Phenothiazines Rapidly Induce Laccase Expression and Lignin-Degrading Properties in the White-Rot Fungus Phlebia radiata

Hirakawa, Matthew P.; Rodriguez, Alberto; Tran-Gyamfi, Mary B.; Light, Yooli K.; Martinez, Salvador; Diamond-Pott, Henry; Simmons, Blake A.; Sale, Kenneth L.

doi:10.3390/jof9030371

Title: Phenothiazines Rapidly Induce Laccase Expression and Lignin-Degrading Properties in the White-Rot Fungus Phlebia radiata

Journal Article · 17 March 2023 · Journal of Fungi

DOI: https://doi.org/10.3390/jof9030371 · OSTI ID:2234219

^[1]; Rodriguez, Alberto ^[1]; Tran-Gyamfi, Mary B. ^[1];

^[1]; Martinez, Salvador ^[1]; Diamond-Pott, Henry ^[1];

^[2];

^[3]

Sandia National Lab. (SNL-CA), Livermore, CA (United States)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Joint BioEnergy Institute, Emeryville, CA (United States)
Joint BioEnergy Institute, Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)

Phlebia radiata is a widespread white-rot basidiomycete fungus with significance in diverse biotechnological applications due to its ability to degrade aromatic compounds, xenobiotics, and lignin using an assortment of oxidative enzymes including laccase. In this work, a chemical screen with 480 conditions was conducted to identify chemical inducers of laccase expression in P. radiata. Among the chemicals tested, phenothiazines were observed to induce laccase activity in P. radiata, with promethazine being the strongest laccase inducer of the phenothiazine-derived compounds examined. Secretomes produced by promethazine-treated P. radiata exhibited increased laccase protein abundance, increased enzymatic activity, and an enhanced ability to degrade phenolic model lignin compounds. Transcriptomics analyses revealed that promethazine rapidly induced the expression of genes encoding lignin-degrading enzymes, including laccase and various oxidoreductases, showing that the increased laccase activity was due to increased laccase gene expression. Finally, the generality of promethazine as an inducer of laccases in fungi was demonstrated by showing that promethazine treatment also increased laccase activity in other relevant fungal species with known lignin conversion capabilities including Trametes versicolor and Pleurotus ostreatus.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Sandia National Laboratories (SNL-CA), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Laboratory Directed Research and Development (LDRD) Program; USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC02-05CH11231; NA0003525

OSTI ID:: 2234219

Journal Information:: Journal of Fungi, Journal Name: Journal of Fungi Journal Issue: 3 Vol. 9; ISSN 2309-608X

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (61)

