation of oil palm residues produces a 51.91% delignified material after three weeks, without any significant alteration of the cellulose fraction. Therefore, the fungal treatment should be performed for no longer than three weeks if the objective of the treatment is the production of fermentable sugars, as the degradation of cellulose was low during this period. 4. Conclusion The experimental data determined for the biodegradation of lignin, cellulose and hemicellulose were described by the Weibull kinetic model. The model can be considered as a suitable tool for describing the changes suffered by lignocellulosic materials when treated with white rot fungi cultivated using the solid state fermentation technique and to study the culture conditions on the biomass biodegradation. A higher lignin degradation rate compared to the polysaccharides degradation rates was observed using P. ostreatus. The degradation of cellulose, an important component for the production of fermentable sugars, remained low (7.63%) while the total degradation of lignin reached 51.91% after treating for three weeks. Acknowledgements The present work was supported by the project: “Hydrolysis of oil palm lignocellulosic wastes to obtain fermentable sugars” funded by the Science, Technology and Innovation Administrative Department COLCIENCIAS project 110140520201; and executed by the Universidad Nacional de Colombia in Bogotá, in agreement with the Universidad de Bogotá Jorge Tadeo Lozano. References Agosin, E., Daudin, J.J., Odier, E., 1985. Screening of white-rot fungi on (14 C) ligninlabelled and (14 C) whole-labelled wheat straw. Appl. Microbiol. Biotechnol. 22, 132e138. Akin, D., Rigsby, L., Sethuraman, A., Morrison 3rd, W., Gamble, G., Eriksson, K., 1995. Alterations in structure, chemistry, and biodegradability of grass lignocellulose treated with the white rot fungi Ceriporiopsis subvermispora and Cyathus stercoreus. Appl. Environ. Microbiol. 61, 1591. Bates, D.M., Watts, D.G., 2008. Practical Considerations in Nonlinear Regression, Nonlinear Regression analysis and its Applications. John Wiley Sons, Inc, pp. 67e133. Camarero, S., Galletti, G.C., Martinez, A.T., 1994. Preferential degradation of phenolic lignin units by two white rot fungi. Appl. Environ. Microbiol. 60, 4509. Corzo, O., Bracho, N., 2008. Application of Weibull distribution model to describe the vacuum pulse osmotic dehydration of sardine sheets. LWT e sFood Sci. Technol. 41, 1108e1115. Cunha, L.M., Oliveira, F.A.R., Oliveira, J.C., 1998. Optimal experimental design for estimating the kinetic parameters of processes described by the Weibull probability distribution function. J. Food Eng. 37, 175e191. del Ri’o, J., Gutiérrez, A., 2001. Py-GC/MS study of eucalyptus globulus wood treated with different fungi. J. Anal. Appl. Pyrolysis 58, 441e452. Dias, A.A., Freitas, G.S., Marques, G.S.M., Sampaio, A., Fraga, I.S., Rodrigues, M.A.M., Evtuguin, D.V., Bezerra, R.M.F., 2010. Enzymatic saccharification of biologically
pre-treated wheat straw with white-rot fungi. Bioresour. Technol. 101, 6045e 6050. Duyvesteyn, W.S., Shimoni, E., Labuza, T.P., 2001. Determination of the end of shelflife for milk using Weibull hazard method. LWT e Food Sci. Technol. 34, 143e 148. Fillingham, I.J., Kroon, P.A., Williamson, G., Gilbert, H.J., Hazlewood, G.P., 1999. A modular cinnamoyl ester hydrolase from the anaerobic fungus Piromyces equi acts synergistically with xylanase and is part of a multiprotein cellulosebinding cellulase-hemicellulase complex. Biochem. J. 343, 215. Gupta, R., Mehta, G., Khasa, Y., Kuhad, R., 2011. Fungal delignification of lignocellulosic biomass improves the saccharification of cellulosics. Biodegradation 22, 797e804. Huang, D., Zeng, G., Peng, Z., Zhang, P., Hu, S., Jiang, X., Feng, C., Chen, Y., 2008. Biotransformation of rice straw by Phanerachaete chrysosporium and the related ligninolytic enzymes. Int. J. Biotechnol. 10, 86e92. Karunanandaa, K., Varga, G., 1996. Colonization of crop residues by white-rot fungi: cell wall monosaccharides, phenolic acids, ruminal fermentation characteristics and digestibility of cell wall fiber components in vitro. Anim. Feed Sci. Technol. 