NC State
BioResources
An, Q., Zhou, Z.-G. Wang, Y.-H., Guo, S., Chen, Z., Yuan, Y.-N., Sun, X.-Q., Yang, Y.-L., Zhang, T.-X., and Han, M-L. (2023). “Laccase produced by Coriolopsis trogii and Cerrena unicolor with the mixed of metal ions and lignocellulosic materials,” BioResources 18(2), 3895-3908.

Abstract

Coriolopsis trogii and Cerrena unicolor were investigated for laccase production in submerged fermentation with different nutrient medium containing metal ions and lignocellulosic materials. The maximum laccase activity of C. trogii Han751 was 8584.44 ± 98.45 U/L and was obtained from nutrient medium 7. However, the maximum laccase activity of C. unicolor Han 849 was 16144.26 ± 635.30 U/L from nutrient medium 9. Thus, the capacity of secreting laccase of C. unicolor Han 849 was superior to that of C. trogii Han751. Different fungal species have different medium components suitable for laccase production. The content of CuSO4·5H2O and MnSO4 in nutrient medium with the concentration of 0.25 g/L and 0.151 g/L, respectively, was more beneficial to C. trogii Han751 secreting laccase. However, the vital components of nutrient medium that contribute to the laccase activity of C. unicolor Han 849 were corncob, glucose, and CuSO4·5H2O, with the corresponding concentrations of 1 g/flask, 5 g/L, and 0.25 g/L, respectively. The results will contribute to the development of new methods to produce low-cost laccase.


Download PDF

Full Article

Laccase Produced by Coriolopsis trogii and Cerrena unicolor with the Mixed of Metal Ions and Lignocellulosic Materials

Qi An,a,b Zhi-Guo Zhou,a,b Yu-Hua Wang,a Sa Guo,a Zhe Chen,a Yun-Na Yuan,a Xiao-Qing Sun,a Yu-Lu Yang,a Tian-Xin Zhang,a and Mei-Ling Han a,b,c,*

Coriolopsis trogii and Cerrena unicolor were investigated for laccase production in submerged fermentation with different nutrient medium containing metal ions and lignocellulosic materials. The maximum laccase activity of C. trogii Han751 was 8584.44 ± 98.45 U/L and was obtained from nutrient medium 7. However, the maximum laccase activity of C. unicolor Han 849 was 16144.26 ± 635.30 U/L from nutrient medium 9. Thus, the capacity of secreting laccase of C. unicolor Han 849 was superior to that of C. trogii Han751. Different fungal species have different medium components suitable for laccase production. The content of CuSO4·5H2O and MnSO4 in nutrient medium with the concentration of 0.25 g/L and 0.151 g/L, respectively, was more beneficial to C. trogii Han751 secreting laccase. However, the vital components of nutrient medium that contribute to the laccase activity of C. unicolor Han 849 were corncob, glucose, and CuSO4·5H2O, with the corresponding concentrations of 1 g/flask, 5 g/L, and 0.25 g/L, respectively. The results will contribute to the development of new methods to produce low-cost laccase.

DOI: 10.15376/biores.18.2.3895-3908

Keywords: Coriolopsis trogii; Cerrena unicolor; Laccase; Populus beijingensis; Corncob; Metal ions

Contact information: a: College of Life Science, Langfang Normal University, Langfang 065000, Hebei, China; b: Technical Innovation Center for Utilization of Edible and Medicinal Fungi in Hebei Province, Langfang 065000, Hebei, China; c: Edible and Medicinal Fungi Research and Development Center of Universities/Colleges in Hebei Province, Langfang 065000, Hebei, China;

* Corresponding author: meilinghan309@163.com

INTRODUCTION

There is a great need for enzymes for use in biodegradation and biochemical processes (Kremer et al. 2015; Rao et al. 2019; Han et al. 2021b, 2022). Laccase (EC 1.10.3.2), belonging to the blue copper oxidase family; it oxidizes a wide range of phenols and aromatic amines, such as monophenol, diphenol, polyphenol, aminophenol, and methoxyphenol (Gupta and Jana 2019). Laccase was first discovered by Yoshida (1883) in lacquer trees (Rhus vernicifera). Supporting studies that identified fungal extracellular secretions as laccase were carried out by Bertrand (1896) and Laborde (1896). Laccase has been found in higher plants, insects, fungi, and bacteria (Geng et al. 2018; Unuofin et al. 2019b; An et al. 2021a, 2021b; Khatami et al. 2022). Due to the specificity of low substrate and high catalytic efficiency, laccases have broad application prospects in bio-pulping, biocatalysis, bioremediation, biopolymers, food and beverage processing, biosensor, lignin degradation, nanobiotechnology, and organic synthesis (Upadhyay et al. 2016; Bertrand et al. 2017; Hadibarata et al. 2018; Yashas et al. 2018; Navas et al. 2019; Singh and Arya 2019; Unuofin et al. 2019a; Zerva et al. 2019; Khatami et al. 2022; Zhang et al. 2022).

Because of the huge application potential of laccase, the search for environmentally friendly and economically feasible compounds to stimulate laccase production has been extensive (Chenthamarakshan et al. 2017). The wide use of inexpensive raw materials (industrial and lignocellulosic wastes) containing cellulose, hemicellulose, and lignin to produce laccase can be an economical approach (Leite et al. 2019). When lignocellulosic materials are used as nutrients, solid-state fermentation (SSF) is usually adopted. Solid-state fermentation imitates the environment where white-rot fungi grow in nature, and lignocellulosic materials can be used as the substrates for white-rot fungi (WRF) to attach to facilitate their growth (Jaramillo et al. 2017). However, solid-state fermentation does not take advantage of industrial production, mainly because it is inconvenient to operate. Therefore, submerged fermentation (SF) is still the main way of industrial production of laccase. Research on WRF laccase production has focused on continuous soaking fermentation using soluble nutrients in complex and synthetic culture medium.

