Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, sp. KUC8613
Abstract
The environmental accumulation of polycyclic aromatic hydrocarbons (PAHs) is of great concern due to potential carcinogenic and mutagenic risks, as well as their resistance to remediation. While many fungi have been reported to break down PAHs in environments, the details of gene-based metabolic pathways are not yet comprehensively understood. Specifically, the genome-scale transcriptional responses of fungal PAH degradation have rarely been reported. In this study, we report the genomic and transcriptomic basis of PAH bioremediation by a potent fungal degrader, Dentipellis sp. KUC8613. The genome size of this fungus was 36.71 Mbp long encoding 14,320 putative protein-coding genes. The strain efficiently removed more than 90% of 100 mg/l concentration of PAHs within 10 days. The genomic and transcriptomic analysis of this white rot fungus highlights that the strain primarily utilized non-ligninolytic enzymes to remove various PAHs, rather than typical ligninolytic enzymes known for playing important roles in PAH degradation. PAH removal by non-ligninolytic enzymes was initiated by both different PAH-specific and common upregulation of P450s, followed by downstream PAH-transforming enzymes such as epoxide hydrolases, dehydrogenases, FAD-dependent monooxygenases, dioxygenases, and glycosyl- or glutathione transferases. Among the various PAHs, phenanthrene induced a more dynamic transcriptomic response possibly due to its greater cytotoxicity, leading to highlymore »
- Authors:
-
- Korea Univ., Seoul (South Korea)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Korea Research Inst., Seoul (South Korea)
- Oregon State Univ., Corvallis, OR (United States)
- Centre National de la Recherche, Paris (France); Univ. of Aix-Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); Korea Institute of Energy Technology Evaluation and Planning
- OSTI Identifier:
- 1619129
- Grant/Contract Number:
- AC02-05CH11231; 20173010092460
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Applied Microbiology and Biotechnology
- Additional Journal Information:
- Journal Volume: 103; Journal Issue: 19; Journal ID: ISSN 0175-7598
- Publisher:
- Springer
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; PAH (polycyclic aromatic hydrocarbon); mycoremediation; Dentipellis sp. KUC8613; white rot fungus; genomics; transcriptomics
Citation Formats
Park, Hongjae, Min, Byoungnam, Jang, Yeongseon, Kim, Jungyeon, Lipzen, Anna, Sharma, Aditi, Andreopoulos, Bill, Johnson, Jenifer, Riley, Robert, Spatafora, Joseph W., Henrissat, Bernard, Kim, Kyoung Heon, Grigoriev, Igor V., Kim, Jae-Jin, and Choi, In-Geol. Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, sp. KUC8613. United States: N. p., 2019.
Web. doi:10.1007/s00253-019-10089-6.
Park, Hongjae, Min, Byoungnam, Jang, Yeongseon, Kim, Jungyeon, Lipzen, Anna, Sharma, Aditi, Andreopoulos, Bill, Johnson, Jenifer, Riley, Robert, Spatafora, Joseph W., Henrissat, Bernard, Kim, Kyoung Heon, Grigoriev, Igor V., Kim, Jae-Jin, & Choi, In-Geol. Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, sp. KUC8613. United States. https://doi.org/10.1007/s00253-019-10089-6
Park, Hongjae, Min, Byoungnam, Jang, Yeongseon, Kim, Jungyeon, Lipzen, Anna, Sharma, Aditi, Andreopoulos, Bill, Johnson, Jenifer, Riley, Robert, Spatafora, Joseph W., Henrissat, Bernard, Kim, Kyoung Heon, Grigoriev, Igor V., Kim, Jae-Jin, and Choi, In-Geol. Tue .
"Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, sp. KUC8613". United States. https://doi.org/10.1007/s00253-019-10089-6. https://www.osti.gov/servlets/purl/1619129.
