Bleaching of Hardwood Kraft Pulp with Manganese Peroxidase from Phanerochaete sordida YK-624 without Addition of MnSO 4
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1 APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Mar. 1996, p Vol. 62, No /96/$ Copyright 1996, American Society for Microbiology Bleaching of Hardwood Kraft Pulp with Manganese Peroxidase from Phanerochaete sordida YK-624 without Addition of MnSO 4 KOICHI HARAZONO, RYUICHIRO KONDO,* AND KOKKI SAKAI Department of Forest Products, Faculty of Agriculture, Kyushu University, Fukuoka , Japan Received 7 August 1995/Accepted 27 December 1995 In vitro bleaching of an unbleached hardwood kraft pulp was performed with partially purified manganese peroxidase (MnP) from the fungus Phanerochaete sordida YK-624 without the addition of MnSO 4 in the presence of oxalate, malonate, or gluconate as manganese chelator. When the pulp was treated without the addition of MnSO 4, the pulp brightness increased by about 10 points in the presence of 2 mm oxalate, but the brightness did not significantly increase in the presence of 50 mm malonate, a good manganese chelator. Residual MnP activity decreased faster during the bleaching with MnP without MnSO 4 in the presence of malonate than in the presence of oxalate. Oxalate reduced MnO 2 which already existed in the pulp or was produced from Mn 2 by oxidation with MnP and thus supplied Mn 2 to the MnP system. The presence of gluconate, produced by the H 2 O 2 -generating enzyme glucose oxidase, also improved the pulp brightness without the addition of MnSO 4, although treatment with gluconate was inferior to that with oxalate with regard to increase of brightness. It can be concluded that bleaching of hardwood kraft pulp with MnP, using manganese originally existing in the pulp, is possible in the presence of oxalate, a good manganese chelator and reducing reagent. * Corresponding author. Mailing address: Department of Forest Products, Faculty of Agriculture, Kyushu University, Hakozaki, Fukuoka , Japan. Phone: (92) , ext Fax: (92) Electronic mail address: kondo@agr.kyushu-u.ac.jp. Multistage bleaching procedures using a combination of treatment with chlorine-based chemicals and alkaline extraction are normally used in bleaching of kraft pulp, the most popular chemical pulp. There has been growing environmental concern about chlorinated organic substances, including toxic, mutagenic, and carcinogenic polychlorinated dioxins, dibenzofurans, and phenols, in the effluent from such bleaching of conventional kraft pulp (4, 7, 36). Today, general concern about the environmental impact of chlorine bleaching effluents has led to a trend toward elementary chlorine-free or totally chlorine-free bleaching methods. Biobleaching with white rot fungi, including Trametes (Coriolus) versicolor (1, 32, 38) and fungus strain IZU-154 (9, 10, 30), which can selectively degrade lignin in wood, has been studied by some workers to establish chlorine-free bleaching processes. However, bio bleaching with fungi is rather slow compared with chemical bleaching, and the cellulose in the pulp may be attacked by polysaccharidases. Thus, direct application of the ligninolytic enzymes involved in bleaching with fungi, lignin peroxidase (2), manganese peroxidase (MnP) (23, 33), and laccase (6), has been attempted. Paice et al. and we have reported that MnP and laccase activities but not lignin peroxidase activity are detected during biobleaching of unbleached hardwood kraft pulp by white rot fungi with bleaching ability (15, 23, 32). Recently, some reports have shown that MnP plays an important role in the bleaching of unbleached hardwood kraft pulp by white rot fungi (15, 17, 19, 23, 33). MnP, first discovered in Phanerochaete chrysosporium (26, 34), is known to be secreted by many lignin-degrading fungi, including T. versicolor (18, 33), P. sordida (41), and