Acessibilidade / Reportar erro

Testing for the ability to modify antibiotics of Panus tigrinus 8/18 Lentinus strigosus 1566 laccase

Teste de capacidade para modificar antibióticos a partir da lacase de Panus tigrinus 8/18 e Lentinus strigosus 1566

Abstract

In advanced biotechnology, the utilization of enzymes to achieve new or modified compounds with antibacterial, fungicidal, and anti-cancer specifications is crucial. Mushroom lactases are a hopeful biocatalyst for the synthesis and modification of different compounds. They are an accessible and inexpensive enzyme for the preparation of reaction objects and have recently received attention. Laccase purification was performed from basidiomycete Lentinus strigosus (LS) in several stages: Stage 1. On ion-exchange chromatography on TEAE Servacell 23 (400 ml), two distinctly separated laccase activity peaks were observed, eluted from the carrier at 0.21 and 0.27 M NaCl. In order to reduce the loss of enzymes, all fractions with laccase activity were collected, concentrated, and desalted using an ultrafiltration cell (Amicon, United States) with a UM-10 membrane. Stage 2. The resulting preparation with laccase activity was applied to a Q-Sepharose column (60 ml). Two well-separated peaks with laccase activity were obtained during the elution: laccase I (0.12 M NaCl) and laccase II (0.2 M NaCl). Stage 3. In the course of further purification of both enzymes, carried out on anion-exchange carrier Resource Q (6 ml), a broken gradient was used: 0 - 10%, 10 - 20%, and 20 - 100% with 1M NaCl. Stage 4. Both laccase I and laccase II, obtained after Resource Q, were desalted, concentrated to 1 ml each, and applied to a Superdex 75 gel filtration column. As a result, two laccases were obtained in a homogeneous form.

Keywords:
laccase; basidiomycetes; enzymes; microorganisms; antibiotics

Resumo

Na biotecnologia moderna, o uso de enzimas para obter compostos novos ou modificados com propriedades antibacterianas, antifúngicas e anticancerígenas é crucial. Lactases de cogumelos são biocatalisadores promissores para síntese e modificação de diferentes compostos, por serem enzimas baratas e disponíveis para a preparação de componentes de reação, e vem recebendo a devida atenção recentemente. A purificação da lacase foi realizada a partir do basidiomiceto Lentinus strigosus em vários estágios: Etapa 1 - na cromatografia de troca iônica em TEAE Servacell 23 (400 ml), foram observados dois picos de atividade da lacase distintamente separados, com eluição do transportador a 0,21 e 0,27 M de NaCl. Para reduzir a perda de enzimas, todas as frações com atividade de lacase foram coletadas, concentradas e dessalinizadas em uma célula de ultrafiltração (Amicon, Estados Unidos) com membrana UM-10; Etapa 2 - a preparação resultante com atividade de lacase foi aplicada a uma coluna Q-Sepharose (60 ml). Durante a eluição, foram obtidos dois picos bem separados com atividade de lacase: lacase I (NaCl 0,12 M) e lacase II (NaCl 0,2 M); Etapa 3 - no decurso da purificação adicional de ambas as enzimas, realizada no Recurso Q de transportador de troca aniônica (6 ml), um gradiente quebrado foi usado: 0-10%, 10-20% e 20-100% com NaCl 1M; Etapa 4 - tanto a lacase I como a lacase II, obtidas após o Recurso Q, foram dessalinizadas e concentradas para 1 ml cada e aplicadas a uma coluna de filtração em gel Superdex 75. Como resultado, duas lacases foram obtidas de forma homogênea.

