Influence of saprophytic fungi and inorganic additives on enzyme activities and chemical properties of the biodegradation process of wheat straw for the production of organo-mineral amendments

Journal of Environmental Management 255 (2020) 109922

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Research article

Influence of saprophytic fungi and inorganic additives on enzyme activities and chemical properties of the biodegradation process of wheat straw for the production of organo-mineral amendments Jorge Medina a, b, Carlos M. Monreal c, Luis Orellana a, Marcela Calabi-Floody d, �lez e, Sebastia �n Meier f, Fernando Borie a, g, Pablo Cornejo a, * María E. Gonza a

Centro de Investigaci� on en Micorrizas y Sustentabilidad Agroambiental (CIMYSA), Departamento de Ciencias Químicas y Recursos Naturales, Scientific and Technological Bioresources Nucleus-BIOREN, Universidad de La Frontera, Temuco, Chile b Instituto de Ciencias Agron� omicas y Veterinarias, Universidad de O’Higgins, Campus Colchagua, San Fernando, Chile c Agriculture and Agri-Food Canada, Eastern Cereal and Oilseed Research Center, Ottawa, Ontario, Canada d Center of Plant, Soil Interaction and Natural Resources Biotechnology, Scientific and Biotechnological Bioresource Nucleus, BIOREN-UFRO, Universidad de La Frontera, Temuco, Chile e Departamento de Ingeniería Química, Universidad de La Frontera, Temuco, Chile. Scientific and Biotechnological Bioresource Nucleus, BIOREN-UFRO, Universidad de La Frontera, Temuco, Chile f Instituto de Investigaciones Agropecuarias (INIA), CRI Carillanca, P.O. Box 58-D, Temuco, Chile g Facultad de Ciencias de Recursos Naturales, Universidad Cat� olica de Temuco, Temuco, Chile

A R T I C L E I N F O

A B S T R A C T

Keywords: Enzymatic activities Lignocellulosic materials Organic matter stabilization

Cellulose and lignin as main components of crop residues have a significant influence on composting operations and composition of the final products. Both are strongly associated, and lignin can be considered an important barrier during the biodegradation process of lignocellulosic materials. Saprophytic fungi are efficient lignin degraders due to their complex enzymatic system. Therefore, the influence of the inoculation of saprophytic fungi (Coriolopsis rigida, Pleurotus ostreatus, Trichoderma harzianum and Trametes versicolor) and the supply of inorganic additives (Al2O3, Fe2O3 and allophanic soil) that promote the stabilization of carbon (C), were analyzed in the biodegradation of wheat straw (WS). The activity of Laccase (LAC), manganese peroxidase (MnP) and β-glucosidase and changes in temperature, pH and E4/E6 ratio were analyzed in a biodegradation process of 126 days. The activity of LAC, MnP and the E4/E6 ratio were significantly influenced and increased (enzymes) by fungi species, inorganic additives, and time of inorganic material addition, as well as their interactions (p < 0.05). The WS inoculated with T. versicolor showed the highest average activities for LAC, MnP and β-glucosidase (2000, 220 UL 1 and 400 μmol pNP g 1 h 1 respectively). Furthermore, the addition of Al2O3 and Fe2O3 increased all the activities regarded to the decomposition of WS and influenced the changes associated with the stabilization of OM in composted WS. In conclusion, the inoculation of WS with T. versicolor in combination with metal oxides improved the enzyme related to the biodegradation process of WS favorizing its stabilization in the medium time, which is of importance in the composting of residues with high C/N ratio.

1. Introduction It is projected that global crop production need to increase in 2% annually by 2050 to satisfy the growing food global demand with a concomitant raise of crop residues and stubbles produced. Wheat (Tri­ ticum aestivum L.) is one of the main crop worldwide produced, and current estimations suggest that about 1000 million tons of wheat

residues are annually produced and available for further use (Cala­ bi-Floody et al., 2018; Talebnia et al., 2010). Nevertheless, one of the main practice globally used for the removal of these residues is the open-field burning with the concomitant negative impacts in the at­ mospheric and soil environment (Udeigwe et al., 2015). As well as the open-field burning, the mismanagement of this materials in the fields and their decomposition may be associated to an increase of greenhouse

* Corresponding author. E-mail address: [email protected] (P. Cornejo). https://doi.org/10.1016/j.jenvman.2019.109922 Received 7 March 2019; Received in revised form 29 October 2019; Accepted 23 November 2019 0301-4797/© 2019 Elsevier Ltd. All rights reserved.

