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Title: 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 » 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.« less

Authors:
 [1];  [2];  [3];  [1];  [2];  [2];  [2];  [2];  [2];  [4];  [5];  [1];  [6];  [1]; ORCiD logo [1]
  1. Korea Univ., Seoul (South Korea)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Korea Research Inst., Seoul (South Korea)
  4. Oregon State Univ., Corvallis, OR (United States)
  5. Centre National de la Recherche, Paris (France); Univ. of Aix-Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  6. 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. 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, & 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}
}

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