63, 273e288. Kelly-Yong, T.L., Lee, K.T., Mohamed, A.R., Bhatia, S., 2007. Potential of hydrogen from oil palm biomass as a source of renewable energy worldwide. Energy Policy 35, 5692e5701. Khajavi, S.H., Kimura, Y., Oomori, T., Matsuno, R., Adachi, S., 2005. Degradation kinetics of monosaccharides in subcritical water. J. Food Eng. 68, 309e313. Kirk, T.K., Croan, S., Tien, M., Murtagh, K.E., Farrell, R.L., 1986. Production of multiple ligninases by Phanerochaete chrysosporium: effect of selected growth conditions and use of a mutant strain. Enzyme Microb. Technol. 8, 27e32. Kuhad, R., Singh, A., Eriksson, K.E., 1997. Microorganisms and Enzymes Involved in the Degradation of Plant Fiber Cell Walls. Biotechnology in the Pulp and Paper Industry, pp. 45e125. Kumar, R., Mago, G., Balan, V., Wyman, C.E., 2009. Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies. Bioresour. Technol. 100, 3948e3962. Oms-Oliu, G., Odriozola-Serrano, I., Soliva-Fortuny, R., Martín-Belloso, O., 2009. Use of Weibull distribution for describing kinetics of antioxidant potential changes in fresh-cut watermelon. J. Food Eng. 95, 99e105. Pandey, K.K., Nagveni, H., 2007. Rapid characterisation of brown and white rot degraded chir pine and rubberwood by FTIR spectroscopy. Eur. J. Wood Prod. 65, 477e481. Peleg, M., 2000. Microbial survival curves e the reality of flat “shoulders” and absolute thermal death times. Food Res. Int. 33, 531e538. Salvachúa, D., Prieto, A., López-Abelairas, M., Lu-Chau, T., Martínez, Á.T., Martínez, M.J., 2011. Fungal pretreatment: an alternative in second-generation ethanol from wheat straw. Bioresour. Technol. 102, 7500e7506. Sánchez, C., 2009. Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol. Adv. 27, 185e194. Schmidt, K., Bouma, J., 1992. Estimating shelf-life of cottage cheese using hazard analysis. J. Dairy Sci. 75, 2922e2927. Shi, J., Chinn, M.S., Sharma-Shivappa, R.R., 2008. Microbial pretreatment of cotton stalks by solid state cultivation of Phanerochaete chrysosporium. Bioresour. Technol. 99, 6556e6564. Shi, J., Sharma-Shivappa, R.R., Chinn, M., Howell, N., 2009. Effect of microbial pretreatment on enzymatic hydrolysis and fermentation of cotton stalks for ethanol production. Biomass Bioenergy 33, 88e96. Singh, D., Chen, S., 2008. The white-rot fungus Phanerochaete chrysosporium: conditions for the production of lignin-degrading enzymes. Appl. Microbiol. Biotechnol. 81, 399e417. Sluiter, A., Hames, B., Ruiz, R., Scarlata, C., Sluiter, J., Templeton, D., Crocker, D., 2008. Determination of Structural Carbohydrates and Lignin in Biomass. Laboratory Analytical Procedure NREL/TP-510e42618. Taniguchi, M., Suzuki, H., Watanabe, D., Sakai, K., Hoshino, K., Tanaka, T., 2005. Evaluation of pretreatment with Pleurotus ostreatus for enzymatic hydrolysis of rice straw. J. Biosci. Bioeng. 100, 637e643. Tomati, U., Galli, E., Pasetti, L., Volterra, E., 1995. Bioremediation of olive-mill wastewaters by composting. Waste Manage. Res. 13, 509e518. Torres, R., Girón, E., Rincón, F., Delgado, J., 2013. Colombian Oil Palm Statistical Data 2013. Fedepalma. Tuomela, M., Vikman, M., Hatakka, A., Itävaara, M., 2000. Biodegradation of lignin in a compost environment: a review. Bioresour. Technol. 72, 169e183. Unluturk, S., AtIlgan, M.R., Baysal, A.H., Unluturk, M.S., 2010. Modeling inactivation kinetics of liquid egg white exposed to UV-C irradiation. Int. J. Food Microbiol. 142, 341e347. van Boekel, M.A.J.S., 2002. On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells. Int. J. Food Microbiol. 74, 139e159. Yu, J., Zhang, J., He, J., Liu, Z., Yu, Z., 2009. Combinations of mild physical or chemical pretreatment with biological pretreatment for enzymatic hydrolysis of rice hull. Bioresour. Technol. 100, 903e908. Zhang, X., Yu, H., Huang, H., Liu, Y., 2007. Evaluation of biological pretreatment with white rot fungi for the enzymatic hydrolysis of bamboo culms. Int. Biodeterior. Biodegradation 60, 159e164. Zheng, H., Lu, H., 2011. Use of kinetic, Weibull and PLSR models to predict the retention of ascorbic acid, total phenols and antioxidant activity during storage of pasteurized pineapple juice. LWT e Food Sci. Technol. 44, 1273e1281.