others (31, 35). MnP is a heme-containing enzyme and oxidizes Mn 2 to Mn 3, which chelated with an organic acid, in turn oxidizes phenolic substrates, including lignin model compounds (47 49), dehydrogenative polymerizate (50), and highmolecular-weight chlorolignin (27, 30). Therefore, we performed in vitro bleaching of the kraft pulp with MnP from the fungus P. sordida YK-624 (22), which was isolated from decayed wood obtained from a forest and exhibited remarkable bleaching ability with the pulp (15, 23). When the pulp was treated with partially purified MnP in the presence of MnSO 4, Tween 80, and malonate with continuous addition of H 2 O 2, the brightness of the pulp increased by about 10 points and the kappa number decreased by about 6 points, suggesting that in vitro degradation of residual lignin in hardwood kraft pulp with MnP is possible (22). However, there are some differences between in vivo bleaching with fungi and in vitro bleaching with MnP with respect to treatment conditions. Major differences between the two bleaching systems were the use of additional MnSO 4 and high concentrations of malonate as an Mn 3 chelator during in vitro bleaching with MnP; the consistency of pulp during bleaching also differed significantly between the two systems. Since the solid-state fermentation system used in our work added only water and mycelia to the pulp (15, 23), the manganese in the pulp must have been used by the MnP catalytic system. We reported that unbleached hardwood kraft pulp was not brightened by P. sordida YK-624 when metal ions had previously been removed from the pulp by acid treatment but that the ability of the fungus to bleach this pulp was restored when Mn salts were added back to the pulp (16). Chemical species of Mn present in the pulp is unclear. Insoluble MnO 2 accumulates in wood decayed by some white rot fungi (5). Mn 3 oxidized by MnP is transformed to Mn 4 (MnO 2 ) and Mn 2 due to hydrolysis and disproportionation (11). Organic acids such as lactate, malonate, and oxalate, which chelate Mn 3 generated by MnP, stabilizing Mn 3 in aqueous solution, play important roles in the MnP system. The white rot fungi, including P. chrysosporium and T. versicolor, secrete organic acids which function as Mn 3 chelators (21, 25, 39). It was reported that millimolar concentrations of oxalate are produced by various fungi such as P. chrysosporium and T. versicolor (8, 25, 28, 42, 49). The physiological concentrations of oxalate stimulate optimal MnP activity (21, 24, 28, 39). 913
2 914 HARAZONO ET AL. APPL. ENVIRON. MICROBIOL. Oxalate is also known to have reductive activity (44). In the present paper, we show the successful bleaching of kraft pulp with MnP without the addition of MnSO 4 by using oxalate as an effective Mn 3 -chelating and reductive agent. MATERIALS AND METHODS Microorganism. A fungus strain, P. sordida YK-624 (22) (ATCC 90872), isolated from a forest (15) was used for MnP preparation. The fungus was maintained on a potato dextrose agar (Difco Laboratories) slant. Production and preparation of MnP. Strain YK-624 was grown on potato dextrose agar in petri plates (diameter, 9 cm) for 3 days at 30C. The contents of one-quarter of each plate, homogenized in a liquid culture medium with a Waring blender, were inoculated into a 500-ml Erlenmeyer flask containing 200 ml of culture medium. One liter of this medium contained 10 g of glucose, 0.22 g of ammonium tartrate, 1.64 g of sodium acetate, 1.0 g of Tween 80, and Kirk s trace elements and salts (45); the ph was adjusted to 4.5. The flasks were shaken at 30C and 150 rpm. After 0.25 g of veratryl alcohol was added to the medium in each flask on day 3, the flasks were purged with oxygen every day. After 7 days of incubation, the supernatant was separated from the mycelium by filtration through glass fiber filters. The filtrate was dialyzed against sodium acetate