Structure and Action Mechanism of Ligninolytic Enzymes Wong, Dominic W. S. Applied Biochemistry and Biotechnology, Vol. 157, Issue 2 https://doi.org/10.1007/s12010-008-8279-z	journal	June 2008
Intracellular pathways for lignin catabolism in white-rot fungi del Cerro, Carlos; Erickson, Erika; Dong, Tao Proceedings of the National Academy of Sciences, Vol. 118, Issue 9 https://doi.org/10.1073/pnas.2017381118	journal	February 2021
Microbial enzyme systems for lignin degradation and their transcriptional regulation Furukawa, Takanori; Bello, Fatai Olumide; Horsfall, Louise Frontiers in Biology, Vol. 9, Issue 6 https://doi.org/10.1007/s11515-014-1336-9	journal	November 2014
Time-scale dynamics of proteome and transcriptome of the white-rot fungus Phlebia radiata: growth on spruce wood and decay effect on lignocellulose Kuuskeri, Jaana; Häkkinen, Mari; Laine, Pia Figshare https://doi.org/10.6084/m9.figshare.c.3641717	collection	January 2016
Transcriptome and Secretome Analyses of Phanerochaete chrysosporium Reveal Complex Patterns of Gene Expression Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M. Applied and Environmental Microbiology, Vol. 75, Issue 12 https://doi.org/10.1128/AEM.00314-09	journal	April 2009
Induction and Transcriptional Regulation of Laccases in Fungi Piscitelli, Alessandra; Giardina, Paola; Lettera, Vincenzo Current Genomics, Vol. 12, Issue 2 https://doi.org/10.2174/138920211795564331	journal	April 2011
Multiple non-psychiatric effects of phenothiazines: A review Sudeshna, Gangopadhyay; Parimal, Karmakar European Journal of Pharmacology, Vol. 648, Issue 1-3 https://doi.org/10.1016/j.ejphar.2010.08.045	journal	December 2010
Phenotype MicroArrays as a complementary tool to next generation sequencing for characterization of tree endophytes Blumenstein, Kathrin; Macaya-Sanz, David; Martín, Juan A. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.01033	journal	September 2015
Can laccases catalyze bond cleavage in lignin? Munk, Line; Sitarz, Anna K.; Kalyani, Dayanand C. Biotechnology Advances, Vol. 33, Issue 1 https://doi.org/10.1016/j.biotechadv.2014.12.008	journal	January 2015
Reactive Oxygen Species and Induction of Lignin Peroxidase in Phanerochaete chrysosporium Belinky, P. A.; Flikshtein, N.; Lechenko, S. Applied and Environmental Microbiology, Vol. 69, Issue 11 https://doi.org/10.1128/AEM.69.11.6500-6506.2003	journal	November 2003
The production of laccases by white-rot fungi under solid-state fermentation conditions Chmelová, Daniela; Legerská, Barbora; Kunstová, Jana World Journal of Microbiology and Biotechnology, Vol. 38, Issue 2 https://doi.org/10.1007/s11274-021-03207-y	journal	January 2022
Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium Vanden Wymelenberg, A.; Gaskell, J.; Mozuch, M. Applied and Environmental Microbiology, Vol. 76, Issue 11 https://doi.org/10.1128/AEM.00058-10	journal	April 2010
The effect of culture conditions on the production of lignin modifying enzymes by the white-rot fungus Phlebia radiata Niku-Paavola, M. -L.; Karhunen, E.; Kantelinen, A. Journal of Biotechnology, Vol. 13, Issue 2-3 https://doi.org/10.1016/0168-1656(90)90106-L	journal	February 1990
The White-Rot Basidiomycete Dichomitus squalens Shows Highly Specific Transcriptional Response to Lignocellulose-Related Aromatic Compounds Kowalczyk, Joanna E.; Peng, Mao; Pawlowski, Megan Frontiers in Bioengineering and Biotechnology, Vol. 7 https://doi.org/10.3389/fbioe.2019.00229	journal	September 2019
Near-optimal probabilistic RNA-seq quantification Bray, Nicolas L.; Pimentel, Harold; Melsted, Páll Nature Biotechnology, Vol. 34, Issue 5 https://doi.org/10.1038/nbt.3519	journal	April 2016