Contents lists available at ScienceDirect
International Biodeterioration & Biodegradation journal homepage: www.elsevier.com/locate/ibiod
Short communication
Biodegradation kinetics of oil palm empty fruit bunches by white rot fungi Yineth Piñeros-Castro a, *, Mario Velásquez-Lozano b a b
Engineering Department, Natural Sciences and Engineering Faculty, Universidad Jorge Tadeo Lozano, Cra 4 22-61, Bogotá, Colombia Chemical and Environmental Engineering Department, Universidad Nacional de Colombia, Bogotá, Colombia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 January 2014 Received in revised form 7 March 2014 Accepted 9 March 2014 Available online
The biodegradation of lignin, cellulose and hemicellulose from oil palm empty fruit bunches by white rot fungi Phanerochaete chrysosporium and Pleurotus ostreatus was investigated. The results showed higher mass loss and polysaccharide degradation when the biological treatment was carried out with P. chrysosporium. Biodegradation curves were modelled by a Weibull kinetic model and the kinetic parameters were obtained for each one of the components. Even though the lignin degradation rates were similar for both fungi, the biodegradation of this component reached 50% with P. ostreatus, a higher value than the 41% reached with P. chrysosporium after harvesting for four weeks. Higher polysacharides biodegradation rates were observed for P. chrysosporium compared to P. ostreatus. Consequently, the P. ostreatus pretreatment can be considered adequate for the delignification of palm residues without considerably affecting the cellulose fraction, which is important for the production of fermentable sugars. Ó 2014 Elsevier Ltd. All rights reserved.
Keywords: Biodegradation kinetics Oil palm empty fruit bunch Biological pretreatment White rot fungi Lignocelullolosic biodegradation
1. Introduction Colombia is the world’s fifth producer of palm oil and the first in Latin America. Palmiculture is one of the most promising agricultural activities and considered an important source for national development. 4.6 million tons of oil palm fruits were processed in 2012 (Torres et al., 2013) and generated Mt (Million tonnes) of lignocellulosic materials. In 2007, the worldwide annual production of oil palm biomass reached 184.6 Mt (Kelly-Yong et al., 2007). Lignocellulosic materials are the main source of renewable materials on the surface of the earth. For this reason, their biological degradation has gained interest for investigation, especially for the production of bioenergy and bioproducts (Singh and Chen, 2008). Lignocelluloses are degraded by many microorganisms and, particularly with high efficiencies by white rot fungi. These fungi exhibit an oxidative enzymatic system and a lignolytic extracellular system, and consequently are the most efficient for lignin degradation (Sánchez, 2009). White rot fungi including Phanerochaete chyrsosporium, Ceriporia lacerata, Cyathus stercoreus, Ceriporiopsis subvermispora, Pycnoporus cinnabarinus and Pleurotus ostreatus have been studied for the degradation of different
* Corresponding author. Tel.: þ57 1 2427030 ext 1444. E-mail addresses: [email protected], [email protected] (Y. Piñeros-Castro). http://dx.doi.org/10.1016/j.ibiod.2014.03.009 0964-8305/Ó 2014 Elsevier Ltd. All rights reserved.
lignocellulosic biomasses showing high delignification efficiencies (Shi et al., 2008; Kumar et al., 2009). The study of the biodegradation kinetics of the lignocellulosic materials is important considering the fungal treatment breaks the lignin-carbohydrate complex. This improves the availability of cellulose to the hydrolytic enzymes (Taniguchi et al., 2005; Zhang et al., 2007; Shi et al., 2009; Yu et al., 2009), which is considered a requirement for the production of fermentable sugars (Gupta et al., 2011). So far, no studies on the kinetics biodegradation of oil palm residues by white rot fungi have been reported. In the present work, the process of biodegradation of lignin, cellulose and hemicellulose by the fungi P. chysosporium and P. ostreatus in solid state fermentation was studied. In the present work, the experimental data for the biodegradation of lignin, cellulose and hemicellulose were described by Weibull kinetic model. It is potentially interesting for the kinetic description of chemical, microbial or enzymatic degradation. One of the advantages of this model is its flexibility when adjusting the experimental data (van Boekel, 2002) using two parameters: the reaction rate constant (a) and the shape factor (b) (Cunha et al., 1998). The distribution has been used with satisfactory results when investigating shelf life (Schmidt and Bouma, 1992; Duyvesteyn et al., 2001), microbial deactivation curves (Peleg, 2000; Unluturk et al., 2010), vitamins and antioxidants degradation (Oms-Oliu et al., 2009; Zheng and Lu, 2011), osmotic dehydration (Corzo and Bracho, 2008), amongst others. It has also been
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
evaluated in degradation kinetics of monosaccharides under supercritical conditions (Khajavi et al., 2005). During the literature review, no reports in the use of the Weibull model for biodegradation of lignocellulosic materials were found. In general, a kinetics model is important to study the effect of the culture conditions on the biomass biodegradation.