buffer (20 mm; ph 4.5) overnight. Polyethylene glycol (average molecular weight, 3,000) was added to the filtrate to make a 5% solution for the removal of polysaccharide slime. The ph was then adjusted to 7.2 with 5 M aqueous NaOH. After the slime was filtered off with filter paper and a membrane filter (cellulose nitrate; pore size, 0.45 m), the filtrate was subjected to anion-exchange chromatography (DEAE-Sepharose CL-6B; Pharmacia), as previously reported (22). The fraction containing MnP activity was used for pulp treatments. Enzyme assays. MnP activity was assayed by monitoring the oxidation of 2,6-dimethoxyphenol at 470 nm. The mixtures contained 2,6-dimethoxyphenol (1.0 mm), H 2 O 2 (0.2 mm), and MnSO 4 (1.0 mm) in 50 mm malonate buffer (ph 4.5). The enzyme assay was performed with a 3-ml reaction mixture at 37C. MnP activity was expressed as the amount of spectral change (change in absorbance per minute). The assay was also used to measure the activity of MnP remaining in the solution and absorbed onto the pulp during bleaching of the pulp with MnP. After pulp treatments, pulp suspensions were filtered. The pulp was added to the above reaction mixture, and the oxidation of 2,6-dimethoxyphenol was monitored. The dry weight of the pulp used for the assay was measured after the reaction. MnP activity was expressed as the amount of change in absorbance per minute and per gram of pulp. To evaluate the effect of organic acids on the oxidation of 2,6-dimethoxyphenol by MnP, 50 mm succinate buffer (ph 4.5) was used in the assay instead of malonate buffer. Glucose oxidase activity was determined by the peroxidase-coupled production of hydrogen peroxide in the presence of glucose (43). The glucose oxidase activity was expressed in units (micromoles of H 2 O 2 produced per minute). Pulp treatments. An unbleached hardwood kraft pulp (brightness, 31.0%; kappa number, 16.7) produced in an industrial pulp mill was used in this study. Manganese content in the pulp was determined by ashing the pulp at 600 to 700C, washing the sample with 0.1 N nitric acid, and analyzing the sample in an inductively coupled plasma mass spectrometer (ICP-MS model PMS 2000; Yokogawa Denki, Yokogawa, Japan). This pulp contained 30.0 mg of manganese per kg. The pulp was suspended at a consistency of 1% (1 g/100 ml) in 50 mm malonate buffer (ph 4.5) or 50 mm succinate buffer (ph 4.5) containing 0.05% Tween 80 and 100 U of MnP. The suspension was stirred at 30C. The enzymatic reaction was started and maintained by continuously adding H 2 O 2 at a flow rate of 3 ml/h with a peristaltic pump. The reaction of glucose and glucose oxidase (from Aspergillus niger [Wako Pure Chemicals Industries, Ltd.]) was also used to supply H 2 O 2 continuously to the pulp suspension. The suspension contained 0.5 g of kraft pulp, 50 U of MnP, 0.05% Tween 80, 25 mm glucose and 0 to 0.5 U of glucose oxidase in 50 ml of 50 mm succinate buffer (ph 4.5) in a 100-ml Erlenmeyer flask. The flasks were shaken at 150 rpm and 30C after they were purged with oxygen for about 30 min. All experiments were reproducible. Pulp properties. After the enzyme bleaching, pulp was washed with distilled water. Pulp sheet preparation and determination of pulp brightness and kappa number were conducted as described in a previous paper (22). Measurement of manganese dioxide reduction. The reaction mixtures (50 ml) contained 5 mm MnO 2 (powder and Japan Industrial Standards [JIS] first grade; Wako Pure Chemicals) in oxalate, malonate, or gluconate buffer (50 mm, ph 4.5) and were stirred at 30C in air. Reduction of MnO 2 was measured by monitoring the appearance of the Mn 3 complex. The absorptivities of Mn 3 complexes were directly measured: ε and ε mm 1 cm 1 were used for the determination of Mn 3 -oxalate and Mn 3 -malonate, respectively (51); ε mm 1 cm 1 was used for the determination of Mn 3 - gluconate. RESULTS