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Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments

Steroidal oestrogens are often accumulated in urban estuarine sediments worldwide at microgram per gram levels. These aromatic steroids have been classified as endocrine disruptors and group 1 carcinogens. Microbial degradation is a naturally occurring mechanism that mineralizes oestrogens in the bi...

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Autores principales: Hsiao, Tsun‐Hsien, Chen, Yi‐Lung, Meng, Menghsiao, Chuang, Meng‐Rong, Horinouchi, Masae, Hayashi, Toshiaki, Wang, Po‐Hsiang, Chiang, Yin‐Ru
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8085986/
https://www.ncbi.nlm.nih.gov/pubmed/33764689
http://dx.doi.org/10.1111/1751-7915.13798
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author Hsiao, Tsun‐Hsien
Chen, Yi‐Lung
Meng, Menghsiao
Chuang, Meng‐Rong
Horinouchi, Masae
Hayashi, Toshiaki
Wang, Po‐Hsiang
Chiang, Yin‐Ru
author_facet Hsiao, Tsun‐Hsien
Chen, Yi‐Lung
Meng, Menghsiao
Chuang, Meng‐Rong
Horinouchi, Masae
Hayashi, Toshiaki
Wang, Po‐Hsiang
Chiang, Yin‐Ru
author_sort Hsiao, Tsun‐Hsien
collection PubMed
description Steroidal oestrogens are often accumulated in urban estuarine sediments worldwide at microgram per gram levels. These aromatic steroids have been classified as endocrine disruptors and group 1 carcinogens. Microbial degradation is a naturally occurring mechanism that mineralizes oestrogens in the biosphere; however, the corresponding genes in oestrogen‐degrading actinobacteria remain unidentified. In this study, we identified a gene cluster encoding several putative oestrogen‐degrading genes (aed; actinobacterial oestrogen degradation) in actinobacterium Rhodococcus sp. strain B50. Among them, the aedA and aedB genes involved in oestrogenic A‐ring cleavage were identified through gene‐disruption experiments. We demonstrated that actinobacterial oestrone 4‐hydroxylase (AedA) is a cytochrome P450‐type monooxygenase. We also detected the accumulation of two extracellular oestrogenic metabolites, including pyridinestrone acid (PEA) and 3aα‐H‐4α(3'‐propanoate)‐7aβ‐methylhexahydro‐1,5‐indanedione (HIP), in the oestrone‐fed strain B50 cultures. Since actinobacterial aedB and proteobacterial edcB shared < 40% sequence identity, 4‐hydroxyestrone 4,5‐dioxygenase genes (namely aedB and edcB) could serve as a specific biomarker to differentiate the contribution of actinobacteria and proteobacteria in environmental oestrogen degradation. Therefore, 4‐hydroxyestrone 4,5‐dioxygenase genes and the extracellular metabolites PEA and HIP were used as biomarkers to investigate oestrogen biodegradation in an urban estuarine sediment. Interestingly, our data suggested that actinobacteria are active oestrogen degraders in the urban estuarine sediment.
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spelling pubmed-80859862021-05-07 Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments Hsiao, Tsun‐Hsien Chen, Yi‐Lung Meng, Menghsiao Chuang, Meng‐Rong Horinouchi, Masae Hayashi, Toshiaki Wang, Po‐Hsiang Chiang, Yin‐Ru Microb Biotechnol Research Articles Steroidal oestrogens are often accumulated in urban estuarine sediments worldwide at microgram per gram levels. These aromatic steroids have been classified as endocrine disruptors and group 1 carcinogens. Microbial degradation is a naturally occurring mechanism that mineralizes oestrogens in the biosphere; however, the corresponding genes in oestrogen‐degrading actinobacteria remain unidentified. In this study, we identified a gene cluster encoding several putative oestrogen‐degrading genes (aed; actinobacterial oestrogen degradation) in actinobacterium Rhodococcus sp. strain B50. Among them, the aedA and aedB genes involved in oestrogenic A‐ring cleavage were identified through gene‐disruption experiments. We demonstrated that actinobacterial oestrone 4‐hydroxylase (AedA) is a cytochrome P450‐type monooxygenase. We also detected the accumulation of two extracellular oestrogenic metabolites, including pyridinestrone acid (PEA) and 3aα‐H‐4α(3'‐propanoate)‐7aβ‐methylhexahydro‐1,5‐indanedione (HIP), in the oestrone‐fed strain B50 cultures. Since actinobacterial aedB and proteobacterial edcB shared < 40% sequence identity, 4‐hydroxyestrone 4,5‐dioxygenase genes (namely aedB and edcB) could serve as a specific biomarker to differentiate the contribution of actinobacteria and proteobacteria in environmental oestrogen degradation. Therefore, 4‐hydroxyestrone 4,5‐dioxygenase genes and the extracellular metabolites PEA and HIP were used as biomarkers to investigate oestrogen biodegradation in an urban estuarine sediment. Interestingly, our data suggested that actinobacteria are active oestrogen degraders in the urban estuarine sediment. John Wiley and Sons Inc. 2021-03-25 /pmc/articles/PMC8085986/ /pubmed/33764689 http://dx.doi.org/10.1111/1751-7915.13798 Text en © 2021 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Hsiao, Tsun‐Hsien
Chen, Yi‐Lung
Meng, Menghsiao
Chuang, Meng‐Rong
Horinouchi, Masae
Hayashi, Toshiaki
Wang, Po‐Hsiang
Chiang, Yin‐Ru
Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
title Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
title_full Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
title_fullStr Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
title_full_unstemmed Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
title_short Mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
title_sort mechanistic and phylogenetic insights into actinobacteria‐mediated oestrogen biodegradation in urban estuarine sediments
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8085986/
https://www.ncbi.nlm.nih.gov/pubmed/33764689
http://dx.doi.org/10.1111/1751-7915.13798
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