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Journal of Environmental Management 255 (2020) 109922

gas (GHG) emissions resulting from the process. Therefore, to avoid these adverse effects in the environment, nowadays, the reutilization practices appears as an essential biotechnological approach under food security and climate global change scenarios (Calabi-Floody et al., 2018, 2019). The incorporation of crop residues into the soil can positively in­ fluence the biological, chemical and physical properties of soil and enhance crop yields by increasing available nitrogen (N), phosphorus (P) and potassium (K) as well as organic C and N stocks in the soil (Cassman et al., 1996). However, the incorporation of excessive fresh organic residues into the soil may have adverse impacts (Senesi and Plaza, 2007; Bernal et al., 2009) because many soil functions require mature/stable organic matter (OM) (Guenet et al., 2012). Moreover, considering that the lignocellulosic residues are mainly composed of cellulose (30–40%), hemicellulose (20–25%) and lignin (15–25%), its relative chemical stability and high C/N ratio can also retard its de­ gradability being one of most important barriers under natural condi­ tions (Chen, 2014; Hubbe et al., 2010). Composting is an environmentally friendly treatment for the con­ version of organic wastes, where the OM is biologically decomposed, transformed and stabilized (Parillo et al., 2017). The resulting humified-OM is a suitable amendment for degraded or contaminated soils (Meier et al., 2015; Madej� on et al., 2016). Despite compost is defined as a stabilized material, some types of organic residues and compost have a higher rate of decomposition, lower stabilization of C and may affect the environment by serving as sources of GHG emissions during their production or even after being incorporated into soils. For example, Gao et al. (2019) described different levels of stability and humification in mixtures composted under the same conditions, as consequence of the diverse microbes and raw material composition, producing dissimilar mechanisms for humins formation. Under the context of C sequestration, compost can be a source of CO2 emissions from soils instead of being a sink in comparison to another more recal­ citrant organic amendments such as biochar (Bernstad et al., 2016; Bolan et al., 2012; Godbout et al., 2010; S� anchez-Monedero et al., 2010). Long-term observations showed that frequent compost application may increase soil C content (Paetsch et al., 2016), although a large part of the applied OM may be subject to a quick decomposition. In this sense, according to Fischer and Glasser (2013) the potential C sequestration due to compost management is limited in terms of C use efficiency and long-term C preservation even combined with organic farming and no till management. Inorganic materials such as clay minerals and metallic oxides have an €gel-Knabner et al., 2008). important role in soil OM stabilization (Ko Considering their physic-chemical properties, the latter materials are being applied in composting mixtures including animal manures, green waste compost, sewage sludge, olive oil mill wastewater, among others (Brunetti et al., 2008; Bolan et al., 2012; Chowdhury et al., 2016; Tu et al., 2016). These materials improve some physical properties of composting mixtures and may interact with OM through different re­ actions widely described in soil systems (Medina et al., 2015; Barthod et al., 2018). For example, Bolan et al. (2012) reported that oxides and clay minerals such as goethite and allophane, which are important constituents of soils, can enhance the C stabilization and end-product quality in composting mixtures, increasing the half-life (t1/2) of the amendments in soils. Furthermore, the utilization of these materials was also described for the reduction of GHG emission during composting being of increasing interest in the management of residues and there­ fore, production of organo-mineral amendments (Ren et al., 2019; Mao et al., 2018). Lignin is a polymer of phenylpropanoid substructures which forms a macromolecular complex with cellulose and hemicellulose preventing microbes from accessing simple organic substrates in lignocellulosic residues (Tuomela et al., 2000). Due to the random aromatic structure of lignin and its strong association, its breakdown is considered an important rate-limiting step during the composting of lignocellulosic

�pez and Garcia, 2006). The lignin depolymerization in the residues (Lo environment and laboratory conditions is mainly carried out by non-specific oxidizing enzymes which are able to use as substrate a large degree of compounds that includes benzyl, cinnamyl, naphthyl and aliphatic unsaturated alcohols (Hatakka, 2001; Zeng et al., 2014). Some basidiomycetes can decompose and mineralize lignin. These microor­ ganisms synthesize extracellular enzymes including lignin peroxidase (LiP), manganese peroxidase (MnP), and oxidases, such as laccase (LAC), making them proficient lignin degraders (Sahadevan et al., 2016; Hermosilla et al., 2017). To the best of our knowledge, no studies have been performed to evaluate the effect of fungi inoculation in combina­ tion with inorganic additives such as metallic oxides and clay minerals on the biodegradation and composting of lignocellulosic materials, and their further effect on enzyme production and OM stabilization. We hypothesized that the inoculation of saprophytic fungi in combination with the supply of inorganic additives will enhance the enzyme pro­ duction linked to the decomposition of WS and also will promote the stabilization of the mixture in an aerobic biodegradation process as model of a composting system at laboratory scale. Therefore, the main objective of this study was to evaluate the effects of different fungi strains (C. rigida, P. ostreatus, T. versicolor and T. harzianum) and the inorganic additives supply (metallic oxides and clay minerals from an allophanic soil) in the activity of LAC, MnP, and β-glucosidase. More­ over, this study also aimed to evaluate the changes in chemical prop­ erties associated to the stabilization of mixture and the potential degree of aromaticity and condensation of humic substances determined by the optical density via the E4/E6 ratio during the aerobic biodegradation of WS. 2. Material and methods 2.1. Wheat straw, fungi and inorganic materials The biodegradation process of wheat straw (WS) (Triticum aestivum L. var. Kumpa) was carried out in a dark room at a temperature of 25–28 � C for 126 days. The WS with a C/N ratio of ~130 was obtained from Maquehue experimental station (Universidad de La Frontera), La Araucanía Region, Chile. The WS was chopped into 1–2 cm and immersed in hot water at 60–80 � C for 2 h to reduce microbial contamination and enhance the fungal colonization (Colavolpe et al., 2014). The biodegradation process of WS was performed in autoclave bags containing 1.5 kg of moist WS (moisture content adjusted to 60%), that were kept open and at constant moisture applying distilled water weekly. The WS was initially inoculated with different fungal strains corresponding to Coriolopsis rigida (Berk. Et Mont.) Murrill (CR), Tra­ metes versicolor (L.:Fr.) Pillat (TV), Trichoderma harzianum Rifai (TH) and Pleurotus ostreatus (Jacq.) P. Kumm. (PO), obtained from the Laboratorio �n, Universidad de La Frontera, Temuco, Chile. The de Biorremediacio inoculum for each strain was prepared on Sabouraud Agar plates (65 g L 1 Sabouraud medium; 0.5 g L 1 MgSO4, 0.5 g L 1 KH2PO4, 0.16 g L 1 Fe2(SO4)3, and 0.2 μg L 1 thiamine dissolved into 1 L of distilled water; pH 5.6). The fungi were incubated for 7 days at 28 � C. When the culture with spores and heavy mycelia growth was generated, plates were dis­ rupted and suspended in 400 mL of sterilized dH2O (Almonacid et al., 2015). Suspensions (200 mL) were then added to each WS experimental units and thoroughly mixed. The inorganic additives: iron oxide (Fe2O3; Sigma Aldrich®), aluminum oxide (Al2O3; Sigma Aldrich®) and a ster­ ilized allophanic soil (Alloph Soil) collected from an allophane-rich horizon (Bt1) of the Pemehue soil series (Allophanic soil that contains 25% w/w of allophane), obtained at La Araucanía Region, Chile (39� 050 25’’, 72� 310 47’’, 140 m a.s.l.) were added in a proportion of 2% (w/w) at different times corresponding to 14, 56 and 112 days after fungus inoculation which is the starting time of this biodegradation experiment. Treatments with No additives (inorganic materials) were also conducted.