25
2.5. Statistical analysis All experiments and measurements were made by triplicates and the mean values were used for calculations and data analysis. The ANOVA (p ¼ 0.05) and the means difference tests (Tukey test) were carried out using Statgraphics 5.0 (Statistical Graphics Corp USA).
2. Materials and methods 3. Results and discussion 2.1. Feedstock 3.1. Weight loss percentage The oil palm empty fruit bunches were supplied by the farmhouse Hacienda La Cabaña in Cumaral, Meta, Colombia. The material was washed, dried and chopped (3 cm approx.). The characterization of the material included the determination of cellulose, hemicellulose and lignin using the methodology described by the National Renewable Energy Laboratory NREL (Sluiter et al., 2008). The structural carbohydrate composition was determined based on monomeric sugars content measured after an acid hydrolysis with 72% H2SO4 at 30 C for 60 min and 4% H2SO4 at 121 C for 1 h. This hydrolysis liquid was analyzed by high performance liquid chromatography (HPLC) with refractive index detector, in an AMINEX HPX-87H sugars analysis column (Bio-RAD) operating at 60 C with 5 mM H2SO4 as a mobile-phase (0.6 ml/ min). Acid-soluble lignin was determined by UV adsorption and insoluble lignin by gravimetric method.
The weight loss percentage of the palm residues caused by the biological treatment is showed in Table 1. During first week, the weight loss was similar between both fungi. However, a higher weight loss was observed for bunches treated with the fungus P. chrysosporium during the following two weeks. The results are similar to those obtained by Camarero et al. (1994), who reported that P. chrysosporium causes higher weight losses when compared to Pleurotus eryngii in the biodegradation of wheat residues. This can be attributed to the simultaneous attack to lignin and polysaccharides by P. chrysosporium, whereas P. eryngii preferentially degrades lignin and xylans while slightly affecting the cellulose. The observed values are within the ranges reported for white rot fungi degradation of eucalyptus and grasses (Akin et al., 1995) as well as rubberwood (Pandey and Nagveni, 2007).
2.2. Strains, culture preparation and solid substrate
3.2. Biodegradation of palm residues
Two fungi from the white rot were used: the Phanerochaete chrysosporium CECT 2798 and the P. ostreatus CECT 20311 from the Spanish Type Culture Collection. The strains were kept using potato dextrose agar (PDA) as medium, and were cultivated for six days at 30 C to prepare the inoculants. For P. chrysosporium, spores were suspended in sterile distilled water (1.4 108 spores/mL) and 2 mL were added to each experimental unit. For P. ostreatus, 4 cm2 of the agar surface were scraped for each experimental unit. Polyetylene bags were used as experimental units. 10 g of lignocellulosic material were added (dry basis), and humidity was adjusted to 67% (w/w) using saline supplement (Kirk medium) (Kirk et al., 1986). Subsequently, the units were sterilized for 20 min at 121 C and the inoculant was added after cool down. The experimental units were incubated at 30 C for four weeks.
