Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species
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...
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American Society for Microbiology
2019
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oai:doaj.org-article:48c5dccecca94506aa764248267d2b942021-11-15T15:55:24ZCytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species10.1128/mBio.00558-192150-7511https://doaj.org/article/48c5dccecca94506aa764248267d2b942019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00558-19https://doaj.org/toc/2150-7511ABSTRACT 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.Erin M. Ostrem LossMi-Kyung LeeMing-Yueh WuJulia MartienWanping ChenDaniel Amador-NoguezColin JefcoateChristina RemucalSeunho JungSun-Chang KimJae-Hyuk YuAmerican Society for MicrobiologyarticleAspergillusbenzo[a]pyrenecatabolic enzyme systemcytochrome P450 monooxygenasepolycyclic aromatic hydrocarbonsvelvet regulatorsMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019) |
| institution |
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DOAJ |
| language |
EN |
| topic |
Aspergillus benzo[a]pyrene catabolic enzyme system cytochrome P450 monooxygenase polycyclic aromatic hydrocarbons velvet regulators Microbiology QR1-502 |
| spellingShingle |
Aspergillus benzo[a]pyrene catabolic enzyme system cytochrome P450 monooxygenase polycyclic aromatic hydrocarbons velvet regulators Microbiology QR1-502 Erin M. Ostrem Loss Mi-Kyung Lee Ming-Yueh Wu Julia Martien Wanping Chen Daniel Amador-Noguez Colin Jefcoate Christina Remucal Seunho Jung Sun-Chang Kim Jae-Hyuk Yu Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species |
| description |
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. |
| format |
article |
| author |
Erin M. Ostrem Loss Mi-Kyung Lee Ming-Yueh Wu Julia Martien Wanping Chen Daniel Amador-Noguez Colin Jefcoate Christina Remucal Seunho Jung Sun-Chang Kim Jae-Hyuk Yu |
| author_facet |
Erin M. Ostrem Loss Mi-Kyung Lee Ming-Yueh Wu Julia Martien Wanping Chen Daniel Amador-Noguez Colin Jefcoate Christina Remucal Seunho Jung Sun-Chang Kim Jae-Hyuk Yu |
| author_sort |
Erin M. Ostrem Loss |
| title |
Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species |
| title_short |
Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species |
| title_full |
Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species |
| title_fullStr |
Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species |
| title_full_unstemmed |
Cytochrome P450 Monooxygenase-Mediated Metabolic Utilization of Benzo[<italic toggle="yes">a</italic>]Pyrene by <italic toggle="yes">Aspergillus</italic> Species |
| title_sort |
cytochrome p450 monooxygenase-mediated metabolic utilization of benzo[<italic toggle="yes">a</italic>]pyrene by <italic toggle="yes">aspergillus</italic> species |
| publisher |
American Society for Microbiology |
| publishDate |
2019 |
| url |
https://doaj.org/article/48c5dccecca94506aa764248267d2b94 |
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