2

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2.2. Experimental design and sampling

was extracted using 50 mL of 0.5 M NaOH, shaken overnight at 20 � C, and centrifuged at 4500�g for 25 min. Absorbances of the supernatant were determined at 472 and 664 nm.

This biodegradation trial was a completely randomized experiment with a 3-level factorial design to evaluate the effect of the three factors: fungal strains (4), inorganic additives (3), and time of inorganic addi­ tives supply (3) in the different enzyme activities and chemical prop­ erties of compost, producing a total of 48 treatments (SD 1). The mixtures were aerated by manual turning at a regular interval of 2 weeks at the beginning and then weekly and sampled every 14 days. Three samples of 20 g were taken from each bag and thoroughly mixed to obtain a representative sample for biochemical and physicochemical analyses. Collected samples were homogenized, oven dried at 70 � C for 3 days, grounded to <1 mm and stored at 20 � C until chemical analysis. For the enzymatic activities determination, fresh samples were stored at 4 � C previous to their analysis.

2.5. Statistics All data sets were subjected to three-way ANOVA after corroborating normality and homoscedasticity to determine the main effects of fungal inoculation, inorganic additive, application time and their interactions. When experimental data did not show a normal distribution according to Kolmogorow-Smirnov test, data were transformed using Ln function before statistical analysis. Levene test was used to analyze the homo­ geneity of variances. Repeated measures analyses were performed to analyze the above-mentioned factors. The global means were subjected to principal components (PC) analysis to generate groups with homo­ geneous behavior. Cluster analyses using the farthest-neighbor as agglomerative method were performed for clustering the different experimental individuals. The correlation among the different variables was analyzed using the Pearson coefficient (r). Significance level was established at p < 0.05. Statistical analyses were performed using IBMSPSS v.23 (IBM Corp., USA).

2.3. Enzyme assays Enzymatic extracts were obtained every two weeks. Briefly, 2 g of WS compost from the biodegradation process were mixed with 25 mL 50 mM CH3COONa, pH 4.5 (Ballaminut et al., 2009), shaken at 120 cycles per min for 2 h at 4 � C and centrifuged at 5000�g for 20 min. The su­ pernatant was filtered (Whatman no. 3) and kept frozen ( 80 � C) until use. LAC and MnP activities were used as proxies for ligninolytic ac­ tivity, whereas β-glucosidase activity (Tabatabai, 1982) was used as a proxy for hydrolytic activity. LAC activity was determined by the oxidation of 2,20 -azino-bis-(3-ethylbenzothiazoline-6-sulphonic acid) (ABTS). The reaction mixture contained 300 μL of CH3COONa 50 mM, pH 5.0), 100 μL ABTS (20 mM), and 1000 μL of enzymatic extract. Re­ actions were carried out for 5 min at 25 � C, and absorbance related to the formation of stable cation radical ABTS was measured at 420 nm (Pal­ mieri et al., 1993). MnP was assayed through the oxidation of 2,6-dime­ thoxyphenol (DMP) (Peri�e and Gold, 1991). The reaction mixture contained 200 μL of buffer sodium malonate (250 mM; pH 4.5), 50 μL of DMP (20 mM), 100 μL of H2O2 (4 mM), 50 μL MnSO4 (20 mM), and 600 μL of enzymatic extract. Enzyme activity was determined after a 5-min reaction at 25 � C, and absorbance of the reaction product was measured at 469 nm. For both ligninolytic activities, one activity unit was defined as the amount of enzyme that oxidized 1 μmol of ABTS/DMP per minute, and the activities were expressed in U L 1 (unit of enzymatic activity). The activity of β-glucosidase was related to the amount of p-nitrophenol (pNP) released using p-nitro­ phenyl-β-D-glucopyranosyde (pNPG) as substrate. The reaction mixture contained 400 μL of 2 mM pNPG (Herr, 1979) in 50 mM of sodium citrate buffer (pH 4.8), 100 μL of enzymatic extract and incubated at 50 � C for 30 min. At the end of the incubation 1 mL of 2 M Na2CO3 (pH 11.0) was added to stop the reaction. The amount of pNP released was determined by measuring absorbance at 410 nm.