@article{osti_1619129,
title = {Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, sp. KUC8613},
author = {Park, Hongjae and Min, Byoungnam and Jang, Yeongseon and Kim, Jungyeon and Lipzen, Anna and Sharma, Aditi and Andreopoulos, Bill and Johnson, Jenifer and Riley, Robert and Spatafora, Joseph W. and Henrissat, Bernard and Kim, Kyoung Heon and Grigoriev, Igor V. and Kim, Jae-Jin and Choi, In-Geol},
abstractNote = {The environmental accumulation of polycyclic aromatic hydrocarbons (PAHs) is of great concern due to potential carcinogenic and mutagenic risks, as well as their resistance to remediation. While many fungi have been reported to break down PAHs in environments, the details of gene-based metabolic pathways are not yet comprehensively understood. Specifically, the genome-scale transcriptional responses of fungal PAH degradation have rarely been reported. In this study, we report the genomic and transcriptomic basis of PAH bioremediation by a potent fungal degrader, Dentipellis sp. KUC8613. The genome size of this fungus was 36.71 Mbp long encoding 14,320 putative protein-coding genes. The strain efficiently removed more than 90% of 100 mg/l concentration of PAHs within 10 days. The genomic and transcriptomic analysis of this white rot fungus highlights that the strain primarily utilized non-ligninolytic enzymes to remove various PAHs, rather than typical ligninolytic enzymes known for playing important roles in PAH degradation. PAH removal by non-ligninolytic enzymes was initiated by both different PAH-specific and common upregulation of P450s, followed by downstream PAH-transforming enzymes such as epoxide hydrolases, dehydrogenases, FAD-dependent monooxygenases, dioxygenases, and glycosyl- or glutathione transferases. Among the various PAHs, phenanthrene induced a more dynamic transcriptomic response possibly due to its greater cytotoxicity, leading to highly upregulated genes involved in the translocation of PAHs, a defense system against reactive oxygen species, and ATP synthesis. Finally, our genomic and transcriptomic data provide a foundation of understanding regarding the mycoremediation of PAHs and the application of this strain for polluted environments.},
doi = {10.1007/s00253-019-10089-6},
journal = {Applied Microbiology and Biotechnology},
number = 19,
volume = 103,
place = {United States},
year = {2019},
month = {9}
}
Web of Science
Works referenced in this record:
Genome-wide identification of ATP-binding cassette ( ABC ) transporters and their roles in response to polycyclic aromatic hydrocarbons (PAHs) in the copepod Paracyclopina nana
journal, February 2017
- Jeong, Chang-Bum; Kim, Duck-Hyun; Kang, Hye-Min
- Aquatic Toxicology, Vol. 183
Biodegradation of Phenanthrene by Fungi Screened from Nature
journal, December 2007
- Hadibarata, Tony; Tachibana, Sanro; Itoh, Kazutaka
- Pakistan Journal of Biological Sciences, Vol. 10, Issue 15
Lignin-Modifying Enzymes of the White Rot Basidiomycete Ganoderma lucidum
journal, December 1999
- D’Souza, Trevor M.; Merritt, Carlos S.; Reddy, C. Adinarayana
- Applied and Environmental Microbiology, Vol. 65, Issue 12
Remediation of soils contaminated with polycyclic aromatic hydrocarbons (PAHs)
journal, December 2009
- Gan, S.; Lau, E. V.; Ng, H. K.
- Journal of Hazardous Materials, Vol. 172, Issue 2-3
Environmental applications for biosurfactants
journal, January 2005
- Mulligan, Catherine N.
- Environmental Pollution, Vol. 133, Issue 2
Natural roles of biosurfactants. Minireview
journal, April 2001
- Ron, Eliora Z.; Rosenberg, Eugene
- Environmental Microbiology, Vol. 3, Issue 4
Initial oxidative and subsequent conjugative metabolites produced during the metabolism of phenanthrene by fungi
journal, April 1996
- Casillas, R. P.; Crow, S. A.; Heinze, T. M.