Metal ions, fungal species, particle size of lignocellulosic materials, pH, and temperature all affect the ability of fungi to produce laccase (Atila et al. 2017; Kostadinova et al. 2018; Gaikwad and Meshram 2019; Jasinska et al. 2019; Lallawmsanga et al. 2019; Sun et al. 2021). Along with the in-depth study of the existing laccase-producing strains, many researchers are also working on the discovery of new laccase-producing fungi (Myasoedova et al. 2017; Yadav and Vivekanand 2019). Coriolopsis trogii and Cerrena unicolor are the model white-rot fungi that produce extracellular enzymes, including laccase. Previous studies have shown that these two fungi have excellent ability of secreting laccase (Han et al. 2021b; Qiu and Liu 2022). The appropriate concentration of metal ions (e.g., Cd2+, Cu2+ and Mn2+) can promote the production of laccase by white-rot fungi, such as Flammulina velutipes, Phlebia radiata, and Pleurotus ostreatus. (Baldrian and Gabriel 2002; Liu et al. 2009; Mäkela et al. 2013; Janusz et al. 2015; An et al. 2016, 2020; Zhou et al. 2017). The laccase activities of Pleurotus ostreatus and Flammulina velutipes induced by different metal ions were analyzed by An et al. (2020), and the results showed that single copper ion or manganese ion could enhance the laccase activities secreted by P. ostreatus and F. velutipes. Some types and high concentration of metal ions (e.g., Fe2+ and Hg2+) which act as an inducer can also inhibit fungal laccase activity (Lorenzo et al. 2005; Juarez-Gomez et al. 2018; Xu et al. 2018; Li et al. 2022). Other studies have analyzed the laccase activity of Coriolopsis trogii and Cerrena unicolor on lignocellulosic materials, such as Populus beijingensis, rice straw, cottonseed hull, and corncob (Han et al. 2021b, 2022, 2023; Liu et al. 2022). The content of lignin, hemicellulose and cellulose of hardwood stems and corncobs was 18-25%, 24-40%, 40-55% and 15%, 35%, 45% (Howard et al. 2003; Sanchez 2009). The effects of mixed metal ions, such as Fe2+ and Cu2+, on the activity of fungal laccase have been reported (Zhuo et al. 2017a,b; An et al. 2020). Xu et al. (2020) investigated the growth, quality, and ligninolytic enzymes activities of Lentinula edodes when fermented on mixed lignocellulosic biomass. Han et al. (2021b) analyzed the laccase activity secreted by Cerrena unicolor on the mixture of Pinus tabuliformis and Firmiana platanifolia. However, there are few studies on laccase production by fungi stimulated by mixed conditions of lignocellulosic materials and metal ions. This study examined the laccase activity of Cerrena unicolor and Coriolopsis trogii under the mixed condition of metal ions and lignocellulosic materials. The results will contribute to developing new low-cost methods to produce laccase.

EXPERIMENTAL

Materials

Microorganisms

Coriolopsis trogii Han751 and Cerrena unicolor Han 849 were collected from Maojingba National Nature Reserve (Longhua County, Chengde City, Hebei Province, China) and Wulingshan National Nature Reserve (Xinglong County, Chengde City, Hebei Province, China). These two fungi strains were maintained on malt extract agar (MEA) medium (g/L: glucose 10, malt extract 20, KH2PO4 3, and agar 20), and stored at 4 ℃.

Chemicals

2,2’-Azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) was purchased from Sigma-Aldrich (Sigma Aldrich (Shanghai) Trading Co., LTD). Malt extract, yeast extract, and peptone were purchased from AOBOX (BEIJING AOBOXING BIO-TECH CO., LTD). Other chemicals used in present work were purchased from Tianjin Zhiyuan Chemical Reagent Co. Ltd. (Tianjin, China).

Lignocellulosic biomass

Corncob was kindly provided by farmers in Chengde city, Hebei province (China), and Populus beijingensis was obtained from Langfang city, Hebei province (China). All lignocellulosic biomass was air-dried, then ground by a micro plant grinding machine with the practical size between 20- and 60-mesh.

Methods

Microbial culture

Coriolopsis trogii Han751 and Cerrena unicolor Han 849 were isolated from the natural habitat and stored in College of Life Science, Langfang Normal University. All of these fungal strains were cultured on CYM (g/L: glucose 20, peptone 2, yeast extract 2, MgSO4·7H2O 0.5, K2HPO4·3H2O 1, KH2PO4 0.46, and agar 15) to perform the activation process of fungi at 26 ℃ for 7 days. Five inoculants with a diameter of 1.0 cm were picked with a round punch tool and inoculated into liquid CYM medium (100 mL) in triangular flask (250 mL). Then, all flasks were transferred to a shaker and cultured at 150 rpm to obtain fungal seed liquid at 26 ℃.

Inoculum preparation

After 7 days, the preparation of the inoculum was obtained by breaking up the mycelium pellets in the triangular flask with a homogenizer at 5000 rpm for 90 s.