Palavras-chave:
lacases; basidiomicetos; enzimas; microorganismos; antibióticos

1. Introduction

Usage of enzymes to produce new compounds or modify antibacterial compounds is important (Zengin et al., 2018ZENGIN, M., GENC, H., TASLIMI, P., KESTANE, A., GUCLU, E., OGUTLU, A., KARABAY, O. and GULCIN, I., 2018. Novel thymol bearing oxypropanolamine derivatives as potent some metabolic enzyme inhibitors: their antidiabetic, anticholinergic and antibacterial potentials. Bioorganic Chemistry, vol. 81, pp. 119-126. http://dx.doi.org/10.1016/j.bioorg.2018.08.003. PMid:30118983.
http://dx.doi.org/10.1016/j.bioorg.2018....
; Saleem et al., 2020SALEEM, A., BUKHARI, S.M., ZAIDI, A., FAROOQ, U., ALI, M., KHAN, A., KHAN, S., SHAH, K.H., MAHMOOD, A. and KHAN, F.A., 2020. Enzyme inhibition and antibacterial potential of 4-Hydroxycoumarin derivatives. Brazilian Journal of Pharmaceutical Sciences, vol. 56, pp. e18654.http://dx.doi.org/10.1590/s2175-97902019000418654.
http://dx.doi.org/10.1590/s2175-97902019...
; Zhao et al., 2020ZHAO, S., XIAO, C., WANG, J., TIAN, K., JI, W., YANG, T., KHAN, B., QIAN, G., YAN, W. and YE, Y., 2020. Discovery of natural FabH inhibitors using an immobilized enzyme column and their antibacterial activity against Xanthomonas oryzae pv. oryzae. Journal of Agricultural and Food Chemistry, vol. 68, no. 48, pp. 14204-14211. http://dx.doi.org/10.1021/acs.jafc.0c06363. PMid:33201689.
http://dx.doi.org/10.1021/acs.jafc.0c063...
; Tukenova et al., 2021TUKENOVA, Z., MUSTAFAYEV, M., ALIMZHANOVA, M., AKYLBEKOVA, T. and ASHIMULY, K., 2021. Influence of pesticides on the biological activity of light chestnut soils in South-East Kazakhstan. Journal of Water and Land Development, no. 48, pp. 141-147.). Fungal laccases are an inexpensive and readily accessible enzyme for earning reaction components. They have recently been considered as an important biocatalyst for the synthesis and reformation of diverse compounds. In addition, this enzyme has an extensive range of attacked substrates, a wealthy arsenal of catalyzed reactions, and great sustainability (Ferraroni et al., 2007FERRARONI, M., MYASOEDOVA, N.M., SCHMATCHENKO, V., LEONTIEVSKY, A.A., GOLOVLEVA, L.A., SCOZZAFAVA, A. and BRIGANTI, F., 2007. Crystal structure of a blue laccase from Lentinus tigrinus: evidences for intermediates in the molecular oxygen reductive splitting by multicopper oxidases. BMC Structural Biology, vol. 7, no. 1, pp. 60. http://dx.doi.org/10.1186/1472-6807-7-60. PMid:17897461.
http://dx.doi.org/10.1186/1472-6807-7-60...
). In modern biotechnology, researchers are interested in using laccases with the possibility of biodegradation under mild conditions. Mild conditions are conditions that have three conditions, which are: (i) low temperatures, (ii) under relative zero pressure, and (iii) without the usage of toxic solvents. However, we see the feasibility of a one-stage reaction to earn the needed compounds using laccases as biocatalysts to be particularly relevant (Myasoedova et al., 2008MYASOEDOVA, N.M., CHERNYKH, A.M., PSURTSEVA, N.V., BELOVA, N.V. and GOLOVLEVA, L.A., 2008. New efficient producers of fungal laccases. Applied Biochemistry and Microbiology, vol. 44, no. 1, pp. 73-77. http://dx.doi.org/10.1134/S0003683808010122.
http://dx.doi.org/10.1134/S0003683808010...
; Kolomytseva et al., 2019KOLOMYTSEVA, M.P., MYASOEDOVA, N.M., CHERNYKH, A.M., GAIDINA, A.S., SHEBANOVA, A.D., BASKUNOV, B.P., ASCHENBRENNER, J., ROSENGARTEN, J.F., RENFELD, Z.V., GASANOV, N.B., PINCHUK, I.P., CLASSEN, T., PIETRUSZKA, J. and GOLOVLEVA, L.A., 2019. Laccase isoform diversity in basidiomycete Lentinus strigosus 1566: potential for phenylpropanoid polymerization. International Journal of Biological Macromolecules, vol. 137, pp. 1199-1210. http://dx.doi.org/10.1016/j.ijbiomac.2019.07.056. PMid:31295487.
http://dx.doi.org/10.1016/j.ijbiomac.201...
).