- Journal of Industrial Microbiology, Vol. 16, Issue 4
Fungal degradation of polycyclic aromatic hydrocarbons (PAHs) by Scopulariopsis brevicaulis and its application in bioremediation of PAH-contaminated soil
journal, February 2016
- Mao, Jian; Guan, Wenwen
- Acta Agriculturae Scandinavica, Section B — Soil & Plant Science, Vol. 66, Issue 5
Transcriptome Profile of Polycyclic Aromatic Hydrocarbon-Degrading Fungi Isolated from Taxus rhizosphere
journal, April 2019
- Gao, Rui; Hao, Da Cheng; Hu, Wenli
- Current Science, Vol. 116, Issue 7
Current State of Knowledge in Microbial Degradation of Polycyclic Aromatic Hydrocarbons (PAHs): A Review
journal, August 2016
- Ghosal, Debajyoti; Ghosh, Shreya; Dutta, Tapan K.
- Frontiers in Microbiology, Vol. 7
Involvement of the Ligninolytic System of White-Rot and Litter-Decomposing Fungi in the Degradation of Polycyclic Aromatic Hydrocarbons
journal, January 2012
- Pozdnyakova, Natalia N.
- Biotechnology Research International, Vol. 2012
Polycyclic aromatic hydrocarbons and cancer in man.
journal, November 1996
- Mastrangelo, G.; Fadda, E.; Marzia, V.
- Environmental Health Perspectives, Vol. 104, Issue 11
clusterProfiler: an R Package for Comparing Biological Themes Among Gene Clusters
journal, May 2012
- Yu, Guangchuang; Wang, Li-Gen; Han, Yanyan
- OMICS: A Journal of Integrative Biology, Vol. 16, Issue 5
High-quality draft assemblies of mammalian genomes from massively parallel sequence data
journal, December 2010
- Gnerre, S.; MacCallum, I.; Przybylski, D.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 4
Biodegradation of polycyclic aromatic hydrocarbons by new isolates of white rot fungi.
journal, January 1992
- Field, J. A.; de Jong, E.; Feijoo Costa, G.
- Applied and Environmental Microbiology, Vol. 58, Issue 7
Microbial biodegradation of polyaromatic hydrocarbons
journal, November 2008
- Peng, Ri-He; Xiong, Ai-Sheng; Xue, Yong
- FEMS Microbiology Reviews, Vol. 32, Issue 6
Genetics of Polycyclic Aromatic Hydrocarbon Metabolism in Diverse Aerobic Bacteria
journal, January 2003
- Habe, Hiroshi; Omori, Toshio
- Bioscience, Biotechnology, and Biochemistry, Vol. 67, Issue 2
Potential of non-ligninolytic fungi in bioremediation of chlorinated and polycyclic aromatic hydrocarbons
journal, December 2015
- Marco-Urrea, Ernest; García-Romera, Inmaculada; Aranda, Elisabet
- New Biotechnology, Vol. 32, Issue 6
Levels and patterns of polycyclic aromatic hydrocarbons in incineration ashes
journal, July 2003
- Johansson, Inger; van Bavel, Bert
- Science of The Total Environment, Vol. 311, Issue 1-3
Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs)
journal, September 2010
- Syed, Khajamohiddin; Doddapaneni, Harshavardhan; Subramanian, Venkataramanan
- Biochemical and Biophysical Research Communications, Vol. 399, Issue 4
Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: A review
journal, January 2017
- Kadri, Tayssir; Rouissi, Tarek; Kaur Brar, Satinder
- Journal of Environmental Sciences, Vol. 51
FunGAP: Fungal Genome Annotation Pipeline using evidence-based gene model evaluation
journal, June 2017
- Min, Byoungnam; Grigoriev, Igor V.; Choi, In-Geol
- Bioinformatics, Vol. 33, Issue 18
Stress responses to polycyclic aromatic hydrocarbons in Arabidopsis include growth inhibition and hypersensitive response-like symptoms
journal, October 2005
- Alkio, Merianne; Tabuchi, Tomoko M.; Wang, Xuchen