The effect of the addition of MnSO 4 on bleaching of kraft pulp with MnP in the presence of various organic acids was examined by changing the concentration of aqueous H 2 O 2 FIG. 1. Effect of addition of MnSO 4 on the brightness of kraft pulp treated with MnP with the continuous addition of various concentrations of aqueous H 2 O 2 at 3 ml/h for 24 h. Symbols: F, no MnSO 4 ; E, 0.1 mm MnSO 4 added. added. The pulp was treated with MnP, adding 1, 3, 5, and 10 mm aqueous H 2 O 2 for 24 h (Fig. 1). In 50 mm malonate buffer, an increase in brightness was observed with the addition of MnSO 4 but not without additional MnSO 4. When the pulp was treated with the continuous addition of 3 and 5 mm aqueous H 2 O 2 in the presence of 2 mm oxalate, the brightness increased by about 13 points without the addition of MnSO 4. An increase in brightness was observed in the presence of 2 mm gluconate without the addition of MnSO 4, although it was less than that in oxalate. Brightening was also observed in 50 mm succinate buffer without the addition of MnSO 4 in the pulp treatment in which H 2 O 2 was supplied by glucose and glucose oxidase (Fig. 2), because gluconate was produced by glucose oxidase. Figure 3 shows changes in residual MnP activity during bleaching of kraft pulp with MnP in the presence of each organic acid with or without the addition of MnSO 4.Inthe presence of 50 mm malonate or 2 mm oxalate, higher MnP activity remained during the treatment with the addition of MnSO 4 than during that without the addition of MnSO 4. Especially in 50 mm malonate buffer, when MnSO 4 was not added to the pulp suspension, residual MnP activity in the reaction mixture decreased rapidly and disappeared after 12 h. Enzyme activities during pulp treatments with and without MnSO 4 were similar to each other in the experiments in which mixtures were buffered with gluconate or succinate. Changes in residual MnP activity and pulp brightness as a function of time during bleaching with MnP without the addition of MnSO 4 and in the presence of organic acids are shown in Fig. 4. The low MnP amounts adsorbed onto the pulp were detected early in treatment. The brightness increased progressively in the presence of oxalate, and the rate of the decrease in MnP activity was lower than that in the presence of other organic acids. Unbleached hardwood kraft pulp used in this study contained FIG. 2. Effect of glucose oxidase activity on the brightness of kraft pulp treated with MnP without the addition of MnSO 4 in 50 mm succinate buffer (ph 4.5) for 24 h.
3 VOL. 62, 1996 BLEACHING OF HARDWOOD KRAFT PULP WITH MnP 915 FIG. 3. Change in residual MnP activity as a function of time during the bleaching of kraft pulp with MnP. Aqueous H 2 O 2, 5 mm, was added at a rate of 3 ml/h for 24 h. Symbols: F, no MnSO 4 ; E, 0.1 mm MnSO 4 added mg of manganese per kg. After treatment with MnP without exogenous manganese in the presence of 2 mm oxalate, the pulp contained 2.3 mg of manganese per kg. The decrease in manganese content suggests that MnP uses manganese originally present in the pulp, resulting in brightening. When the oxidation of 2,6-dimethoxyphenol by MnP was measured with various concentrations of MnSO 4 in the presence of 2 mm oxalate or gluconate in 50 mm succinate buffer (ph 4.5), MnP activity in 2 mm oxalate was better than that in 2 mm gluconate and 50 mm succinate (Fig. 5). This result suggested that oxalate was a good chelator for supporting phenol oxidation by MnP. Oxalate was capable of reducing MnO 2 rapidly and complexed with Mn 3, whereas malonate and gluconate reduced MnO 2 slowly (Fig. 6). It could be that oxalate reduces MnO 2 which either existed in the pulp or was formed from Mn 2 by oxidation with MnP. It can be concluded that the presence of oxalate, which is a good Mn 3 chelator and MnO 2 reducing agent, supports the bleaching of the kraft pulp with