Laccases are able to polymerize the primary molecules through C-C, C-O, C-S, C-N crosslinks and form di-, tri-, and polymer products. Also, laccases can oxidize various molecules containing phenolic rings with the formation of oxidized products (Williamson, 1994WILLIAMSON, P.R., 1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. Journal of Bacteriology, vol. 176, no. 3, pp. 656-664. http://dx.doi.org/10.1128/jb.176.3.656-664.1994. PMid:8300520.
http://dx.doi.org/10.1128/jb.176.3.656-6...
; Myasoedova et al., 2015MYASOEDOVA, N.M., GASANOV, N.B., CHERNYKH, A.M., KOLOMYTSEVA, M.P. and GOLOVLEVA, L.A., 2015. Selective regulation of laccase isoform production by the Lentinus strigosus 1566 fungus. Applied Biochemistry and Microbiology, vol. 51, no. 2, pp. 222-229. http://dx.doi.org/10.1134/S0003683815020131. PMid:26027358.
http://dx.doi.org/10.1134/S0003683815020...
).

Laccase (EC 1.10.3.2, p-diphenol: oxygen oxidoreductase), a copper-containing blue oxidase found in plants, fungi, and bacteria, catalyzes one-electron oxidation of a wide range of substrates, mainly phenols and aromatic amines, reducing oxygen to water (Thurston, 1994THURSTON, C.F., 1994. The structure and function of fungal laccases. Microbiology, vol. 140, no. 1, pp. 19-26. http://dx.doi.org/10.1099/13500872-140-1-19.
http://dx.doi.org/10.1099/13500872-140-1...
; Burke and Cairney, 2002BURKE, R. and CAIRNEY, J., 2002. Laccases and other polyphenol oxidases in ecto-and ericoid mycorrhizal fungi. Mycorrhiza, vol. 12, no. 3, pp. 105-116. http://dx.doi.org/10.1007/s00572-002-0162-0. PMid:12072980.
http://dx.doi.org/10.1007/s00572-002-016...
; Bains et al., 2003BAINS, J., CAPALASH, N. and SHARMA, P., 2003. Laccase from a non-melanogenic, alkalotolerant γ-proteobacterium JB isolated from industrial wastewater drained soil. Biotechnology Letters, vol. 25, no. 14, pp. 1155-1159. http://dx.doi.org/10.1023/A:1024569722413. PMid:12967004.
http://dx.doi.org/10.1023/A:102456972241...
; Alcalde, 2007ALCALDE, M., 2007. Laccases: biological functions, molecular structure and industrial applications. In: J. Polaina and A.P. MacCabe, eds. Industrial enzymes. Dordrecht: Springer, pp. 461–476. http://dx.doi.org/10.1007/1-4020-5377-0_26.
http://dx.doi.org/10.1007/1-4020-5377-0_...
; Madhavi and Lele, 2009MADHAVI, V. and LELE, S.S., 2009. Laccase: properties and applications. BioResources, vol. 4, no. 4, pp. 1694-1717.; Babu et al., 2012BABU, P.R., PINNAMANENI, R. and KOONA, S., 2012. Occurrences, physical and biochemical properties of laccase. Universal Journal of Environmental Research and Technology, vol. 2, no. 1, pp. 1-13.).

Considering the broad substrate specificity, ease of use, and stability, fungal laccases serve as enzymatic catalysts in the transformation of antibiotics (Rave et al., 2019RAVE, A.F.G., KUSS, A.V., PEIL, G.H.S., LADEIRA, S.R., VILLARREAL, J.P.V. and NASCENTE, P.S., 2019. Biochemical identification techniques and antibiotic susceptibility profile of lipolytic ambiental bacteria from effluents. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 79, no. 4, pp. 555-565. http://dx.doi.org/10.1590/1519-6984.05616. PMid:30484476.
http://dx.doi.org/10.1590/1519-6984.0561...
; Guardado et al., 2019GUARDADO, A.L.P., BELLEVILLE, M. and ALANIS, M., 2019. Effect of redox mediators in pharmaceuticals degradation by laccase: a comparative study. Process Biochemistry, vol. 78, pp. 123-131. http://dx.doi.org/10.1016/j.procbio.2018.12.032.
http://dx.doi.org/10.1016/j.procbio.2018...
; Navada and Kulal, 2019NAVADA, K.K. and KULAL, A., 2019. Enzymatic degradation of chloramphenicol by laccase from Trametes hirsuta and comparison among mediators. International Biodeterioration & Biodegradation, vol. 138, pp. 63-69. http://dx.doi.org/10.1016/j.ibiod.2018.12.012.
http://dx.doi.org/10.1016/j.ibiod.2018.1...
; Aldayel et al., 2021ALDAYEL, F.M., ALSOBEG, M.S. and KHALIFA, A., 2021. In vitro antibacterial activities of silver nanoparticles synthesised using the seed extracts of three varieties of Phoenix dactylifera. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, pp. e242301. PMid:34346959.). The objective of the research was to study the possibility of using fungal laccases to modify famous antibiotics to earn their analogs with new features.