Process of submerged fermentation

Triangular flasks (250 mL) containing nutrient medium for inducing laccase production (Table 1) were autoclaved at 121 ℃ for 30 min. After cooling to room temperature, 3 mL of homogenized inoculum was added to each flask. All flasks were transferred to a rotary shaker to perform the submerged fermentation process with the speed of 150 rpm at 26 ℃. The crude enzyme was filtered through a filter paper, then centrifuged at 12000 rpm for 20 min with the temperature of 4 °C.

Table 1. Description of the Nutrient Medium

Laccase activity assay

Laccase activity was determined by monitoring the oxidation of 2,2’-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS) to ABTS-azine at 415 nm (Ɛ415 = 3.16 × 104 M-1 cm-1). One unit of laccase activity was defined as the amount of laccase required to oxidize 1.0 µmol of ABTS per minute.

Statistical analysis

All experiments were performed in triplicate. The values were expressed as mean ± standard deviation. In colored graphs, standard deviation was represented as error bars. The graphs were generated by the Origin 2016 (OriginLab Corporation, Northampton, MA, USA). Data were subjected to two-way analysis of variance (ANOVA) by SPSS 22.0 (PROC GLM, Armonk, NY, USA).

RESULTS AND DISCUSSION

Effect of Nutrient Medium on Laccase Activity Secreted by Coriolopsis trogii Han751

The laccase secretion capacity of Coriolopsis trogii had been demonstrated in previous studies (Yan et al. 2014; Campos et al. 2016; An et al. 2021b; Han et al. 2022; Liu et al. 2022; Qiu and Liu 2022). Previous studies examined laccase activity in solid or submerged fermentation with lignocellulosic materials. As a complex carbon/nitrogen source and energy source for the growth of white rot fungi, lignocellulosic materials are excellent materials for the production of low-cost laccase (Nawaz et al. 2019; Wang et al. 2019). In addition, metal ions can induce white rot fungi to produce laccase. Thus, the effect of the mixture of metal ions and lignocellulosic materials on laccase activity secreted by C. trogii Han751 was analyzed. The results are shown in Fig. 1 and Table 2.

Comparative analysis of laccase activity from Coriolopsis trogii Han 751 in submerged fermentation with lignocellulosic biomass showed that the maximum value of laccase activity was 55.35 ± 0.76 U/L, 134.72 ± 3.55 U/L, 72.03 ± 3.06 U/L, and 80.97 ± 2.53 U/L when in Sorghum straw, Populus beijingensis, Toona sinensis, and Salix babylonica submerged fermentation (An et al. 2021b). Han et al. (2022) analyzed the laccase activity of species belonging to the genus of Coriolopsis fermented on different lignocellulosic wastes, and maximum laccase activity of Coriolopsis trogii Han 1211 was 223.03 ± 11.51 U/L, 118.24 ± 3.48 U/L, 151.50 ± 3.32 U/L, and 75.85 ± 3.62 U/L on cottonseed hull, rice straw, corncob, and Populus beijingensis, respectively. Liu et al. (2022) investigated the laccase activities of Coriolopsis trogii Han 751 on solid-state fermentation, and maximum laccase activity of Coriolopsis trogii Han 751 on stalk of Helianthus annuus (SOHA), stalk of Sorghum bicolor (SOSB), Pinus tabuliformis, Populus beijingensis, cottonseed hull, and corncob was 122.26 ± 4.57 U/L, 799.03 ± 40.89 U/L, 13.96 ± 0.46 U/L, 18.59 ± 0.92 U/L, 16.58 ± 0 U/L, and 90.92 ± 4.01 U/L. The laccase activity of C. trogii Han751 in different nutrient media is shown in Table 2 and Fig. 1.

Fig. 1. Laccase activity of Coriolopsis trogii Han751 fermented in nutrient medium

Obviously, the laccase activity of C. trogii Han 751 fermented with NM7 (containing corncob 1 g/flask, Populus beijingensis 2 g/flask, glucose 20 g/L, yeast extract 4 g/L, sucrose 5 g/L, CuSO4·5H2O 0.25 g/L, MnSO4 0.151 g/L, and peptone 4 g/L) was 3167.69-fold, 32.16-fold, 3.16-fold, 860.16-fold, 547.83-fold, 1113.42-fold, 1369.13-fold, 29.74-fold, 2189.91-fold, 1524.77-fold, and 2.02-fold. In addition, the maximum laccase activity of C. trogii Han 751 under NM3 and NM12 culture conditions was also greater than 2700 U/L (Fig. 1). In conclusion, the content of CuSO4·5H2O and MnSO4 in nutrient medium of 0.25g/L and 0.151g/L, respectively, was more beneficial to C. trogii Han 751 secreting laccase.

Table 2. Maximum Laccase Activity and Occurrence Time of Coriolopsis trogii Han 751 and Cerrena unicolor Han 849 in Nutrient Medium Submerged Fermentation

Effect of Nutrient Medium on Laccase Activity Secreted by Cerrena unicolor Han 849

Previous studies had indicated excellent laccase secretion ability of Cerrena unicolor (Jamroz et al. 2004; Rola et al. 2013; Kachlishvili et al. 2014, 2021; Pawlik et al. 2021; Zhang et al. 2021). There are also many studies on the effect of lignocellulose materials on laccase activity from C. unicolor. The study of metal ions on laccase activity of C. unicolor mainly focused on the tolerance of purified laccase to metal ions. Under these conditions, the effect of mixing metal ions and lignocellulosic materials on the activity of laccase secreted by C. unicolor Han 849 were examined in the present work.