3. Results 3.1. Influence of factors on enzyme activities The activities of LAC, MnP, β-glucosidase, and the E4/E6 ratio increased significantly and were influenced by fungi and inorganic ad­ ditives, as well as the single and triple interactions of fungi*time, fun­ gi*additives, additives*time and fungi*additives*time (Table 1). The time of inorganic material addition as single factor was only significant for LAC and MnP activities. All factors and interactions significantly increased LAC activity, Table 1 F-values and significance for the main effects and factors interactions related to the analyzed dependent variables by means of a multifactorial ANOVA. Variable

Factor

F-value

p-value

Laccase

Fungus (F) Inorganic Material (M) Time of addition (T) FxM FxT MxT FxMxT F M T FxM FxT MxT FxMxT F M T FxM FxT MxT FxMxT F M T FxM FxT MxT FxMxT

1483.8 890.7 280.4 226.1 603 292.2 384.5 2207.9 928.8 413.4 196.9 726 278.3 227.4 200.76 20.66 0.19 27.33 22.003 62.75 38.99 14.48 8.30 3.98 8.32 5.10 2.93 3.25

*** *** *** *** *** *** *** *** *** *** *** *** *** *** *** *** NS *** *** *** *** *** *** ** *** *** * ***

MnP

2.4. Chemical analyzes for monitoring the process β-glucosidase

For monitoring the evolution and phases of the biodegradation process, temperature, pH and E4/E6 ratio were determined every two weeks. The pH was measured on water-extracts obtained from the samples (1:10 w/v), by stirring a 0.5 g of the WS with 5 mL of distilled water for 30 min at room temperature. The pH was measured by potentiometry using a digital pH meter. The temperature was monitored thrice weekly at different places and depths into the experimental unit (bags), including the middle of the pile and external layers by using a digital thermometer. As index of optical density of humic fraction we used the E4/E6 ratio, that express the relative aromaticity and conden­ sation of humic substances (related to the degree of humification) (Zbytniewski and Buszewski, 2005; Filcheva et al., 2018). High E4/E6 values (>5) are characteristic of fulvic acids and indicate low humifi­ cation, and values < 5 indicate high humification and presence of humic acids (Pansu and Gautheyrou, 2006). Briefly, 1 g of oven dried samples

E4/E6

* p-value <0.05. ** p-value <0.01. ***p-value<0.001. NS: not significant. 3

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explaining the total LAC variability by 20, 12 and 2% for single factors (fungi, additives and time of addition, respectively) (Table 1). The sig­ nificant interactions accounted for 65% of all the LAC variability. TV showed the highest LAC activity (2000 UL 1), greater than that caused by other fungi (Fig. 1A). Moreover, significant differences for LAC ac­ tivity were also observed between inorganic materials (Fig. 1B, black bars) and time of addition of inorganic materials (Fig. 1C). The addition of Fe2O3 and time of addition at 112 and 56 days after fungi inoculation showed the highest LAC activity (1830 UL 1, 1710 UL 1 and 1650 UL 1, respectively) in comparison to the other treatments. Conversely, treat­ ments inoculated with TH (1430 UL 1), the addition of Alloph Soil (1380 UL 1) and time of addition at day 14 showed the lowest activity (Fig. 1A, B and 1C; black bars). Also, the addition of Al2O3 and time of addition 56 days after the fungi inoculation showed a high LAC activity after 126 days of biodegradation process (Fig. 1B and C). All factors and interactions significantly influence MnP activity. Fungi, additives and time of addition accounted for 30, 13 and 4%, respectively of the total MnP variability. Single, double and triple in­ teractions accounted for 54% of all the variability in MnP activity (Table 1). TV showed a higher MnP activity (220 UL 1) compared to TH (138 UL 1), PO (142 UL 1), and CR (145 UL 1) (Fig. 1A, grey bars). As for LAC activity, the addition of Fe2O3 also increased the MnP activity (190 UL 1), and it was greater than the activity observed in treatment without additives (NA) (151 UL 1), and higher than those shown under Al2O3 and Alloph Soil (Fig. 1B). The addition of Alloph Soil decreased MnP activity (135 UL 1). The time of addition also influenced the MnP activity (Table 1) and inorganic materials added at 112 days (175 UL 1) and 56 days (160 UL 1) after fungi inoculation presented the higher MnP activity relative to those treatments added 14 days (145 UL 1) after fungi inoculation (Fig. 1C).