2. Methodology

The main objects of the article were laccases of basidiomycetes of “white rot” Panus tigrinus 8/18 and Lentinus strigosus (LS) 1566. The fungi were grown by submerged cultivation. Laccase activity was determined spectrophotometrically by the rate of ABTS oxidation (2,2-Azino-bis (3-ethylbenzothiazoline 6-sulfonic acid), ε436 = 29300 M-1cm-1 at 436 nm on a UV-160 spectrophotometer (Shimadzu, Japan).

The enzymes were purified from the culture liquid of fungi collected at the peak of laccase activity using ion-exchange chromatography on TEAE Servacell 23 (400 ml). We determined the mass of the enzyme subunit using SDS-PAGE electrophoresis (Andlar et al., 2018ANDLAR, M., REZIĆ, T., MARĐETKO, N., KRACHER, D., LUDWIG, R. and ŠANTEK, B., 2018. Lignocellulose degradation: an overview of fungi and fungal enzymes involved in lignocellulose degradation. Engineering in Life Sciences, vol. 18, no. 11, pp. 768-778. http://dx.doi.org/10.1002/elsc.201800039. PMid:32624871.
http://dx.doi.org/10.1002/elsc.201800039...
; Yesilada et al., 2018YESILADA, O., BIRHANLI, E. and GECKIL, H., 2018. Bioremediation and decolorization of textile dyes by white rot fungi and laccase enzymes. In: R. Prasad, ed. Mycoremediation and environmental sustainability mycoremediation and environmental sustainability. Cham: Springer, vol. 2, pp. 121–153. http://dx.doi.org/10.1007/978-3-319-77386-5_5.
http://dx.doi.org/10.1007/978-3-319-7738...
). Antibiotic modification products were identified using thin layer chromatography and spectrophotometry (Li et al., 2018LI, Q., YU, X., YANG, Y. and LIU, X., 2018. Simple determination of diacylglycerols using thin layer chromatography and visible spectrophotometry. Food Analytical Methods, vol. 11, no. 1, pp. 236-242. http://dx.doi.org/10.1007/s12161-017-0993-0.
http://dx.doi.org/10.1007/s12161-017-099...
).

3. Results and Discussion

The study of the dynamics of laccase activity showed that laccase reached its maximum activity in the fungus P. tigrinus 8/18 on the 5th day and amounted to 50 ME/ml, while the fungus LS 1566 had a higher level of biosynthesis of this enzyme (250 ME/ml) and the peak of activity shifted on the 3rd day of cultivation (Figure 1).

Figure 1
Dynamics of laccase activity of fungi P. tigrinus 8/18 and LS F-1566.

As shown in Figure 1, the laccase activity of LS F-1566 is significantly higher than that of P. tigrinus 8/18. Therefore, for further work, we used LS F-1566 culture liquid. At the stage of ion-exchange chromatography on TEAE Servacell 23 (400 ml), two peaks of laccase activity were observed, eluted from the support at 0.21 and 0.27 M NaCl (see Figure 2).

Figure 2
Elution of laccase activity from the column «ТЕАЕ servacell 23».

The data on the elution peaks of laccase activity shows that there are two isoforms of laccase: laccase I and laccase II. The study with SDS electrophoresis showed that both laccases are monomers with molecular weights of 62 and 60 kDa (laccase I and laccase II, respectively) (Figure 3). In further studies, the dominant isoform – -laccase I – was selected.