Experimental data obtained for the degradation of the different components present in the palm residues is presented in Fig. 1. Both P. ostreatus and P. chrysosporium fungi degraded the lignin to a similar extent, but also degraded the polysaccharides at the evaluated conditions. The fungus P. ostreatus can be considered as selective for delignification, since the degradation of cellulose starts only after the third week of treatment. In contrast, P. chrysosporium simultaneously removes lignin and structural carbohydrates, homogeneously degrading the material as has been reported for rubber in previous studies (Pandey and Nagveni, 2007). Other authors have also reported the results of the biodegradation of rice (Oriza sativa L.) and corn residues (Zea maize L.) by P. chrysosporium, which degraded cellulose and hemicellulose indiscriminately (Karunanandaa and Varga, 1996). Table 2 summarizes the characterization results for the palm residues after the third week of treatment. Data reported in other scientific studies using the same fungi is also presented for comparison. The wide range of variation observed for the biodegradation of lignin reflects differences in the complexity of this molecule depending on the feedstock (Agosin et al., 1985). With regard to the degradation of polysaccharides, the behavior observed for the palm residues has a similar tendency to that reported for wheat straw (Salvachúa et al., 2011), where higher degradation was observed for P. chrysosporium. It has been reported that the lignin degradation by P. chrysosporium reached 70% for olive residues (Tomati et al., 1995),
2.3. Biomass biodegradation The progress of the oil palm empty fruit bunches pretreated with P. ostreatus and P. chrysosporium was monitored for 4 weeks. Each week, three random samples were removed and washed. Weight loss was calculated as the percentage of total solids lost after each week. Lignin content and polysaccharide composition (cellulose and hemicellulose) of biopretreated palm biomass were determined as described in section 2.2.1. The weight loss and the kinetic parameters of the Weibull model (a and b) were set as response variables. 2.4. Methods for Weibull model parameters estimation Weibull model kinetic parameters were obtained by adjusting experimental data of lignin, cellulose and hemicellulose degraded fraction. Such procedure was carried out by minimizing the square of the experimental error using the LevenbergeMarquardt algorithm (Bates and Watts, 2008) available in the SciDavis software v.0.2.4. (http://scidavis.sourceforge.net/).
Table 1 Weight loss percentage observed during the biological treatment (wt %). Week
P. chrysosporium
0 1 2 3 4
0.00 3.24 23.24 27.48 33.43
0.00 0.03 0.61 3.08 2.24
P. ostreatus 0.00 3.33 6.63 14.63 42.69
0.00 0.03 0.27 0.57 2.37
26
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
Fig. 1. Biodegradation of the main components of the residue. - Cellulose, lignin, Ahemicellulose.
30% for wheat residues (Tuomela et al., 2000) and 15% for eucalyptus (del Ri’o and Gutiérrez, 2001). Reports using P. ostreatus showed the lignin degradation reached 1% for eucalyptus and 2.67% for bamboo (Zhang et al., 2007). However, the results in the present study showed higher delignification percentages with P. ostreatus compared to P. chrysosporium. 3.3. Palm residue degradation kinetics The experimental data obtained for the biodegradation of lignin, cellulose and hemicellulose were adjusted applying the Weibull kinetic model. The model is described in Eq. (1), where ni represents the fractional quantity of component X, which varies between the initial value Xo and the equilibrium value Xe. The time required to reach the equilibrium is represented by f(t), which is the Weibull distribution function (Cunha et al., 1998).
Za nðtÞ ¼
f ðtÞdt ¼ 1 FðtÞ ¼ 1 expðatÞb
(1)
t
Eq. (2) is the expression used to calculate the fraction of degraded lignin (L (t)) in the present work.
Lðt Þ ¼
Lo Lt ¼ expðat Þb Lo Le
(2)
where Lo, Lt and Le represent the initial lignin fraction, the lignin fraction at time t, and the lignin content at equilibrium (t ¼ a), respectively. (a) represents the kinetic rate constant and (b) is the Weibull shape parameter. Likewise, the accumulated fractions of degraded cellulose C(t) and degraded hemicellulose H(t) were calculated. The accumulated fractions of degraded lignin, cellulose and hemicellulose for oil palm residues are presented in Fig. 2, where it can be observed that the data accurately fits the proposed model (relative mean difference <0.1, correlation coefficient r2 > 0,97). The values obtained for the Weibull parameters, the rate constant (a) and the shape parameter (b), are presented in Fig. 3. The values for the rate constant (a) and the shape factor (b) of the different components as were found to between 0.066 and
Table 2 Composition and biodegradation of biologically pretreated feedstocks using white rot fungi. Characteristic
Lignocellullosic material Oil palm empty fruit bunch
Lignin (%) Cellulose (%) Hemicellulose (%) Lignin biodegradation (%) Cellulose biodegradation (%) Hemicellulose biodegradation (%) a b c d e f
Wheat straw (Camarero et al., 1994)
Wheat straw (Salvachúa et al., 2011)
Control
P.ca
P.ob
Control
P.cc
P.ed
Control
25.17 49.95 18.91
20.24 53.73 19.81 42.09 28.24 27.70
14.25 54.23 18.43 51.91 7.63 13.77
15.9 40.7 20.5
14.4 24.6 14.7 45.0 63 50
10.2 42.8 14.6 47.0 14 43
24,0 36.9 23.0
Phanerochaete chrysosporium CECT 2798, 3 weeks at 30 C. Pleurotus ostreatus CECT 20311, 3 weeks at 30 C. Phanerochaete chrysosporium ATCC 24725, 30 days. Pleurotus eryngii, 60 days. Phanerochaete chrysosporium, 3 weeks at 30 C. Pleurotus ostreatus, 3 weeks at 30 C.