Han et al. (2021a) detected the laccase activity of C. unicolor Han 849 on different lignocellulosic residues and maximum laccase activity was 295.96 ± 4.85 U/L on Populus beijingensis, 625.98 ± 24.08 U/L on Firmiana platanifolia, 371.71 ± 5.69 U/L on Sorghum bicolor, and 102.17 ± 3.55 U/L on Oryza sativa. Another, Han et al. (2021b) also found that mixing lignocellulosic materials could be increased the activity of laccase secreted by the white rot fungus C. unicolor Han 849, and the laccase activity in submerged fermentation with Pinus tabuliformis, Firmiana platanifolia, and the mixture of Pinus tabuliformis and Firmiana platanifolia was 223.53 ± 21.06 U/L, 552.34 ± 49.14 U/L, and 876.23 ± 20.82 U/L. However, laccase activity of C. unicolor Han 849 in submerged fermentation with NM 1, NM 2, NM 3, NM 4, NM 5, NM 6, NM 7, NM 8, NM 9, NM 10, NM 11, and NM 12 was 377.74 ± 10.85 U/L, 582.48 ± 15.89 U/L, 12517.58 ± 488.15 U/L, 1366.28 ± 114.10 U/L, 754.17 ± 88.87 U/L, 1185.45 ± 69.60 U/L, 2822.99 ± 75.85 U/L, 7.03 ± 0.17 U/L, 16144.26 ± 635.30 U/L, 8.04 ± 0.46 U/L, 34.06 ± 2.17 U/L, and 5686.16 ± 453.42 U/L, respectively (Fig. 2, Table 2). Obviously, nutrient medium of NM 9 and NM 3 were more beneficial to increase laccase activity of C. unicolor, followed by NM 12 and NM 7. In this study, the laccase activity of C. unicolor Han 849 in nutrient medium of NM9 and NM3 conditions was much higher than that of C. unicolor in previous studies.

Fig. 2. Laccase activity of Cerrena unicolor Han 849 fermented in Nutrient Medium

Comparative Analyze of Coriolopsis trogii Han751 and Cerrena unicolor Han 849 on Laccase Activity

White-rot fungi, famous for their laccase secreting ability, are widely studied. Meanwhile, the ability of secreting laccase from different species was commonly significant (Elisashvili et al. 2008; An et al. 2021a; Han et al. 2021a). Similarly, laccase activities could be significantly affected by fungal species and nutrient medium (P < 0.001).

Maximum laccase activities of Cerrena unicolor Han 849 in submerged fermentation of NM 1, NM 2, NM 3, NM 4, NM 5, NM 6, NM 8, NM 9, NM 10, NM 11, and NM 12 was nearly 139.39-fold, 2.18-fold, 4.61-fold, 136.90-fold, 48.13-fold, 153.75-fold, 1.12-fold, 55.93-fold, 2.05-fold, 6.05-fold, and 1.34-fold higher than that of Coriolopsis trogii Han751 in corresponding nutrient medium, while maximum laccase activities of C. trogii Han751 in NM 7 submerged fermentation was nearly 3.04-fold higher than that of C. unicolor Han 849. On the whole, the ability of secreting laccase of C. unicolor Han 849 was superior to that of C. trogii Han751. Maximum laccase activities of Trametes trogii and T. versicolor on solid-state fermentation with Corylus maxima were 384 U/L and 68 U/L (Birhanli and Yesilada 2013). Gupta and Jana (2019) analyzed the laccase activity of Ganoderma lucidum fermented in repeated batch semi-solid fermentation (sSF) process with wheat straw and the optimized highest laccase activity in batch sSF was 15257.2 ± 353.4UL on the 9th day. Previous work (Lorenzo et al. 2002) investigated the optimized production of laccase by T. versicolor in submerged cultures with the lignocellulosic residues, and the highest activity was 639 U/L with barely bran. Laccase activity obtained in barley bran submerged cultures of T. versicolor mixed with Mn2+ (1 mM) or Cu2+ (2 mM) was 938 U/L or 6342 U/L (Lorenzo et al. 2006). Obviously, it can be found that the maximum laccase activity of C. trogii Han751 and C. unicolor Han 849 in the present study under the condition of nutrient medium 7 (8584.44 ± 98.45 U/L) and nutrient medium 9 (16144.26 ± 635.30 U/L) was higher than the results of some previous studies. However, the maximum laccase activity detected in present study was lower than that from T. trogii S0301 (352.09 U/L) after the laccase purification process (ammonium sulfate precipitation, anionic exchange chromatography, and Sephadex G-75 chromatography) (Yan et al. 2014).

CONCLUSIONS

  1. Overall, the laccase secretion capacity of Cerrena unicolor Han 849 in submerged fermentation with nutrient medium was superior to that of Coriolopsis trogii Han751.
  2. Maximum laccase activity of Coriolopsis trogii Han751 obtained from nutrient medium 7 was 8584.44 ± 98.45 U/L, while the maximum laccase activity of Cerrena unicolor Han 849 was 16144.26 ± 635.30 U/L from nutrient medium 9.
  3. The content of CuSO4·5H2O and MnSO4 in nutrient medium of 0.25g/L and 0.151g/L, respectively, was more beneficial to Coriolopsis trogii Han751 secreting laccase.
  4. The vital components of nutrient medium that contribute to the laccase activity of Cerrena unicolor Han 849 were corncob, glucose, and CuSO4·5H2O, and corresponding content was 1 g/flask, 5 g/L, and 0.25 g/L.

ACKNOWLEDGMENTS

This research was supported by the National Natural Science Foundation of China (31900009), the Science and Technology Project of Hebei Education Department (BJK2022052), the Fundamental Research Funds for the Universities in Hebei Province (JYQ202201), and the Top-notch Youth Project of Langfang City, China.