Figure 3
SDS electrophoresis (12% PAGE gel) of pure preparations of laccase I (1) and laccase II (2), isolated from the fungus LS 1566.3 - marker proteins.

The resulting enzymatic provision of LS 1566 laccase was experimented for its capability to correct the precursors of antibiotics of various classes (penicillin, cephalosporin, tetracycline, imidazole, and erythramycin).

As can be seen in Figure 4, our experiments showed a modification of the antibiotic of the penicillin series. Formation of new compounds with Rf - 0.18; 0.15; 0.11; 0.07, absent in all control variants, was observed in the reaction mixture using 6-APA, hydroquinone, and laccase preparation.

Figure 4
Thin-layer chromatogram of the tested compounds (1-2) and compounds obtained in experiments with the addition of laccase (3-5). 1 - 6-APA; 2 - hydroquinone; 3- hydroquinone + laccase; 4 - 6-APA + laccase; 5 - 6-APA + hydroquinone laccase.

The study of the spectral features of the 6-APA correction found that the reactions of antibiotic correction with laccase do not proceed without adding hydroquinone (Morsi et al., 2020MORSI, R., BILAL, M., IQBAL, H.M. and ASHRAF, S.S., 2020. Laccases and peroxidases: the smart, greener and futuristic biocatalytic tools to mitigate recalcitrant emerging pollutants. The Science of the Total Environment, vol. 714, pp. 136572. http://dx.doi.org/10.1016/j.scitotenv.2020.136572. PMid:31986384.
http://dx.doi.org/10.1016/j.scitotenv.20...
). When this enzyme is added to a mixture of hydroquinone and 6-APA, new peaks are formed in the absorption region of 250 nm. Given that hydroquinone is a good bed for laccase, in the reaction, it can act as an activator of the formation of new transformation products of the antibiotic 6-APA (see Figure 5).

Figure 5
Dynamics of 6-APA correction upon its reaction with hydroquinone under the action of LS 1566 laccase for 2 hr.

Mikolasch and Schauer (2009)MIKOLASCH, A. and SCHAUER, F., 2009. Fungal laccases as tools for the synthesis of new hybrid molecules and biomaterials. Applied Microbiology and Biotechnology, vol. 82, no. 4, pp. 605-624. http://dx.doi.org/10.1007/s00253-009-1869-z. PMid:19183983.
http://dx.doi.org/10.1007/s00253-009-186...
, in their studies, showed the possibility of modifying antibiotics of a number of penicillins using the laccase Trametes Versicolor. The products formed were homo- and heteromolecular compounds of the original antibiotic. In our case, investigation the spectral specifications of the interaction of 6-APA with the LS 1566 laccase for 2 hours, no new compounds are created, as no spectrum changes occur. Nevertheless, we observe a remarkable variation in the spectrum of the reaction of the interaction of 6-APA with hydroquinone under the action of LS 1566 laccase for 2 hours. This may indicate the formation of heteromolecular compounds of the antibiotic.

To increase the efficiency of the 6-APA modification process, we have optimized the conditions of this reaction. A significant formation of new products was observed already after 60 minutes of incubation; a further increase in the reaction time did not lead to the formation of new compounds, but the accumulation of already formed products took place. A change in the absorption spectrum is observed at 250 nm after 30 min of incubation (see Figure 6).

Figure 6
Reaction spectra of 6-APC modification: A - without the use of a mediator (60 minutes of incubation); B - using the mediator 4-hydroxy-TEMPO (15 min incubation).