P.ce
P.of
0.0 35 70
27 22 52
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
27
The relation between the parameter (b) and the mass transfer in drying processes has been reported before (Corzo and Bracho, 2008), showing that lower values are obtained when the water loss is fast. A similar relation has been established for the degradation of components with antioxidant activity in watermelon (Oms-Oliu et al., 2009), where higher biodegradation rates resulted in lower (b) values. A similar relation was expected for the lignin biodegradation and lower (b) values would then suggest higher rates of lignin removal. A higher lignin degradation rate was observed for P. ostreatus for which 50% of the lignin was removed after 4 weeks, higher than the 41% observed for P. chysosporium. However, the kinetic parameters were similar for both fungi. Regarding the biodegradation of cellulose and hemicellulose, Fig. 1 shows higher polysaccharide degradation ability for P. chrysosporium than for P. ostreatus. Significant differences were observed in the calculated kinetic parameters (p < 0.05) presented in Fig. 3. The lowest values for (a) were obtained with P. ostreatus, demonstrating that the affinity for polysaccharides is lower for this strain than for P. chrysosporium. Concerning the parameter (b), the values for P. chrysosporium were lower for cellulose as well as for hemicellulose. This means this fungus exhibits a higher polysaccharides degradation rates than P. ostreatus. Fig. 2B shows there is no significant difference in the degradation of cellulose between the two fungi after the fourth week when an average biodegradation of 40% is reached. The lowest values for (b) were observed for hemicellulose, followed by cellulose and lignin, for the biodegradation carried out with P. chrysosporium (Fig. 3). It has been reported that the enzymes feruloyl and p-coumaroyl esterases present in this strain play an important role in the biodegradation of the cellular walls of grasses (Kuhad et al., 1997) and react synergically with xylanases to break the bond with the lignin (Fillingham et al., 1999). The degradation rate of the fractions of palm residues was studied in the present work resulting in higher degradation rates for hemicellulose than for lignin. This means it is necessary to remove the hemicellulose to
Fig. 2. Experimental data and Weibull model adjustment for the degraded fraction of lignin. - P. ostreatus , P. chrysosporium. A. Lignin, B.Cellulose, C. Hemicellulose.
0.632 (weeks1) for (a) and between 1.96 and 6.79 for (b). The shape factor values were higher than one, which indicates the Weibull function increases due to the increase of the degree of biodegradation with time. The (a) parameter, related to the resistance to biodegradation, did not exhibit significant differences between both fungi for lignin (p > 0.05) evidencing their similar affinity for this component.
Fig. 3. Kinetic parameters of the Weibull model (a) and (b) for the degradation of lignin ,, cellulose and hemicellulose .
28
Y. Piñeros-Castro, M. Velásquez-Lozano / International Biodeterioration & Biodegradation 91 (2014) 24e28
achieve an efficient removal of lignin. However, other authors report higher degradation rates for lignin compared to the degradation rate of cellulose when treating wheat residues with P. chrysosporium (Huang et al., 2008). This opposite behavior could be explained by the complex structure of the lignocellulosic matrix of the oil palm residues. With regard to the results obtained with P. ostreatus after three weeks, the lowest values for the parameter (b) were observed for lignin, followed by hemicellulose and then cellulose, corroborating the higher affinity of this strain for lignin than for polysaccharides. The results agree with those reported for the degradation of wheat straw by P. ostreatus (Camarero et al., 1994) and by other white rot fungi like Euc-1 and Irpex lacteus (Dias et al., 2010). As can be observed in Table 2, the biological treatment using P. ostreatus for the degradation of oil palm residues produces a 51.91% delignified material after three weeks, without any significant alteration of the cellulose fraction. Therefore, the fungal treatment should be performed for no longer than three weeks if the objective of the treatment is the production of fermentable sugars, as the degradation of cellulose was low during this period. 