REFERENCES CITED

An, Q., Han, M. L., Bian, L. S., Han, Z. C., Han, N., Xiao, Y. F., and Zhang, F. B. (2020). “Enhanced laccase activity of white rot fungi induced by different metal ions under submerged fermentation,” BioResources 15(4), 8369-8383. DOI: 10.15376/biores.15.4.8369-8383

An, Q., Han, M. L., Wu, X. J., Si, J., Cui, B. K., Dai, Y. C., and Wu, B. (2016). “Laccase production among medicinal mushrooms from the Genus Flammulina (Agaricomycetes) under different treatments in submerged fermentation,” International Journal of Medicinal Mushrooms 18(11), 1049-1059. DOI: 10.1615/IntJMedMushrooms.v18.i11.90

An, Q., Li, C. S., Yang, J., Chen, S. Y., Ma, K. Y., Wu, Z. Y., Bian, L. S., and Han, M. L. (2021a). “Evaluation of laccase production by two white-rot fungi using solid-state fermentation with different agricultural and forestry residues,” BioResources 16(3), 5287-5300. DOI: 10.15376/biores.16.3.5287-5300

An, Q., Shi, W. Y., He, Y. X., Hao, W. Y., Ma, K. Y., Chen, X., Yan, X. Y., Bian, L. S., Li, C. S., and Han, M. L. (2021b). “Evaluation of the capacity of laccase secretion of four novel isolated white-rot fungal strains in submerged fermentation with lignocellulosic biomass,” BioResources 16(4), 6706-6722. DOI: 10.15376/biores.16.4. 6706-6722

Atila, F., Tuzel, Y., Cano, A. F., and Fernandez, J. A. (2017). “Effect of different lignocellulosic wastes on Hericium americanum yield and nutritional characteristics,” Journal of the Science of Food and Agriculture 97(2), 606-612. DOI: 10.1002/jsfa.7772

Baldrian, P., and Gabriel, J. (2002). “Copper and cadmium increase laccase activity in Pleurotus ostreatus,” FEMS Microbiology Letters 206(1), 69-74. DOI: 10.1111/j.1574-6968.2002.tb10988.x

Bertrand, B., Martinez-Morales, F., and Trejo-Hernandez, M. R. (2017). “Upgrading laccase production and biochemical properties: Strategies and challenges,” Biotechnology Progress 33(4), 1015-1034. DOI: 10.1002/btpr.2482

Bertrand, G. (1896). “Sur la presence simultanee de la laccase et de la tyrosinase dans le sue de quelques champignons,” C. R. Hebd. Seances Acad. Sci. 123, 463-465.

Birhanli, E., and Yesilada, O. (2013). “The utilization of lignocellulosic wastes for laccase production under semisolid-state and submerged fermentation conditions,” Turkish Journal of Biology 37(4), 450-456. DOI: 10.3906/biy-1211-25

Campos, P. A., Levin, L. N., and Wirth, S. A. (2016). “Heterologous production, characterization and dye decolorization ability of a novel thermostable laccase isoenzyme from Trametes trogii BAFC 463,” Process Biochemistry 51(7), 895-903. DOI: 10.1016/j.procbio.2016.03.015

Chenthamarakshan, A., Parambayil, N., Miziriya, N., Soumya, P. S., Lakshmi, M. S. K., Ramgopal, A., Dileep, A., and Nambisan, P. (2017). “Optimization of laccase production from Marasmiellus palmivorus LA1 by Taguchi method of design of experiments,” BMC Biotechnol. 17, Article Number 12. DOI: 10.1186/s12896-017-0333-x

Elisashvili, V., Penninckx, M., Kachlishvili, E., Tsiklauri, N., Metreveli, E., Kharziani, T., and Kvesitadze, G. (2008). “Lentinus edodes and Pleurotus species lignocellulolytic enzymes activity in submerged and solid-state fermentation of lignocellulosic wastes of different composition,” Bioresource Technology 99(3), 457-462. DOI: 10.1016/j.biortech.2007.01.011

Gaikwad, A., and Meshram, A. (2019). “Effect of particle size and mixing on the laccase-mediated pretreatment of lignocellulosic biomass for enhanced saccharification of cellulose,” Chemical Engineering Communications 207(12), 1696-1706. DOI: 10.1080/00986445.2019.1680364

Geng, A., Wu, J., Xie, R. R., Li, X., Chang, F. X., and Sun, J. Z. (2018). “Characterization of a laccase from a wood-feeding termite, Coptotermes formosanus,” Insect Science 25(2), 251-258. DOI: 10.1111/1744-7917.12415

Gupta, A., and Jana, A. K. (2019). “Production of laccase by repeated batch semi-solid fermentation using wheat straw as substrate and support for fungal growth,” Bioprocess and Biosystems Engineering 42(3), 499-512. DOI: 10.1007/s00449-018-2053-6

Hadibarata, T., Syafiuddin, A., Al-Dhabaan, F. A., Elshikh, M. S., and Rubiyatno. (2018). “Biodegradation of Mordant orange-1 using newly isolated strain Trichoderma harzianum RY44 and its metabolite appraisal,” Bioprocess and Biosystems Engineering 41(5), 621-632. DOI: 10.1007/s00449-018-1897-0

Han, M. L., An, Q., Ma, K. Y., An, W. N., Hao, W. Y., Liu, M. Y., Shi, W. Y., Yang, J., and Bian, L. S. (2021a). “A comparative study on the laccase activity of four Basi-diomycete fungi with different lignocellulosic residues via solid-state fermentation,” BioResources 16(2), 3017-3031. DOI: 10.15376/biores.16.2.3017-3031

