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MBio. 2019 May 28;10(3). pii: e00558-19. doi: 10.1128/mBio.00558-19.

Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[a]Pyrene by Aspergillus Species.

Author information

1
Molecular and Environmental Toxicology Center, University of Wisconsin-Madison, Madison, Wisconsin, USA.
2
Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejon, Republic of Korea.
3
Department of Bacteriology, University of Wisconsin-Madison, Madison, Wisconsin, USA.
4
College of Food Science and Technology, Huazhong Agricultural University, Wuhan, People's Republic of China.
5
Department of Civil and Environmental Engineering, University of Wisconsin-Madison, Madison, Wisconsin, USA.
6
Department of Systems Biotechnology, Konkuk University, Seoul, Republic of Korea.
7
Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejon, Republic of Korea.
8
Molecular and Environmental Toxicology Center, University of Wisconsin-Madison, Madison, Wisconsin, USA jyu1@wisc.edu.

Abstract

Soil-dwelling fungal species possess the versatile metabolic capability to degrade complex organic compounds that are toxic to humans, yet the mechanisms they employ remain largely unknown. Benzo[a]pyrene (BaP) is a pervasive carcinogenic contaminant, posing a significant concern for human health. Here, we report that several Aspergillus species are capable of degrading BaP. Exposing Aspergillus nidulans cells to BaP results in transcriptomic and metabolic changes associated with cellular growth and energy generation, implying that the fungus utilizes BaP as a growth substrate. Importantly, we identify and characterize the conserved bapA gene encoding a cytochrome P450 monooxygenase that is necessary for the metabolic utilization of BaP in Aspergillus We further demonstrate that the fungal NF-κB-type velvet regulators VeA and VelB are required for proper expression of bapA in response to nutrient limitation and BaP degradation in A. nidulans Our study illuminates fundamental knowledge of fungal BaP metabolism and provides novel insights into enhancing bioremediation potential.IMPORTANCE We are increasingly exposed to environmental pollutants, including the carcinogen benzo[a]pyrene (BaP), which has prompted extensive research into human metabolism of toxicants. However, little is known about metabolic mechanisms employed by fungi that are able to use some toxic pollutants as the substrates for growth, leaving innocuous by-products. This study systemically demonstrates that a common soil-dwelling fungus is able to use benzo[a]pyrene as food, which results in expression and metabolic changes associated with growth and energy generation. Importantly, this study reveals key components of the metabolic utilization of BaP, notably a cytochrome P450 monooxygenase and the fungal NF-κB-type transcriptional regulators. Our study advances fundamental knowledge of fungal BaP metabolism and provides novel insight into designing and implementing enhanced bioremediation strategies.

KEYWORDS:

Aspergillus; benzo[a]pyrene; bioremediation; catabolic enzyme system; cytochrome P450 monooxygenase; genome-wide expression; high-performance liquid chromatography; metabolomics; molecular genetics; polycyclic aromatic hydrocarbons; velvet regulators

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