Fungi, inorganic additives and their interactions significantly influ­ enced β-glucosidase activity. These two factors accounted for 29 and 3% of the total variability in the enzyme activity, respectively (Table 1). Inoculation with TV caused the highest global activity of β-glucosidase (~400 μmol pNP g 1 h 1, Fig. 1A). The effects by TV on the enzyme activity were significantly greater than those caused by the other fungi. Inoculation with CR also resulted in a high global mean value for β-glucosidase activity compared to PO and TH. When WS was supplied with Al2O3 as additive the activity of β-glucosidase was significantly higher (~350 μmol pNP g 1 h 1) than treatments without inorganic additives (<300 μmol pNP g 1 h 1) (Fig. 1 B, white bars). In general, the dynamics of LAC and MnP enzymatic activities showed higher activity values towards the end of the biodegradation process, while β-glucosi­ dase activity showed a quite different tendency (SD 2, 3, 4). 3.2. Phases of the biodegradation process and organic matter stability Changes in temperature, pH and E4/E6 ratio were used for moni­ toring the process phases, microbial activity and OM transformations that can be related to stability of mixtures. Temperatures reached the typical phases described for lignocellulosic material in aerobic com­ posting systems, with an initial mesophilic phase (>20 � C) followed by a short thermophilic phase (42–45 � C) and finishing with a mesophilic phase during the final stage of this biodegradation process with tem­ peratures near the room temperature (20–25 � C). Overall, the pH in all treatments increased as the process progressed, ranging from pH ~4.0 to 6.0 at the beginning (around day 1–10) up to pH ~8.5–9.0 at the end of the process (around day 112–126; Fig. 2). Wheat straw inoculated with CR and supplied with Al2O3 as additive incorporated at day 112 showed the lowest pH (3.4) at day 14 and 8.5

Fig. 1. Average effect of single factors: fungi species (A), inorganic additives (B) and time of application of inorganic additives (C) on the activity of Laccase (black bars), MnP (grey bars) and β-glucosidase (white bars). Lower-case letters indicate significantly different means at p < 0.05 (LSD test). 4

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Fig. 2. Variation in pH during the biodegradation process of WS inoculated by Coriolopsis rigida, Trametes versicolor, Pleurotus ostreatus, and Trichoderma harzianum with No additives and supplied with the inorganic additives corresponding to: Aluminum oxide (Al2O3); Iron oxide (Fe2O3), and the B horizon (Bt1) of an allophanic soil (Alloph Soil) that were applied at days 14, 56 and 112 after the inoculation of fungi strains. .X axis shows days of composting.

after 112 days of biodegradation process. On the other hand, treatments inoculated with PO showed the highest pH (9.1) at the end of the experiment. Wheat straw inoculated with TV and TH had similar pHs with values below 4.0 during the initial phase (days 1–42), increasing up to 8.0 at the final stage of the process of biodegradation (days 84–112; Fig. 2). The ANOVA test for global means showed that E4/E6 ratio was significantly affected by all the experimental factors and their in­ teractions as well as LAC and MnP activities (Table 1). Fungi species, inorganic additives and time of addition accounted for 17, 10 and 3% of total E4/E6 data variability, respectively (Table 1). All the interactions represent 70% of total data variability being the interaction of fungi species*inorganic addition the most important (30% of total variability; Table 1). Under inoculation with CR the E4/E6 ratio decreased until day 56 and continued to decrease up to day 84 under the inoculation with other fungi species. Subsequently, the E4/E6 ratio increased to day 112, but it decreased again by the end of the biodegradation process (day 126; Fig. 3). The E4/E6 ratio values were lowest (8–8.5) under PO and TH (Fig. 4A). Conversely, treatments inoculated with CR and TV showed higher ratios reaching global mean values of 9–9.3, respectively (Fig. 4A). The addition of Alloph Soil increased the E4/E6 ratio up to ~9.5, whereas the addition of metallic oxides (Al2O3 and Fe2O3) did not

showed significant effects (Fig. 4B). The time of addition had a signifi­ cant effect on the E4/E6 ratio. The E4/E6 ratio was highest (~8.8) at 14 and 56 days of addition, and lowest (~8.5) at 112 days after fungi inoculation (Fig. 4C). 3.3. Multivariate relationships Highly significant correlations were observed between the lig­ ninolytic enzymes LAC and MnP (r ¼ 0.9), whereas moderate correlation between β-glucosidase and the ligninolytic enzymes (r ¼ 0.6) were recorded (Table 2). The high correlations between the ligninolytic enzyme activities were evident after the PC analysis wherein the vari­ ables LAC and MnP are clustered closely in the positive values of PC1 (Fig. 5A). In comparison, pH and E4/E6 appear to be independently distributed. The factorial analysis resulted in two principal components explaining 76% of total variance. Despite of a moderate Pearson corre­ lation coefficient (r ¼ 0.6) between β-glucosidase and ligninolytic en­ zymes, the activity of β-glucosidase was closely correlated with the others and grouped in the same quadrant after PCs extraction. The pH was not correlated with enzymes and E4/E6 ratio, whereas E4/E6 showed a significant correlation (p < 0.05) but with a low-to-moderate negative 5

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Fig. 3. Variation in E4/E6 ratio during the biodegradation process of WS inoculated with Coriolopsis rigida, Trametes versicolor, Pleurotus ostreatus and Trichoderma harzianum with No additives and supplied with the inorganic additives corresponding to: Aluminum oxide (Al2O3); Iron oxide (Fe2O3), and the B horizon (Bt1) of an allophanic soil (Alloph Soil) that were applied at days 14, 56 and 112 after the inoculation of fungi strains. X axis shows days of composting.