Han, M. L., Yang, J., Liu, Z. Y., Wang, C. R., Chen, S. Y., Han, N., Hao, W. Y., An, Q., and Dai, Y. C. (2021b). “Evaluation of laccase activities by three newly isolated fungal species in submerged fermentation with single or mixed lignocellulosic wastes,” Frontiers in Microbiology 12, article 682679. DOI: 10.3389/fmicb.2021.682679

Han, M. L., Yang, J., Ma, J. J., Wang, C. R., Chen, S. Y., Xu, M. X., Yang, Q. Y., Bian, L. S., Yan, X. Y., and An, Q. (2022). “Extracellular laccase activity among Ganoderma and Coriolopsis species grown on lignocellulosic wastes,” BioResources 17(3), 5049-5064. DOI: 10.15376/biores.17.3.5049-5064

Han, M. L., Lin, L., Guo, X. X., An, M., Geng, Y. J., Xin, C., Ma, L. C., Mi, Q., Ping, A. Q., Yang, Q. Y., Zhang, T. X., and An, Q. (2023). “Comparative analysis of the laccase secretion ability of five white-rot fungi in submerged fermentation with lignocellulosic biomass,” BioResources 18(1), 584-598. DOI: 10.15376/biores.18.1. 584-598

Howard, R. L., Abotsi, E., Jansen van Rensburg, E. L., and Howard S. (2003). “Lignocellulose biotechnology: Issues of bioconversion and enzyme production,” African Journal of Biotechnology (12), 602-619.

Jamroz, T., Sencio, B., Ledakowicz, S., and Tarkiewicz, A. (2004). “Optimisation of laccase biosynthesis by Cerrena unicolor,” Chemical and Process Engineering-Inzynieria Chemiczna I Procesowa 25(3), 1017-1022.

Janusz, G., Czuryło, A., Frąc, M., Rola, B., Sulej, J., Pawlik, A., Siwulski, M., and Rogalski, J. (2015). “Laccase production and metabolic diversity among Flammulina velutipes strains,” World Journal of Microbiology and Biotechnology 31(1), 121-133. DOI: 10.1007/s11274-014-1769-y

Jaramillo, A. C., Cobas, M., Hormaza, A., and Sanroman, M. Á. (2017). “Degradation of adsorbed azo dye by solid-state fermentation: Improvement of culture conditions, a kinetic study, and rotating drum bioreactor performance,” Water, Air, & Soil Pollution 228(6), 1-14. DOI: 10.1007/s11270-017-3389-2

Jasinska, A., Goralczyk-Binkowska, A., Sobon, A., and Dlugonski, J. (2019). “Lignocellulose resources for the Myrothecium roridum laccase production and their integrated application for dyes removal,” International Journal of Environmental Science and Technology 16(8), 4811-4822. DOI: 10.1007/s13762-019-02290-x

Juarez-Gomez, J., Rosas-Tate, E. S., Roa-Morales, G., Balderas-Hernandez, P., Romero-Romo, M., and Ramirez-Silva, M. T. (2018). “Laccase inhibition by mercury: kinetics, inhibition mechanism, and preliminary application in the spectrophotometric quantification of mercury ions,” Journal of Chemistry 2018, article 7462697. DOI: 10.1155/2018/7462697

Kachlishvili, E., Jokharidze, T., Kobakhidze, A., and Elisashvili, V. (2021). “Enhancement of laccase production by Cerrena unicolor through fungal interspecies interaction and optimum conditions determination,” Archives of Microbiology 203(7), 3905-3917. DOI: 10.1007/s00203-021-02374-8

Kachlishvili, E., Metreveli, E., and Elisashvili, V. (2014). “Modulation of Cerrena unicolor laccase and manganese peroxidase production,” SpringerPlus 3, article 463. DOI: 10.1186/2193-1801-3-463

Khatami, S. H., Vakili, O., Movahedpour, A., Ghesmati, Z., Ghasemi, H., and Taheri-Anganeh, M. (2022). “Laccase: Various types and applications,” Biotechnology and Applied Biochemistry (in press). DOI: 10.1002/bab.2313

Kostadinova, N., Krumova, E., Boeva, R., Abrashev, R., Miteva-Staleva, J., Spassova, B., and Angelova, M. (2018). “Effect of copper ions on the ligninolytic enzyme complex and the antioxidant enzyme activity in the white-rot fungus Trametes trogii 46,” Plant Biosystems 152(5), 1128-1133. DOI: 10.1080/11263504.2017.1418450

Kremer, F., Blank, L. M., Jones, P. R., and Akhtar, M. K. (2015). “A comparison of the microbial production and combustion characteristics of three alcohol biofuels: Ethanol, 1-butanol, and 1-octanol.” Frontiers in Bioengineering and Biotechnology 3, article 112. DOI: 10.3389/fbioe.2015.00112

Laborde, J. (1896). “Sur la casse des vins,” C. R. Hebd. Seances Acad. Sci. 123, 1074-1075.