4. Conclusion The experimental data determined for the biodegradation of lignin, cellulose and hemicellulose were described by the Weibull kinetic model. The model can be considered as a suitable tool for describing the changes suffered by lignocellulosic materials when treated with white rot fungi cultivated using the solid state fermentation technique and to study the culture conditions on the biomass biodegradation. A higher lignin degradation rate compared to the polysaccharides degradation rates was observed using P. ostreatus. The degradation of cellulose, an important component for the production of fermentable sugars, remained low (7.63%) while the total degradation of lignin reached 51.91% after treating for three weeks. Acknowledgements The present work was supported by the project: “Hydrolysis of oil palm lignocellulosic wastes to obtain fermentable sugars” funded by the Science, Technology and Innovation Administrative Department COLCIENCIAS project 110140520201; and executed by the Universidad Nacional de Colombia in Bogotá, in agreement with the Universidad de Bogotá Jorge Tadeo Lozano. References Agosin, E., Daudin, J.J., Odier, E., 1985. Screening of white-rot fungi on (14 C) ligninlabelled and (14 C) whole-labelled wheat straw. Appl. Microbiol. Biotechnol. 22, 132e138. Akin, D., Rigsby, L., Sethuraman, A., Morrison 3rd, W., Gamble, G., Eriksson, K., 1995. Alterations in structure, chemistry, and biodegradability of grass lignocellulose treated with the white rot fungi Ceriporiopsis subvermispora and Cyathus stercoreus. Appl. Environ. Microbiol. 61, 1591. Bates, D.M., Watts, D.G., 2008. Practical Considerations in Nonlinear Regression, Nonlinear Regression analysis and its Applications. John Wiley Sons, Inc, pp. 67e133. Camarero, S., Galletti, G.C., Martinez, A.T., 1994. Preferential degradation of phenolic lignin units by two white rot fungi. Appl. Environ. Microbiol. 60, 4509. Corzo, O., Bracho, N., 2008. Application of Weibull distribution model to describe the vacuum pulse osmotic dehydration of sardine sheets. LWT e sFood Sci. Technol. 41, 1108e1115. Cunha, L.M., Oliveira, F.A.R., Oliveira, J.C., 1998. Optimal experimental design for estimating the kinetic parameters of processes described by the Weibull probability distribution function. J. Food Eng. 37, 175e191. del Ri’o, J., Gutiérrez, A., 2001. Py-GC/MS study of eucalyptus globulus wood treated with different fungi. J. Anal. Appl. Pyrolysis 58, 441e452. Dias, A.A., Freitas, G.S., Marques, G.S.M., Sampaio, A., Fraga, I.S., Rodrigues, M.A.M., Evtuguin, D.V., Bezerra, R.M.F., 2010. Enzymatic saccharification of biologically
pre-treated wheat straw with white-rot fungi. Bioresour. Technol. 101, 6045e 6050. Duyvesteyn, W.S., Shimoni, E., Labuza, T.P., 2001. Determination of the end of shelflife for milk using Weibull hazard method. LWT e Food Sci. Technol. 34, 143e 148. Fillingham, I.J., Kroon, P.A., Williamson, G., Gilbert, H.J., Hazlewood, G.P., 1999. A modular cinnamoyl ester hydrolase from the anaerobic fungus Piromyces equi acts synergistically with xylanase and is part of a multiprotein cellulosebinding cellulase-hemicellulase complex. Biochem. J. 343, 215. Gupta, R., Mehta, G., Khasa, Y., Kuhad, R., 2011. Fungal delignification of lignocellulosic biomass improves the saccharification of cellulosics. Biodegradation 22, 797e804. Huang, D., Zeng, G., Peng, Z., Zhang, P., Hu, S., Jiang, X., Feng, C., Chen, Y., 2008. Biotransformation of rice straw by Phanerachaete chrysosporium and the related ligninolytic enzymes. Int. J. Biotechnol. 10, 86e92. Karunanandaa, K., Varga, G., 1996. Colonization of crop residues by white-rot fungi: cell wall monosaccharides, phenolic acids, ruminal fermentation characteristics and digestibility of cell wall fiber components in vitro. Anim. Feed Sci. Technol. 