Pearson coefficient (r ¼ 0.2 and 0.4 respectively) regarded to LAC and MnP. Both pH and E4/E6 were not correlated according to PC analysis. (Table 2; Fig. 5A). The non-hierarchical cluster analysis based on PCs generated 5 different groups (Fig. 5B). Groups 1 and 2 are composed mainly of treatments inoculated by CR and PO, which presented a high similarity as determined by the smaller Euclidean distances, and yet they were very different than the other 3 groups. The dendrogram showed high Euclidean distances between the grouped treatments of TH and the other groups of fungal species that showed high enzymatic activities in group 2, suggesting critical differences in terms of ligninolytic activity. Groups 3 and 4 were composed mainly of treatments inoculated with TV and PO that also showed low Euclidean distances between them, suggesting greater similarities, but high differences with the other groups.

et al., 2012; Sahadevan et al., 2016; Zavarzina et al., 2011). High levels of LAC and MnP may suggest that the fungal species are able to rapidly delignify substrates. Our results indicate that TV was the most efficient fungi in producing enzymes involved in WS degradation and OM transformation (Arriagada et al., 2009; Zhang et al., 2016). The inocu­ lation of WS with TV increased the activities of LAC (~2000U L 1) and MnP (~230 U L 1) and showed a significant influence relative to those effects shown by other fungi inoculated treatments, such as TH (~1500 U L 1) for LAC and MnP (150 U L 1) activities (Fig. 1A). It should be noted that treatments inoculated with TV also showed high β-glucosi­ dase activity (~400 μmol pNP g 1 h 1), an indication of cellulose depolymerization. β-glucosidase is associated with the C cycle and transformation/decomposition of cellulose and ligno-cellulose polymers in composting systems (Mondini et al., 2004). In our study, WS inocu­ lated with CR also showed an important β-glucosidase activity (Fig. 1A). The activity of LAC and MnP enzymes were relatively lower compared to previous reports (Sahadevan et al., 2016). Some type of humic acids may inhibit the activity of LAC enzyme due to the effect of carboxylic groups from soil OM (Zavarzina et al., 2011). The inhibition of LAC has been also reported by the negative influence of trace ele­ ments (Lorenzo et al., 2005). Ions as Fe3þ and Fe2þ has been described as strong inhibitors of LAC (Wang et al., 2016); however, other studies

4. Discussion 4.1. Enzymatic activities Production of ligninolytic enzymes is common among selectively lignin-degrading basidiomycetes capable of polymerizing and depoly­ merizing lignin and HS (Zeng et al., 2014; Grinhut et al., 2007; Hachicha 6

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Fe2þ ion was reported by Shah et al. (2010) when compared to copper and iron nanoparticles that decreased the production of Laccase. A positive response was also described by Hermosilla et al. (2017) where the addition of Fe2þ and Mn2þ as inducers of the enzymatic activities increase both the activity of LAC and MnP with a concomitant enhancement of lignin degradation (50%). On the other hand, Gao et al. (2006) reported an increase in the amount and size of mycelium in presence of Fe2þ which suggest a greater activity and production of enzymes by the fungus. Furthermore, the addition of Fe2þ can promote the production of hydroxyl radicals during Fenton like-reactions that can be considered as the initial agents of the lignocellulose degradation (Evans et al., 1994). Fenton like-reactions, as an advanced oxidation process involve the generation of highly oxidizing radical species like hydroxyl radicals (�OH) through the catalytic reaction of Fe2þ to Feþ3 in presence of H2O2 (Garrido-Ramírez et al., 2010) and have been widely described as one of the main mechanism of lignin decomposition related to brown rot fungi strains (Zavarzina et al., 2011). Huang et al. (2019) recently reported the synergism between Phanerochaete chrysosporium with ferroferric nanoparticles in the bio decomposition of lignocellulose that was mainly based on a Fenton-reaction-aid pattern. Accordingly, our results indicate that the single-to-triple interactions of inorganic materials, time of addition and combination with fungal inoculation enhance the activities of LAC and MnP for decomposing WS during the biodegradation process. 4.2. Biodegradation process mediated by fungi and inorganic additives In our study, biochemical and chemical properties were used as criteria to evaluate the stability of WS compost and the impact of mi­ croorganisms and additives as conditioners of the process. The tem­ perature at the center of the experimental units (bags) that relates to the metabolic activity of microorganisms involved in the process increased from >20 � C at day zero (mesophilic and colonizing phase) to a maximum of ~42–45 � C at day 28 (thermophilic phase) (Data not shown). Thereafter, the temperature decreased gradually to ~25–28 � C (room temperature) towards the end of the process (102 days). The temperature rose slowly to the levels associated to thermophilic phase in composting systems and it can be attributed to the high C/N ratio of the initial WS (~130:1), which is a critical factor during process (Hubbe et al., 2010). In fact, the process produces heat as result of growth and activity of microorganisms and the initial C/N ratio above 40 may slows down biodegradation process as consequence of the lack of available N for microorganisms (Eiland et al., 2001; L� opez et al., 2002; Haddadin et al., 2009). In this regard and despite of the high initial C/N ratio of WS, the inoculation with the saprophytic fungi such as T. versicolor and the addition of inorganic additives allowed to significantly reduce the C/N ratio to 30–70 after 126 days of aerobic biodegradation (not pre­ sented results). Temperature has also an important influence in the colonization and growth of fungi species. In this sense, Hao and Wang (2015) reported that optimal temperature for mycelium growth of Pleurotus sp. was 28 � C, with a limited growth at 36 � C. On the other hand, Hachicha et al. (2012) described a rise of temperature (over 45 � C) during the 2 weeks after the inoculation of T. versicolor, (inoculated at the end of the ther­ mophilic phase) and an increase of the humification and lignin