Lallawmsanga, Leo, V. V., Passari, A. K., Muniraj, I. K., Uthandi, S., Hashem, A., Abd Allah, E. F., Alqarawi, A. A., and Singh, B. P. (2019). “Elevated levels of laccase synthesis by Pleurotus pulmonarius BPSM10 and its potential as a dye decolorizing agent,” Saudi Journal of Biological Sciences 26(3), 464-468. DOI: 10.1016/j.sjbs.2018.10.006

Leite, P., Silva, C., Salgado, J. M., and Belo, I. (2019). “Simultaneous production of lignocellulolytic enzymes and extraction of antioxidant compounds by solid-state fermentation of agro-industrial wastes,” Industrial Crops and Products 137, 315-322. DOI: 10.1016/j.indcrop.2019.04.044

Li, S. Y., Liu, Q. Z., Liu, J., Sun, K., Yang, W., Si, Y. B., Li, Y. C., and Gao, Y. Z. (2022). “Inhibition mechanisms of Fe2+/Fe3+ and Mn2+ on fungal laccase-enabled bisphenol a polyreaction,” Chemosphere 307(1), article 135685. DOI: 10.1016/j.chemosphere.2022.135685

Liu, L. H., Lin, Z. W., Zheng, T., Lin, L., Zheng, C. Q., Lin, Z. X., Wang, S. H., and Wang, Z. H. (2009). “Fermentation optimization and characterization of the laccase from Pleurotus ostreatus strain 10969,” Enzyme and Microbial Technology 44(6-7), 426-433. DOI: 10.1016/j.enzmictec.2009.02.008

Liu, W. X., Zhao, M. Y., Li, M. X., Li, X. Q., Zhang, T. X., Chen, X., Yan, X. Y., Bian, L. S., An, Q., Li, W. J., et al. (2022). “Laccase activities from three white-rot fungal species isolated from their native habitat in north China using solid-state fermentation with lignocellulosic biomass,” BioResources 17(1), 1533-1550. DOI: 10.15376/biores.17.1.1533-1550

Lorenzo, M., Moldes, D., Couto, S. R., and Sanroman, A. (2002). “Improving laccase production by employing different lignocellulosic wastes in submerged cultures of Trametes versicolor,” Bioresource Technology 82(2), 109-113. DOI: 10.1016/S0960-8524(01)00176-6

Lorenzo, M., Moldes, D., Couto, S. R., and Sanroman, A. (2005). “Inhibition of laccase activity from Trametes versicolor by heavy metals and organic compounds,” Chemosphere 60(8), 1124-1128. DOI: 10.1016/j.chemosphere.2004.12.051

Lorenzo, M., Moldes, D., and Sanroman, M. A. (2006). “Effect of heavy metals on the production of several laccase isoenzymes by Trametes versicolor and on their ability to decolourise dyes,” Chemosphere 63(6), 912-917. DOI: 10.1016/j.chemosphere.2005.09.046

Mäkela, M. R., Lundell, T., Hatakka, A., and Hildén, K. (2013). “Effect of copper, nutrient nitrogen, and wood-supplement on the production of lignin-modifying enzymes by the white-rot fungus Phlebia radiata,” Fungal Biology 117(1), 62-70. DOI: 10.1016/j.funbio.2012.11.006

Myasoedova, N. M., Renfeld, Z. V., Podieiablonskaia, E. V., Samoilova, A. S., Chernykh, A. M., Classen, T., Pietruszka, J., Kolomytseva, M. P., and Golovleva, L. A. (2017). “Novel laccase-producing Ascomycetes,” Microbiology 86(4), 503-511. DOI: 10.1134/S0026261717030110

Navas, L. E., Martínez, F. D., Taverna, M. E., Fetherolf, M. M., Eltis, L. D., Nicolau, V., Estenoz, D., Campos, E., Benintende, G. B., and Berretta, M. F. (2019). “A thermostable laccase from Thermus sp. 2.9 and its potential for delignification of Eucalyptus biomass,” AMB Express 9, 1-10. DOI: 10.1186/s13568-019-0748-y

Nawaz, A., Mukhtar, H., ul Haq, I., Mazhar, Z., and Mumtaz, M. W. (2019). “Laccase: an environmental benign pretreatment agent for efficient bioconversion of lignocellulosic residues to bioethanol,” Current Organic Chemistry 23(14), 1517-1526. DOI: 10.2174/1385272823666190722163046

Pawlik, A., Ciolek, B., Sulej, J., Mazur, A., Grela, P., Staszczak, M., Niscior, M., Jaszek, M., Matuszewska, A., Janusz, G., and Paszczynski, A. (2021). “Cerrena unicolor laccases, genes expression and regulation of activity,” Biomolecules 11(3), article 468. DOI: 10.3390/biom11030468

Qiu, W. H., and Liu, J. R. (2022). “Fermenting and lignin degradability of a white-rot fungus Coriolopsis trogii using industrial lignin as substrate,” Applied Biochemistry and Biotechnology 194(11), 5220-5235. DOI: 10.1007/s12010-022-04004-5

Rao, A., Ramakrishna, N., Arunachalam, S., and Sathiavelu, M. (2019). “Isolation, screening and optimization of laccase-producing endophytic fungi from Euphorbia milii,” Arabian Journal for Science and Engineering 44(1), 51-64. DOI: 10.1007/s13369-018-3431-8

Rola, B., Mazur, I., Dawidowicz, A., and Rogalski, J. (2013). “The Cerrena unicolor laccase overproduction on waste agricultural based media,” FEBS Journal 280, 614-614.