63, 273e288. Kelly-Yong, T.L., Lee, K.T., Mohamed, A.R., Bhatia, S., 2007. Potential of hydrogen from oil palm biomass as a source of renewable energy worldwide. Energy Policy 35, 5692e5701. Khajavi, S.H., Kimura, Y., Oomori, T., Matsuno, R., Adachi, S., 2005. Degradation kinetics of monosaccharides in subcritical water. J. Food Eng. 68, 309e313. Kirk, T.K., Croan, S., Tien, M., Murtagh, K.E., Farrell, R.L., 1986. Production of multiple ligninases by Phanerochaete chrysosporium: effect of selected growth conditions and use of a mutant strain. Enzyme Microb. Technol. 8, 27e32. Kuhad, R., Singh, A., Eriksson, K.E., 1997. Microorganisms and Enzymes Involved in the Degradation of Plant Fiber Cell Walls. Biotechnology in the Pulp and Paper Industry, pp. 45e125. Kumar, R., Mago, G., Balan, V., Wyman, C.E., 2009. Physical and chemical characterizations of corn stover and poplar solids resulting from leading pretreatment technologies. Bioresour. Technol. 100, 3948e3962. Oms-Oliu, G., Odriozola-Serrano, I., Soliva-Fortuny, R., Martín-Belloso, O., 2009. Use of Weibull distribution for describing kinetics of antioxidant potential changes in fresh-cut watermelon. J. Food Eng. 95, 99e105. Pandey, K.K., Nagveni, H., 2007. Rapid characterisation of brown and white rot degraded chir pine and rubberwood by FTIR spectroscopy. Eur. J. Wood Prod. 65, 477e481. Peleg, M., 2000. Microbial survival curves e the reality of flat “shoulders” and absolute thermal death times. Food Res. Int. 33, 531e538. Salvachúa, D., Prieto, A., López-Abelairas, M., Lu-Chau, T., Martínez, Á.T., Martínez, M.J., 2011. Fungal pretreatment: an alternative in second-generation ethanol from wheat straw. Bioresour. Technol. 102, 7500e7506. Sánchez, C., 2009. Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol. Adv. 27, 185e194. Schmidt, K., Bouma, J., 1992. Estimating shelf-life of cottage cheese using hazard analysis. J. Dairy Sci. 75, 2922e2927. Shi, J., Chinn, M.S., Sharma-Shivappa, R.R., 2008. Microbial pretreatment of cotton stalks by solid state cultivation of Phanerochaete chrysosporium. Bioresour. Technol. 99, 6556e6564. Shi, J., Sharma-Shivappa, R.R., Chinn, M., Howell, N., 2009. Effect of microbial pretreatment on enzymatic hydrolysis and fermentation of cotton stalks for ethanol production. Biomass Bioenergy 33, 88e96. Singh, D., Chen, S., 2008. The white-rot fungus Phanerochaete chrysosporium: conditions for the production of lignin-degrading enzymes. Appl. Microbiol. Biotechnol. 81, 399e417. Sluiter, A., Hames, B., Ruiz, R., Scarlata, C., Sluiter, J., Templeton, D., Crocker, D., 2008. Determination of Structural Carbohydrates and Lignin in Biomass. Laboratory Analytical Procedure NREL/TP-510e42618. Taniguchi, M., Suzuki, H., Watanabe, D., Sakai, K., Hoshino, K., Tanaka, T., 2005. Evaluation of pretreatment with Pleurotus ostreatus for enzymatic hydrolysis of rice straw. J. Biosci. Bioeng. 100, 637e643. Tomati, U., Galli, E., Pasetti, L., Volterra, E., 1995. Bioremediation of olive-mill wastewaters by composting. Waste Manage. Res. 13, 509e518. Torres, R., Girón, E., Rincón, F., Delgado, J., 2013. Colombian Oil Palm Statistical Data 2013. Fedepalma. Tuomela, M., Vikman, M., Hatakka, A., Itävaara, M., 2000. Biodegradation of lignin in a compost environment: a review. Bioresour. Technol. 72, 169e183. Unluturk, S., AtIlgan, M.R., Baysal, A.H., Unluturk, M.S., 2010. Modeling inactivation kinetics of liquid egg white exposed to UV-C irradiation. Int. J. Food Microbiol. 142, 341e347. van Boekel, M.A.J.S., 2002. On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells. Int. J. Food Microbiol. 74, 139e159. Yu, J., Zhang, J., He, J., Liu, Z., Yu, Z., 2009. Combinations of mild physical or chemical pretreatment with biological pretreatment for enzymatic hydrolysis of rice hull. Bioresour. Technol. 100, 903e908. Zhang, X., Yu, H., Huang, H., Liu, Y., 2007. Evaluation of biological pretreatment with white rot fungi for the enzymatic hydrolysis of bamboo culms. Int. Biodeterior. Biodegradation 60, 159e164. Zheng, H., Lu, H., 2011. Use of kinetic, Weibull and PLSR models to predict the retention of ascorbic acid, total phenols and antioxidant activity during storage of pasteurized pineapple juice. LWT e Food Sci. Technol. 44, 1273e1281.