Fig. 4. Average effect of single factors: fungi species (A), inorganic materials (B) and time of addition (C) on the E4/E6 ratio. Lower-case letters indicate significantly different means at p < 0.05 (LSD test).

reported the positive influence of ions such as Fe2þ, Cu2þ and Mn2þ on LAC and Mn2þ on MnP activity (Baldrian et al., 2005; Salvachúa et al., 2013). In our study, the addition of metallic oxides significantly influ­ enced the activity of all the enzymatic activities studied, where Fe2O3 was associated with the highest activity for LAC and MnP (Fig. 1B). Furthermore, the addition of Al2O3 to fungi inoculated WS also increased the activity of all the studied enzymes, especially β-glucosi­ dase (Fig. 1B). The increase in LAC and MnP by TV in the presence of

Table 2 Bivariate correlations (R Pearson) between the analyzed variables and principal components obtained. Variables

2

3

LAC (1) MnP (2) β-glucosidase (3) E4/E6 (4) pH (5)

0.945**

0.641** 0.630**

4

5 0.295* 0.403* 0.132

p-values <0.01**; p-value <0.05*. 7

0.113 0.122 0.252* 0.063

PC1

PC2

0.938** 0.954** 0.790* 0.449 0.236

0.044 0.102 0.279 0.606** 0.809**

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Journal of Environmental Management 255 (2020) 109922

Fig. 5. A) Principal component (PC) analysis of the response variables pH, enzymatic activities (Laccase, MnP and β-glucosidase) and E4/E6 ratio. B) Nonhierarchical cluster analyses grouped in terms of fungi*time of inorganic material addition interaction for Coriolopsis rigida inoculated treatments (CR); Trametes versicolor inoculated treatments (TV); Pleurotus ostreautus inoculated treatments (PO) and Trichoderma harzianum inoculated treatments (TH). Numbers indicate the time of application of inorganic additives where 1 ¼ 14 days after fungi inoculation; 2 ¼ 56 days after fungi inoculation and 3 ¼ 112 days after fungi inoculation.

decomposition, suggesting a positive effect of fungi on composting mixtures with a relative tolerance of T. versicolor to temperatures over 40 � C. In other study, Gong et al. (2017) reported similar results where the white-rot fungi T. versicolor and P. chrysosporium caused a faster and higher increase of temperature, increased the duration of thermophilic phase and reduced the time to achieve the maturity of compost in green waste mixtures. Therefore, the rise of temperature as the recorded on thermophilic phase of composting systems may affect the growth and colonization of some saprophytic fungi species (mesophilic) and should be considered as a factor in future studies to select properly the strains and to stablish a suitable moment for the inoculation. On the other hand, Sundberg et al. (2004) suggested that the low initial pH (4–6) can limit also the microbial activity in the transition from mesophilic to ther­ mophilic conditions and delay the increase of temperature. According to the literature, in regular composting operations, the low initial pH as the observed in this study can be associated to the production of short chain organic acids (e.g., lactic and acetic acids) at the first stages of the biodegradation process as consequence of the activity of certain groups of bacteria, microbial immobilization of NHþ 4 and the nature of starting materials (Cayuela et al., 2008; Haddadin et al., 2009; Hubbe et al., 2010). The increase of pH towards the end of the biodegradation process may be attributed to the degradation of organic acids, OM mineraliza­ tion, active production of NHþ 4 as the process progressed (Hubbe et al., 2010). Nevertheless, caution need to be exercised to avoid incorrect interpretations about pH variations. Here, we used the E4/E6 ratio as a simple and proxy indicator of the degree of humification of the OM, that expresses the degree of condensation of aromatic rings comparing the absorbance at 472 and 664 nm (Filcheva et al., 2018). Low E4/E6 values (<10) stand for highly