One factor that makes it possible to expand the bed specificity of laccases is the use of mediators. The mediator is oxidized by laccase to a stable radical, which is an oxidizing agent of the substrate (Wang et al., 2018WANG, X., YAO, B. and SU, X., 2018. Linking enzymatic oxidative degradation of lignin to organics detoxification. International Journal of Molecular Sciences, vol. 19, no. 11, pp. 3373. http://dx.doi.org/10.3390/ijms19113373. PMid:30373305.
http://dx.doi.org/10.3390/ijms19113373...
; Lee et al., 2019LEE, D., JANG, E., LEE, M., KIM, S., LEE, Y., LEE, K. and BAHN, Y., 2019. Unraveling melanin biosynthesis and signaling networks in Cryptococcus neoformans. mBio, vol. 10, no. 5, pp. e02267-19. http://dx.doi.org/10.1128/mBio.02267-19. PMid:31575776.
http://dx.doi.org/10.1128/mBio.02267-19...
). The presence of mediators significantly hastens the oxidation of pentachlorophenol, anthracene, and other polycyclic hydrocarbons, textile dyes by laccases of basidiomycetes. The inclusion of mediators (vialuronic acid, 4-hydroxy-TEMPO, etc.) in the 6-APA modification reaction did not affect the formation of new compounds but significantly accelerated the reaction up to 15 minutes.

4. Conclusion

The data obtained indicate that purified enzyme preparations of the laccase of the fungus LS 1566 are promising enzymes for the transformation of penicillin antibiotics with the formation of at least three products identified by TLC (Rf - 0.18; 0.15; 0.11; 0.07).

Acknowledgements

The research was carried out at G.K. Scriabin Institute of Biochemistry and Physiology of Microorganisms, RAS, in the laboratory of enzymatic degradation of organic compounds under the guidance of Doctor of Biological Sciences, Prof. L.A. Golovleva. The authors would like to thank Liudmila Aleksandrovna Golovleva for the opportunity to conduct research.

The research has been done within the framework of State Assignment of the Russian Federation Ministry of Science and Higher Education № FZWG-2020-0021