MnP by the effective use of manganese originally present in the pulp. DISCUSSION It has been shown that MnP plays an important role in the bleaching of unbleached hardwood kraft pulp by white rot fungi (15, 17, 19, 23, 33). Although the manganese ion which is necessary for the MnP catalytic system is present in the kraft pulp (14, 16, 33), the pulp was not substantially brightened unless MnSO 4 was added during in vitro bleaching with MnP in 50 mm malonate buffer (ph 4.5), as previously reported (22). The oxidation of Mn 2 by MnP is dependent on the presence of organic acids produced by the fungus. It has been reported that oxalate stimulates MnP optimally from P. chrysosporium at low physiological concentrations while optimal activity is observed at higher concentrations of malonate and lactate (21, 24). Roy et al. also showed that gluconate and cellobionate produced by glucose oxidase and cellobiose:quinone oxidoreductase (CBQase) both worked very well as Mn-complexing agents at lower concentrations (10 mm) in phenol red oxidation (40). The present study indicates that MnP bleaching of kraft pulp can be performed without the addition of MnSO 4 if we use oxalate, which can also reduce insoluble MnO 2.Inthe presence of malonate, a good Mn 3 chelator, the pulp brightness was not increased remarkably without the addition of MnSO 4 (Fig. 1), and a rapid decrease of residual MnP activity during bleaching of pulp with MnP was observed (Fig. 3). If there is a shortage of a reductive substrate such as Mn 2 for MnP, compounds I and II accumulate, and H 2 O 2 is not consumed and also accumulates. Thus, excess H 2 O 2 may lead to inactivation of MnP via compound III (48). Roy et al. proposed a model of in vivo cooperativity between MnP and CBQase from T. versicolor since CBQase catalyzes the reduction of insoluble MnO 2 to soluble Mn 2 and Mn 3 while generating an Mn 3 -complexing sugar acid, cellobionic acid (40). An increase in brightness was observed when pulp was treated with MnP with the continuous addition of 1 mm aqueous H 2 O 2 in the presence of 0.1 mm MnSO 4 2 mm oxalate (Fig. 1). Kuan and Tien reported that oxalate can support the oxidation of phenol red by MnP in the absence of exogenous H 2 O 2 and in the presence of dioxygen, and a lag period is observed (25). They suspected that H 2 O 2 is possibly formed from the autoxidation of oxalate since a low equivalent concentration of added H 2 O 2 can eliminate the lag period, resulting in the immediate oxidation of phenol red. Khindaria et al. also reported the mechanism of oxalate-dependent reductive activity of MnP and concluded that both CO 2 (anaerobic conditions) and O 2 (aerobic conditions) could reduce the ferric ion in reaction mixtures containing MnP, Mn 2, oxalate, H 2 O 2, ferric chloride, and 1,10-phenanthroline while the dismutation of some O 2 would produce H 2 O 2 to provide a constant supply of H 2 O 2 (20). Those reactions may be involved in the bleaching of kraft pulp with MnP in the presence of oxalate, and H 2 O 2 is probably supplied to the MnP catalytic system, resulting in brightening of the pulp. Kraft pulps vary greatly in manganese content (33). It has been shown that Mn 3 formed by MnP is reduced back to Mn 2 by oxalate (20, 42, 44). Bleaching of the pulp with MnP without the addition of MnSO 4 was inhibited by the addition of 10 mm oxalate (data not shown). The inhibition of bleaching with MnP by oxalate disappeared when 0.1 mm MnSO 4 was added. If oxalate also plays a major role in biobleaching by white rot fungi, it may be considered that the production of oxalate must be controlled at lower concentra- FIG. 4. Changes in residual MnP activity and pulp brightness as a function of time during the bleaching of kraft pulp with MnP without the addition of MnSO 4. Aqueous H 2 O 2, 5 mm, was added at a rate of 3 ml/h for 24 h. Symbols: E, MnP activity in solution; Ç, MnP activity sorbed on pulp;, pulp brightness.