Genome description of Phlebia radiata 79 with comparative genomics analysis on lignocellulose decomposition machinery of phlebioid fungi Mäkinen, Mari; Kuuskeri, Jaana; Laine, Pia BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5817-8	journal	May 2019
Antifungal Therapy: New Advances in the Understanding and Treatment of Mycosis Scorzoni, Liliana; de Paula e. Silva, Ana C. A.; Marcos, Caroline M. Frontiers in Microbiology, Vol. 08 https://doi.org/10.3389/fmicb.2017.00036	journal	January 2017
A critical review of the application of white rot fungus to environmental pollution control Gao, Dawen; Du, Lina; Yang, Jiaoling Critical Reviews in Biotechnology, Vol. 30, Issue 1 https://doi.org/10.3109/07388550903427272	journal	January 2010
Production of lignin peroxidase and laccase by Phlebia radiata Kantelinen, Anne; Hatakka, Annele; Viikari, Liisa Applied Microbiology and Biotechnology, Vol. 31, Issue 3 https://doi.org/10.1007/BF00258401	journal	September 1989
Review of advances in the development of laccases for the valorization of lignin to enable the production of lignocellulosic biofuels and bioproducts Leynaud Kieffer Curran, Laure M. C.; Pham, Le Thanh Mai; Sale, Kenneth L. Biotechnology Advances, Vol. 54 https://doi.org/10.1016/j.biotechadv.2021.107809	journal	January 2022
Laccase: addressing the ambivalence associated with the calculation of enzyme activity Agrawal, Komal; Verma, Pradeep 3 Biotech, Vol. 9, Issue 10 https://doi.org/10.1007/s13205-019-1895-1	journal	September 2019
Lignin Biodegradation and Its Valorization Cui, Lingwei; Wang, Zheyi; Zeng, Yan Fermentation, Vol. 8, Issue 8 https://doi.org/10.3390/fermentation8080366	journal	July 2022
Nutritional Regulation of Lignin Degradation by Phanerochaete chrysosporium Jeffries, Thomas W.; Choi, Suki; Kirk, T. Kent Applied and Environmental Microbiology, Vol. 42, Issue 2 https://doi.org/10.1128/aem.42.2.290-296.1981	journal	January 1981
Laccases: structure, function, and potential application in water bioremediation Arregui, Leticia; Ayala, Marcela; Gómez-Gil, Ximena Microbial Cell Factories, Vol. 18, Issue 1 https://doi.org/10.1186/s12934-019-1248-0	journal	November 2019
Characterization of Lignocellulolytic Enzymes from White-Rot Fungi Manavalan, Tamilvendan; Manavalan, Arulmani; Heese, Klaus Current Microbiology, Vol. 70, Issue 4 https://doi.org/10.1007/s00284-014-0743-0	journal	December 2014
Chemical structure of phenothiazines and their biological activity Jaszczyszyn, Agata; Gąsiorowski, Kazimierz; Świątek, Piotr Pharmacological Reports, Vol. 64, Issue 1 https://doi.org/10.1016/S1734-1140(12)70726-0	journal	January 2012
A structural-chemical explanation of fungal laccase activity Mehra, Rukmankesh; Muschiol, Jan; Meyer, Anne S. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35633-8	journal	November 2018
Laccase: a multi‐purpose biocatalyst at the forefront of biotechnology Mate, Diana M.; Alcalde, Miguel Microbial Biotechnology, Vol. 10, Issue 6 https://doi.org/10.1111/1751-7915.12422	journal	October 2016
High-throughput functional annotation and data mining with the Blast2GO suite Gotz, S.; Garcia-Gomez, J. M.; Terol, J. Nucleic Acids Research, Vol. 36, Issue 10 https://doi.org/10.1093/nar/gkn176	journal	April 2008
Membrane of Candida albicans as a target of berberine Zorić, Nataša; Kosalec, Ivan; Tomić, Siniša BMC Complementary and Alternative Medicine, Vol. 17, Issue 1 https://doi.org/10.1186/s12906-017-1773-5	journal	May 2017
Systems biology-guided understanding of white-rot fungi for biotechnological applications: A review Kijpornyongpan, Teeratas; Schwartz, Alexa; Yaguchi, Allison iScience, Vol. 25, Issue 7 https://doi.org/10.1016/j.isci.2022.104640	journal	July 2022
Comparative Studies of Extracellular Fungal Laccases Bollag, Jean-Marc; Leonowicz, Andrzej Applied and Environmental Microbiology, Vol. 48, Issue 4 https://doi.org/10.1128/aem.48.4.849-854.1984	journal	January 1984