References

  • ALCALDE, M., 2007. Laccases: biological functions, molecular structure and industrial applications. In: J. Polaina and A.P. MacCabe, eds. Industrial enzymes Dordrecht: Springer, pp. 461–476. http://dx.doi.org/10.1007/1-4020-5377-0_26
    » http://dx.doi.org/10.1007/1-4020-5377-0_26
  • ALDAYEL, F.M., ALSOBEG, M.S. and KHALIFA, A., 2021. In vitro antibacterial activities of silver nanoparticles synthesised using the seed extracts of three varieties of Phoenix dactylifera. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, pp. e242301. PMid:34346959.
  • ANDLAR, M., REZIĆ, T., MARĐETKO, N., KRACHER, D., LUDWIG, R. and ŠANTEK, B., 2018. Lignocellulose degradation: an overview of fungi and fungal enzymes involved in lignocellulose degradation. Engineering in Life Sciences, vol. 18, no. 11, pp. 768-778. http://dx.doi.org/10.1002/elsc.201800039 PMid:32624871.
    » http://dx.doi.org/10.1002/elsc.201800039
  • BABU, P.R., PINNAMANENI, R. and KOONA, S., 2012. Occurrences, physical and biochemical properties of laccase. Universal Journal of Environmental Research and Technology, vol. 2, no. 1, pp. 1-13.
  • BAINS, J., CAPALASH, N. and SHARMA, P., 2003. Laccase from a non-melanogenic, alkalotolerant γ-proteobacterium JB isolated from industrial wastewater drained soil. Biotechnology Letters, vol. 25, no. 14, pp. 1155-1159. http://dx.doi.org/10.1023/A:1024569722413 PMid:12967004.
    » http://dx.doi.org/10.1023/A:1024569722413
  • BURKE, R. and CAIRNEY, J., 2002. Laccases and other polyphenol oxidases in ecto-and ericoid mycorrhizal fungi. Mycorrhiza, vol. 12, no. 3, pp. 105-116. http://dx.doi.org/10.1007/s00572-002-0162-0 PMid:12072980.
    » http://dx.doi.org/10.1007/s00572-002-0162-0
  • FERRARONI, M., MYASOEDOVA, N.M., SCHMATCHENKO, V., LEONTIEVSKY, A.A., GOLOVLEVA, L.A., SCOZZAFAVA, A. and BRIGANTI, F., 2007. Crystal structure of a blue laccase from Lentinus tigrinus: evidences for intermediates in the molecular oxygen reductive splitting by multicopper oxidases. BMC Structural Biology, vol. 7, no. 1, pp. 60. http://dx.doi.org/10.1186/1472-6807-7-60 PMid:17897461.
    » http://dx.doi.org/10.1186/1472-6807-7-60
  • GUARDADO, A.L.P., BELLEVILLE, M. and ALANIS, M., 2019. Effect of redox mediators in pharmaceuticals degradation by laccase: a comparative study. Process Biochemistry, vol. 78, pp. 123-131. http://dx.doi.org/10.1016/j.procbio.2018.12.032
    » http://dx.doi.org/10.1016/j.procbio.2018.12.032
  • KOLOMYTSEVA, M.P., MYASOEDOVA, N.M., CHERNYKH, A.M., GAIDINA, A.S., SHEBANOVA, A.D., BASKUNOV, B.P., ASCHENBRENNER, J., ROSENGARTEN, J.F., RENFELD, Z.V., GASANOV, N.B., PINCHUK, I.P., CLASSEN, T., PIETRUSZKA, J. and GOLOVLEVA, L.A., 2019. Laccase isoform diversity in basidiomycete Lentinus strigosus 1566: potential for phenylpropanoid polymerization. International Journal of Biological Macromolecules, vol. 137, pp. 1199-1210. http://dx.doi.org/10.1016/j.ijbiomac.2019.07.056 PMid:31295487.
    » http://dx.doi.org/10.1016/j.ijbiomac.2019.07.056
  • LEE, D., JANG, E., LEE, M., KIM, S., LEE, Y., LEE, K. and BAHN, Y., 2019. Unraveling melanin biosynthesis and signaling networks in Cryptococcus neoformans. mBio, vol. 10, no. 5, pp. e02267-19. http://dx.doi.org/10.1128/mBio.02267-19 PMid:31575776.
    » http://dx.doi.org/10.1128/mBio.02267-19
  • LI, Q., YU, X., YANG, Y. and LIU, X., 2018. Simple determination of diacylglycerols using thin layer chromatography and visible spectrophotometry. Food Analytical Methods, vol. 11, no. 1, pp. 236-242. http://dx.doi.org/10.1007/s12161-017-0993-0
    » http://dx.doi.org/10.1007/s12161-017-0993-0
  • MADHAVI, V. and LELE, S.S., 2009. Laccase: properties and applications. BioResources, vol. 4, no. 4, pp. 1694-1717.
  • MIKOLASCH, A. and SCHAUER, F., 2009. Fungal laccases as tools for the synthesis of new hybrid molecules and biomaterials. Applied Microbiology and Biotechnology, vol. 82, no. 4, pp. 605-624. http://dx.doi.org/10.1007/s00253-009-1869-z PMid:19183983.
    » http://dx.doi.org/10.1007/s00253-009-1869-z
  • MORSI, R., BILAL, M., IQBAL, H.M. and ASHRAF, S.S., 2020. Laccases and peroxidases: the smart, greener and futuristic biocatalytic tools to mitigate recalcitrant emerging pollutants. The Science of the Total Environment, vol. 714, pp. 136572. http://dx.doi.org/10.1016/j.scitotenv.2020.136572 PMid:31986384.