humified materials due to polycondensed aromatic rings absorb more light at 664 nm, and high E4/E6 values (>15) stand for low humified OM (Zbytniewski and Buszewski, 2005). On average, the E4/E6 ratio values for the different treatments appeared to decrease, from ~15 to 5 during the first 56 days of biodegradation process and tended to slightly in­ crease thereafter up to ~12 until day 112, to finally decrease to ~8 at day 126 (Fig. 3). Similar trends have been reported for different com­ posting mixtures suggesting potential aromatic polycondensation of macromolecules towards the end of the process (Brunetti et al., 2007; Khan et al., 2009). Like the enzyme activities, the E4/E6 ratio was also significantly influenced by fungi, inorganic materials, time of addition and their interactions (Table 1, Fig. 4). As the biodegradation of WS progressed, the E4/E6 ratio of treatments receiving Fe2O3 and Al2O3 (e. g., TV inoculated) was lower than the measured in untreated WS (~5.3 and 13, respectively) (Fig. 3D). The latter suggests a final relatively humified material but also supports the hypothesis that inorganic ad­ ditives serve as catalyst of the humification/stabilization during the biodegradation process (Brunetti et al., 2008). However, the E4/E6 ratio must be interpreted with care since it can also be governed by the mo­ lecular weight and total acidity of the OM fraction extracted by NaOH, it can be affected by pH and correlated with the concentration of carbon, oxygen and CO2. Therefore, it is not strictly linked to the fused and condensed aromatic rings (Chen et al., 1977). Although most of the humification process is biologically driven, there is also significant ev­ idence for abiotic condensation and oxidative polymerization (Shindo and Huang, 1984; Huang et al., 1999). These reactions occur between added OM with the soil mineral surfaces and newly synthetized HS (Jastrow et al., 2007) and could also occur with other organic matrices such as inorganic amended-compost (Bolan et al., 2012). Moreover, 8

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metallic oxides appear to limit C decomposition by the formation of organo-mineral complexes and micro aggregates of organic matrices (Porras et al., 2018). In this sense, Medina et al. (2017) reported that the addition of inorganic additives to WS composting produce micro-to nano-molecular interactions between the OM matrix and inorganic materials suggesting the formation of inner-sphere complex and microand nano-aggregates. However, other analyzes must be considered in future studies (e.g., FTIR and NMR spectroscopy, characterization of HS among others). Our results warrant further research on the role of inorganic additives in the stabilization of OM from WS and other similar materials during composting of organo-mineral amendments.

Declaration of competing interest None. Acknowledgements The authors thank FONDECYT N� 3170677 (J. Medina), Associative Research Program for Topics in Mining ACM170002 (P. Cornejo), FONDECYT N� 11150555 (M. Calabi) and CONICYT/FONDAP/ 15130015 (P. Cornejo). The ELAP-Canada program financed a stay at the Ottawa Research and Development Center of Agriculture and AgriFood Canada (J. Medina).

4.3. Multivariate analysis

Appendix A. Supplementary data

The measured ligninolytic enzyme activities were significant but low and negatively correlated with the E4/E6 ratio under the studied experimental conditions (Table 2). In this sense, the data obtained from this biodegradation study may indicate that depolymerization/poly­ merization reactions may occur simultaneously with a slight preferential depolymerization as opposed to humification processes during the whole duration of the study. These results may be explained by the heterogeneous spatial distribution of microsites, containing a high di­ versity of microbial communities involved in different reactions during the biodegradation process. Schnitzer and Monreal (2011) indicated that a microbial and biochemical humification pathway in soils proceeds via oxidation of oxo-acids prior to synthesis and polymerization of large size polyketides. In the latter process, intracellular and complex extra­ cellular multi-enzyme systems from different microorganisms, may cooperate to catalyze the biodegradation process. On the other hand, the cluster analysis revealed five different groups where groups 1 and 2 share some similarities related to enzymatic activities, pH and E4/E6 ratio, and cluster 4 and 5 also (Fig. 5). Here, the TH inoculated treat­ ments grouped mainly within group 3 showing high Euclidean distance in comparison to the other groups of fungi inoculated compost. The latter appears to reflect strong differences between TH and the other fungi in terms of enzymatic activities associated to lignin/cellulose depolymerization. Therefore, the results of this study support the search for efficient fungi isolates and inorganic materials as a tool for improving the biodegradation of lignocellulosic materials. Further research is war­ ranted to elucidate chemical and structural changes of end-products, and to identify the main mechanisms operating during the biodegra­ dation process of WS inoculated with fungi and amended with inorganic additives.

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5. Conclusions Our study highlights the use of saprophytic fungi and the supply of inorganic additives at different times of the process due to both signif­ icantly enhanced the activity of LAC, MnP and β-glucosidase, enzymes related to the decomposition of lignocellulosic materials. The utilization of fungi and inorganic additives also affected significantly the E4/E6 ratio used for monitoring OM stabilization. In this regard, TV appears as the most efficient strain increasing the activity of all the enzymes associated with lignocellulose depolymerization, whereas the addition of metallic oxides, especially Fe3O2, also enhanced the enzymatic ac­ tivities, suggesting a potential synergism for WS decomposition between fungi strains and metallic oxides. The activities of LAC and MnP strongly correlated to each other, whereas pH and the E4/E6 ratio were not correlated with any variables. According to the factorial analysis the two chemical properties were independently distributed and together with the enzymatic activities accounted for 75% of the total experimental variance represented in two PCs. Under the experimental conditions of our research, the utilization of fungal inoculation and addition of inor­ ganic materials appear as suitable biotechnological tools capable for enhancing WS composting and produce organo-mineral amendments. 9

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