Genome description of Phlebia radiata 79 with comparative genomics analysis on lignocellulose decomposition machinery of phlebioid fungi MĂ¤Kinen, Mari; Kuuskeri, Jaana; Laine, Pia Figshare https://doi.org/10.6084/m9.figshare.c.4521080	collection	January 2019
Differential analysis of RNA-seq incorporating quantification uncertainty Pimentel, Harold; Bray, Nicolas L.; Puente, Suzette Nature Methods, Vol. 14, Issue 7 https://doi.org/10.1038/nmeth.4324	journal	June 2017
Berberine Antifungal Activity in Fluconazole-Resistant Pathogenic Yeasts: Action Mechanism Evaluated by Flow Cytometry and Biofilm Growth Inhibition in Candida spp da Silva, Anderson Ramos; de Andrade Neto, João Batista; da Silva, Cecília Rocha Antimicrobial Agents and Chemotherapy, Vol. 60, Issue 6 https://doi.org/10.1128/AAC.01846-15	journal	June 2016
Drug repurposing strategies in the development of potential antifungal agents Zhang, Qian; Liu, Fangyan; Zeng, Meng Applied Microbiology and Biotechnology, Vol. 105, Issue 13 https://doi.org/10.1007/s00253-021-11407-7	journal	June 2021
Bioremediation of lignin derivatives and phenolics in wastewater with lignin modifying enzymes: Status, opportunities and challenges Singh, Anil Kumar; Bilal, Muhammad; Iqbal, Hafiz M. N. Science of The Total Environment, Vol. 777 https://doi.org/10.1016/j.scitotenv.2021.145988	journal	July 2021
Systematic Analysis of the Pleurotus ostreatus Laccase Gene (PoLac) Family and Functional Characterization of PoLac2 Involved in the Degradation of Cotton-Straw Lignin Jiao, Xiaoyu; Li, Guoqing; Wang, Yan Molecules, Vol. 23, Issue 4 https://doi.org/10.3390/molecules23040880	journal	April 2018
Influence of aromatic compounds on biodegradation of [ 14 C]-labeled xylan and mannan by the white-rot fungus Phlebia radiata Rogalski, J.; Cho, N-S; Zadora, J. Journal of Industrial Microbiology and Biotechnology, Vol. 28, Issue 3 https://doi.org/10.1038/sj.jim.7000221	journal	March 2002
Conversion of depolymerized sugars and aromatics from engineered feedstocks by two oleaginous red yeasts Rodriguez, Alberto; Ersig, Nadine; Geiselman, Gina M. Bioresource Technology, Vol. 286 https://doi.org/10.1016/j.biortech.2019.121365	journal	August 2019
Effect of copper, nutrient nitrogen, and wood-supplement on the production of lignin-modifying enzymes by the white-rot fungus Phlebia radiata Mäkelä, Miia R.; Lundell, Taina; Hatakka, Annele Fungal Biology, Vol. 117, Issue 1 https://doi.org/10.1016/j.funbio.2012.11.006	journal	January 2013
Phenothiazines as potent modulators of yeast multidrug resistance Kolaczkowski, M. International Journal of Antimicrobial Agents, Vol. 22, Issue 3 https://doi.org/10.1016/S0924-8579(03)00214-0	journal	September 2003
Laccase Properties, Physiological Functions, and Evolution Janusz, Grzegorz; Pawlik, Anna; Świderska-Burek, Urszula International Journal of Molecular Sciences, Vol. 21, Issue 3 https://doi.org/10.3390/ijms21030966	journal	January 2020
Conversion of Milled Pine Wood by Manganese Peroxidase from Phlebia radiata Hofrichter, M.; Lundell, T.; Hatakka, A. Applied and Environmental Microbiology, Vol. 67, Issue 10 https://doi.org/10.1128/AEM.67.10.4588-4593.2001	journal	October 2001
Heterologous Expression, Characterization, and Comparison of Laccases from the White Rot Causing Basidiomycete Cerrena Unicolor Mai Pham, Le Thanh; Deng, Kai; Northen, Trent Catalysis Research, Vol. 02, Issue 03 https://doi.org/10.21926/cr.2203028	journal	September 2022
Trametes versicolor laccase production using agricultural wastes: a comparative study in Erlenmeyer flasks, bioreactor and tray Pinheiro, Vanessa Elisa; Michelin, Michele; Vici, Ana Claudia Bioprocess and Biosystems Engineering, Vol. 43, Issue 3 https://doi.org/10.1007/s00449-019-02245-z	journal	November 2019
Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78 Martinez, Diego; Larrondo, Luis F.; Putnam, Nik Nature Biotechnology, Vol. 22, Issue 6 https://doi.org/10.1038/nbt967	journal	May 2004
Cerrena unicolor Laccases, Genes Expression and Regulation of Activity Pawlik, Anna; Ciołek, Beata; Sulej, Justyna Biomolecules, Vol. 11, Issue 3 https://doi.org/10.3390/biom11030468	journal	March 2021
Enzymatic "Combustion": The Microbial Degradation of Lignin Kirk, T. K.; Farrell, R. L. Annual Review of Microbiology, Vol. 41, Issue 1, p. 465-501 https://doi.org/10.1146/annurev.mi.41.100187.002341	journal	October 1987
Ligninolytic peroxidase gene expression by Pleurotus ostreatus : Differential regulation in lignocellulose medium and effect of temperature and pH Fernández-Fueyo, Elena; Castanera, Raul; Ruiz-Dueñas, Francisco J. Fungal Genetics and Biology, Vol. 72 https://doi.org/10.1016/j.fgb.2014.02.003	journal	November 2014
Mechanism of Laccase Induction via Emodin in Trametes versicolor Wang, Lin; Luo, Xuecai; Pan, Yu Frontiers in Bioengineering and Biotechnology, Vol. 9 https://doi.org/10.3389/fbioe.2021.653800	journal	May 2021
Role of Phenothiazines and Structurally Similar Compounds of Plant Origin in the Fight against Infections by Drug Resistant Bacteria Dastidar, Sujata; Kristiansen, Jette; Molnar, Joseph Antibiotics, Vol. 2, Issue 1 https://doi.org/10.3390/antibiotics2010058	journal	February 2013
Lignin degradation: microorganisms, enzymes involved, genomes analysis and evolution Janusz, Grzegorz; Pawlik, Anna; Sulej, Justyna FEMS Microbiology Reviews, Vol. 41, Issue 6 https://doi.org/10.1093/femsre/fux049	journal	October 2017
Microbial and Enzymatic Degradation of Wood and Wood Components Eriksson, Karl-Erik L.; Blanchette, Robert A.; Ander, Paul Springer Series in Wood Science https://doi.org/10.1007/978-3-642-46687-8	book	January 1990
Antifungal Phenothiazines: Optimization, Characterization of Mechanism, and Modulation of Neuroreceptor Activity Montoya, Marhiah C.; DiDone, Louis; Heier, Richard F. ACS Infectious Diseases, Vol. 4, Issue 4 https://doi.org/10.1021/acsinfecdis.7b00157	journal	October 2017
Formation and Action of Lignin-Modifying Enzymes in Cultures of Phlebia radiata Supplemented with Veratric Acid Lundell, Taina; Leonowicz, Andrzej; Rogalski, Jerzy Applied and Environmental Microbiology, Vol. 56, Issue 9 https://doi.org/10.1128/aem.56.9.2623-2629.1990	journal	January 1990
Fungal-specific PCR primers developed for analysis of the ITS region of environmental DNA extracts Martin, Kendall J.; Rygiewicz, Paul T. BMC Microbiology, Vol. 5, Issue 1, p. 28 https://doi.org/10.1186/1471-2180-5-28	journal	May 2005
fastp: an ultra-fast all-in-one FASTQ preprocessor Chen, Shifu; Zhou, Yanqing; Chen, Yaru Bioinformatics, Vol. 34, Issue 17 https://doi.org/10.1093/bioinformatics/bty560	journal	September 2018
Qualitative and Quantitative Methods for Isolation and Characterization of Lignin-Modifying Enzymes Secreted by Microorganisms Kameshwar, Ayyappa Kumar Sista; Qin, Wensheng BioEnergy Research, Vol. 10, Issue 1 https://doi.org/10.1007/s12155-016-9784-5	journal	August 2016
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
Time-scale dynamics of proteome and transcriptome of the white-rot fungus Phlebia radiata: growth on spruce wood and decay effect on lignocellulose Kuuskeri, Jaana; Häkkinen, Mari; Laine, Pia Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0608-9	journal	September 2016

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59 BASIC BIOLOGICAL SCIENCES
white-rot fungi
laccase
lignin
phenothiazine

Title: Phenothiazines Rapidly Induce Laccase Expression and Lignin-Degrading Properties in the White-Rot Fungus Phlebia radiata

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