4 916 HARAZONO ET AL. APPL. ENVIRON. MICROBIOL. or allow omission of the EDTA treatment step during the subsequent hydrogen peroxide bleaching stage. ACKNOWLEDGMENT Manganese was measured with an ICP-MS model PMS 2000 mass spectrometer at the Center of Advanced Instrumental Analysis, Kyushu University, Fukuoka, Japan. FIG. 5. Effect of organic acids on MnP activity in the presence of various concentrations of MnSO 4. Symbols: F, 50 mm succinate buffer; å, 2 mm oxalate in 50 mm succinate buffer;, 2 mm gluconate in 50 mm succinate buffer. tions in the presence of low concentrations of Mn 2 during biobleaching by fungi. Mn 3 generated by MnP has been thought to oxidize phenolic sites but not nonphenolic sites in lignin. However, there are a few reports that the MnP system oxidizes the nonphenolic substructures of lignin under mild conditions. Hammel et al. reported that low concentrations of Mn 3 suffice to oxidize nonphenolic lignin models at physiological temperatures and ph values (12). Popp and Kirk proposed the mechanism for Mn 3 oxidation of the neutral dienyl radical derived from the cation radical of 1,2,4,5-tetramethoxybenzene (36). Recently, Bao et al. indicated that nonphenolic lignin was oxidized by a lipid peroxidation system that consisted of MnP, Mn 2, and unsaturated fatty acid esters present in Tween 80 (3). We showed that the use of Tween 80 or the combination of an unsaturated fatty acid and Tween 20 improved the brightness of the pulp after bleaching with MnP compared with the use of Tween 20 only (13). We used a culture filtrate containing MnP secreted from P. sordida YK-624 to delignify and bleach oxygen-bleached hardwood kraft pulp for the establishment of a totally chlorine-free bleaching process (46). The pulp was brightened to 91% brightness by a combination of MnP treatment (two times) and hydrogen peroxide treatment. The physical properties of the nonchlorine-bleached pulp were almost the same as those of a pulp bleached with chlorine-based chemicals. The addition of hydrogen peroxide bleaching was needed after treatment with MnP. The metals in pulp should be controlled by using chelating agents, e.g., EDTA, prior to hydrogen peroxide bleaching. Minimizing the use of such substances may be desirable since the environmental effects of chelating agents are unclear. Since manganese content in the pulp decreases by bleaching with MnP without the addition of MnSO 4, the use of oxalate during bleaching with MnP will reduce the amount of EDTA FIG. 6. Change in Mn 3 complex produced by reduction of insoluble MnO 2 by organic acids as a function of time. Symbols: F, Mn 3 -oxalate at 500 nm; å, Mn 3 -malonate at 270 nm;, Mn 3 -gluconate at 300 nm. REFERENCES 1. Addleman, K., and F. 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Totally chlorine-free bleaching process with the introduction of enzyme treatment with crude enzymes secreted from Phanerochaete sordida YK-624. Jpn. TAPPI (Tech. Assoc. Pulp Paper Ind.) J., in press. 47. Tuor, U., H. Wariishi, H. E. Schoemaker, and M. H. Gold Oxidation of phenolic arylglycerol -aryl ether lignin model compounds by manganese peroxidase from Phanerochaete chrysosporium: oxidative cleavage of an -carbonyl model compound. Biochemistry 31: Wariishi, H., L. Akileswaran, and M. H. Gold Manganese peroxidase from the basidiomycete Phanerochaete chrysosporium: spectral characterization of the oxidized states and the catalytic cycle. Biochemistry 27: Wariishi, H., K. Valli, and M. H. Gold Oxidative cleavage of a phenolic diarylpropane lignin model dimer by manganese peroxidase from Phanerochaete chrysosporium. Biochemistry 28: Wariishi, H., K. Valli, and M. H. Gold In vitro depolymerization of lignin by manganese peroxidase of Phanerochaete chrysosporium. Biochem. Biophys. Res. 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