- Journal of Experimental Botany, Vol. 56, Issue 421
Human Cytochromes P450 Associated with the Phase 1 Metabolism of Drugs and other Xenobiotics: A Compilation of Substrates and Inhibitors of the CYP1, CYP2 and CYP3 Families
journal, October 2003
- Lewis, David
- Current Medicinal Chemistry, Vol. 10, Issue 19
Degradation of fluorene, anthracene, phenanthrene, fluoranthene, and pyrene lacks connection to the production of extracellular enzymes by Pleurotus ostreatus and Bjerkandera adusta
journal, April 1999
- Schützendübel, Andres; Majcherczyk, Andrzej; Johannes, Christian
- International Biodeterioration & Biodegradation, Vol. 43, Issue 3
Biotechnological procedures to select white rot fungi for the degradation of PAHs
journal, February 2014
- Lee, Hwanhwi; Jang, Yeongseon; Choi, Yong-Seok
- Journal of Microbiological Methods, Vol. 97
Isolation and Characterization of Phenanthrene Degrading Bacteria from Diesel Fuel-Contaminated Antarctic Soils
journal, August 2017
- Gran-Scheuch, Alejandro; Fuentes, Edwar; Bravo, Denisse M.
- Frontiers in Microbiology, Vol. 8
Degradation of Polyaromatic Hydrocarbons by Organic Solvent-tolerant Bacteria from Deep Sea
journal, January 1995
- Abe, Akihisa; Inoue, Akira; Usami, Ron
- Bioscience, Biotechnology, and Biochemistry, Vol. 59, Issue 6
Genomic and metabolic analysis of fluoranthene degradation pathway in Celeribacter indicus P73T
journal, January 2015
- Cao, Junwei; Lai, Qiliang; Yuan, Jun
- Scientific Reports, Vol. 5, Issue 1
Effect of carbon and nitrogen limitation on lignin peroxidase and manganese peroxidaseproduction by Phanerochaete flavido‐alba
journal, December 1997
- Hamman, O. Ben; De La Rubia, T.; Martinez, J.
- Journal of Applied Microbiology, Vol. 83, Issue 6
Diverse Metabolic Capacities of Fungi for Bioremediation
journal, April 2016
- Deshmukh, Radhika; Khardenavis, Anshuman A.; Purohit, Hemant J.
- Indian Journal of Microbiology, Vol. 56, Issue 3
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
Microprep protocol for extraction of DNA from tomato and other herbaceous plants
journal, September 1995
- Fulton, Theresa M.; Chunwongse, Julapark; Tanksley, Steven D.
- Plant Molecular Biology Reporter, Vol. 13, Issue 3
Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi
journal, June 2014
- Riley, Robert; Salamov, Asaf A.; Brown, Daren W.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 27
Living in a fungal world: impact of fungi on soil bacterial niche development
journal, September 2005
- Boer, Wietse de; Folman, Larissa B.; Summerbell, Richard C.
- FEMS Microbiology Reviews, Vol. 29, Issue 4
Production of Biosurfactants by Soil Fungi Isolated from the Amazon Forest
journal, January 2018
- Sena, Hellen Holanda; Sanches, Michele Alves; Rocha, Diego Fernando Silva
- International Journal of Microbiology, Vol. 2018
Untapped potential: exploiting fungi in bioremediation of hazardous chemicals
journal, February 2011
- Harms, Hauke; Schlosser, Dietmar; Wick, Lukas Y.
- Nature Reviews Microbiology, Vol. 9, Issue 3
Anaerobic Catabolism of Aromatic Compounds: a Genetic and Genomic View
journal, March 2009
- Carmona, M.; Zamarro, M. T.; Blazquez, B.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 1
Genome-scale model reconstruction of the methylotrophic yeast Ogataea polymorpha
text, January 2021
- Liebal, Ulf Winfried; Fabry, Brigida A.; Ravikrishnan, Aarthi
- RWTH Aachen University