Sanchez, C. (2009). “Lignocellulosic residues: Biodegradation and bioconversion by fungi,” Biotechnology Advances 27(2), 185-194. DOI: 10.1016/j.biotechadv.2008.11.001

Singh, G., and Arya, S. K. (2019). “Utility of laccase in pulp and paper industry: A progressive step towards the green technology,” International Journal of Biological Macromolecules 134, 1070-1084. DOI: 10.1016/j.ijbiomac.2019.05.168

Sun, Y., Liu, Z. L., Hu, B. Y., Chen, Q. J., Yang, A. Z., Wang, Q. Y., Li, X. F., Zhang, J. Y., Zhang, G. Q., and Zhao, Y. C. (2021). “Purification and characterization of a thermo- and pH-stable laccase from the litter-decomposing fungus Gymnopus luxurians and laccase mediator systems for dye decolorization,” Frontiers in Microbiology 12, article 672620. DOI: 10.3389/fmicb.2021.672620

Wang, F., Xu, L., Zhao, L. T., Ding, Z. Y., Ma, H. L., and Terry, N. (2019). “Fungal laccase production from lignocellulosic agricultural wastes by solid-state fermentation: A review,” Microorganisms 7(12), article 665. DOI: 10.3390/microorganisms7120665

Xu, S., Wang, F., Fu, Y. P., Li, D., Sun, X. Z., Li, C. T., Song, B., and Li, Y. (2020). “Effects of mixed agro-residues (corn crop waste) on lignin-degrading enzyme activities, growth, and quality of Lentinula edodes,” RSC Advances 10(17), 9798-9807. DOI: 10.1039/c9ra10405d

Xu, X. Q., Huang, X. H., Liu, D., Lin, J., Ye, X. Y., and Yang, J. (2018). “Inhibition of metal ions on Cerrena sp laccase: Kinetic, decolorization and fluorescence studies,” Journal of the Taiwan Institute of Chemical Engineers 84, 1-10. DOI: 10.1016/j.jtice.2017.12.028

Unuofin, J. O., Okoh, A. I., and Nwodo, U. U. (2019a). “Aptitude of oxidative enzymes for treatment of wastewater pollutants: a laccase perspective,” Molecules 24(11), 1-36. DOI: 10.3390/molecules24112064

Unuofin, J. O., Okoh, A. I., and Nwodo, U. U. (2019b). “Utilization of agroindustrial wastes for the production of laccase by Achromobacter xylosoxidans HWN16 and Bordetella bronchiseptica HSO16,” Journal of Environmental Management 231, 222-231. DOI: 10.1016/j.jenvman.2018.10.016

Upadhyay, P., Shrivastava, R., and Agrawal, P. K. (2016). “Bioprospecting and biotechnological applications of fungal laccase,” 3 Biotech 6, article 15. DOI: 10.1007/s13205-015-0316-3

Yadav, M., and Vivekanand, V. (2019). “Chaetomium globosporum: A novel laccase producing fungus for improving the hydrolyzability of lignocellulosic biomass,” Heliyon 5(3), article 01353. DOI: 10.1016/j.heliyon.2019.e01353

Yan, J. P., Chen, D. D., Yang, E., Niu, J. Z., Chen, Y. H., and Chagan, I. (2014). “Purification and characterization of a thermotolerant laccase isoform in Trametes trogii strain and its potential in dye decolorization,” International Biodeterioration & Biodegradation 93, 186-194. DOI: 10.1016/j.ibiod.2014.06.001

Yashas, S. R., Shivakumara, B. P., Udayashankara, T. H., and Krishna, B. M. (2018). “Laccase biosensor: Green technique for quantification of phenols in wastewater (a review),” Oriental Journal of Chemistry 34(2), 631-637. DOI: 10.13005/ojc/340204

Yoshida, H. (1883). “LXIII. – Chemistry of lacquer (Urushi). Part I. Communication from the chemical society of Tokio,” Journal of the Chemical Society, Transactions 43, 472-486. DOI: 10.1039/CT8834300472

Zerva, A., Simić, S., Topakas, E., and Nikodinovic-Runic, J. (2019). “Applications of microbial laccases: Patent review of the past decade (2009-2019),” Catalysts 9(12), 1-26. DOI: 10.3390/catal9121023

Zhang, S. T., Dong, Z. J., Shi, J., Yang, C. R., Fang, Y., Chen, G., Chen, H., and Tian, C. J. (2022). “Enzymatic hydrolysis of corn stover lignin by laccase, lignin peroxidase, and manganese peroxidase,” Bioresource Technology 361, article 127699. DOI: 10.1016/j.biortech.2022.127699

Zhang, Z. C., Shah, A. M., Mohamed, H., Zhang, Y., Tsiklauri, N., and Song, Y. D. (2021). “Genomic studies of white-rot fungus Cerrena unicolor SP02 provide insights into food safety value-added utilization of non-food lignocellulosic biomass,” Journal of Fungi 7(10), article 835. DOI: 10.3390/jof7100835

Zhou, C. X., Dong, A. X., Wang, Q., Yu, Y. Y., Fan, X. R., Cao, Y. L., and Li, T. J. (2017a). “Effect of common metal ions and anions on laccase catalysis of guaiacol and lignocellulosic fiber,” BioResources 12(3), 5102-5117. DOI: 10.15376/biores.12.3.5102-5117

Zhuo, R., Yuan, P., Yang, Y., Zhang, S., Ma, F. Y., and Zhang, X. Y. (2017b). “Induction of laccase by metal ions and aromatic compounds in Pleurotus ostreatus HAUCC 162 and decolorization of different synthetic dyes by the extracellular laccase,” Biochemical Engineering Journal 117, 62-72. DOI: 10.1016/j.bej.2016.09.016

Article submitted: January 30, 2023; Peer review completed: March 11, 2023; Revised version received and accepted: April 12, 2023; Published: April 19, 2023.

DOI: 10.15376/biores.18.2.3895-3908