    » http://dx.doi.org/10.1016/j.scitotenv.2020.136572
  • MYASOEDOVA, N.M., CHERNYKH, A.M., PSURTSEVA, N.V., BELOVA, N.V. and GOLOVLEVA, L.A., 2008. New efficient producers of fungal laccases. Applied Biochemistry and Microbiology, vol. 44, no. 1, pp. 73-77. http://dx.doi.org/10.1134/S0003683808010122
    » http://dx.doi.org/10.1134/S0003683808010122
  • MYASOEDOVA, N.M., GASANOV, N.B., CHERNYKH, A.M., KOLOMYTSEVA, M.P. and GOLOVLEVA, L.A., 2015. Selective regulation of laccase isoform production by the Lentinus strigosus 1566 fungus. Applied Biochemistry and Microbiology, vol. 51, no. 2, pp. 222-229. http://dx.doi.org/10.1134/S0003683815020131 PMid:26027358.
    » http://dx.doi.org/10.1134/S0003683815020131
  • NAVADA, K.K. and KULAL, A., 2019. Enzymatic degradation of chloramphenicol by laccase from Trametes hirsuta and comparison among mediators. International Biodeterioration & Biodegradation, vol. 138, pp. 63-69. http://dx.doi.org/10.1016/j.ibiod.2018.12.012
    » http://dx.doi.org/10.1016/j.ibiod.2018.12.012
  • RAVE, A.F.G., KUSS, A.V., PEIL, G.H.S., LADEIRA, S.R., VILLARREAL, J.P.V. and NASCENTE, P.S., 2019. Biochemical identification techniques and antibiotic susceptibility profile of lipolytic ambiental bacteria from effluents. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 79, no. 4, pp. 555-565. http://dx.doi.org/10.1590/1519-6984.05616 PMid:30484476.
    » http://dx.doi.org/10.1590/1519-6984.05616
  • SALEEM, A., BUKHARI, S.M., ZAIDI, A., FAROOQ, U., ALI, M., KHAN, A., KHAN, S., SHAH, K.H., MAHMOOD, A. and KHAN, F.A., 2020. Enzyme inhibition and antibacterial potential of 4-Hydroxycoumarin derivatives. Brazilian Journal of Pharmaceutical Sciences, vol. 56, pp. e18654.http://dx.doi.org/10.1590/s2175-97902019000418654
    » http://dx.doi.org/10.1590/s2175-97902019000418654
  • THURSTON, C.F., 1994. The structure and function of fungal laccases. Microbiology, vol. 140, no. 1, pp. 19-26. http://dx.doi.org/10.1099/13500872-140-1-19
    » http://dx.doi.org/10.1099/13500872-140-1-19
  • TUKENOVA, Z., MUSTAFAYEV, M., ALIMZHANOVA, M., AKYLBEKOVA, T. and ASHIMULY, K., 2021. Influence of pesticides on the biological activity of light chestnut soils in South-East Kazakhstan. Journal of Water and Land Development, no. 48, pp. 141-147.
  • WANG, X., YAO, B. and SU, X., 2018. Linking enzymatic oxidative degradation of lignin to organics detoxification. International Journal of Molecular Sciences, vol. 19, no. 11, pp. 3373. http://dx.doi.org/10.3390/ijms19113373 PMid:30373305.
    » http://dx.doi.org/10.3390/ijms19113373
  • WILLIAMSON, P.R., 1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. Journal of Bacteriology, vol. 176, no. 3, pp. 656-664. http://dx.doi.org/10.1128/jb.176.3.656-664.1994 PMid:8300520.
    » http://dx.doi.org/10.1128/jb.176.3.656-664.1994
  • YESILADA, O., BIRHANLI, E. and GECKIL, H., 2018. Bioremediation and decolorization of textile dyes by white rot fungi and laccase enzymes. In: R. Prasad, ed. Mycoremediation and environmental sustainability mycoremediation and environmental sustainability Cham: Springer, vol. 2, pp. 121–153. http://dx.doi.org/10.1007/978-3-319-77386-5_5
    » http://dx.doi.org/10.1007/978-3-319-77386-5_5
  • ZENGIN, M., GENC, H., TASLIMI, P., KESTANE, A., GUCLU, E., OGUTLU, A., KARABAY, O. and GULCIN, I., 2018. Novel thymol bearing oxypropanolamine derivatives as potent some metabolic enzyme inhibitors: their antidiabetic, anticholinergic and antibacterial potentials. Bioorganic Chemistry, vol. 81, pp. 119-126. http://dx.doi.org/10.1016/j.bioorg.2018.08.003 PMid:30118983.
    » http://dx.doi.org/10.1016/j.bioorg.2018.08.003
  • ZHAO, S., XIAO, C., WANG, J., TIAN, K., JI, W., YANG, T., KHAN, B., QIAN, G., YAN, W. and YE, Y., 2020. Discovery of natural FabH inhibitors using an immobilized enzyme column and their antibacterial activity against Xanthomonas oryzae pv. oryzae. Journal of Agricultural and Food Chemistry, vol. 68, no. 48, pp. 14204-14211. http://dx.doi.org/10.1021/acs.jafc.0c06363 PMid:33201689.
    » http://dx.doi.org/10.1021/acs.jafc.0c06363

Publication Dates

  • Publication in this collection
    07 Mar 2022
  • Date of issue
    2024

History

  • Received
    07 Oct 2021
  • Accepted
    16 Nov 2021
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br