Harnessing microbial phylum-specific molecular markers for assessment of environmental estrogen degradation

Tsun-Hsien Hsiao; Po-Hao Chen; Po-Hsiang Wang; Guo-Jie Brandon-Mong; Chen-Wei Li; Masae Horinouchi; Toshiaki Hayashi; Wael Ismail; Menghsiao Meng; Yi-Lung Chen; Yin-Ru Chiang

doi:10.1016/j.scitotenv.2023.165152

Harnessing microbial phylum-specific molecular markers for assessment of environmental estrogen degradation

Sci Total Environ. 2023 Oct 20:896:165152. doi: 10.1016/j.scitotenv.2023.165152. Epub 2023 Jun 28.

Authors

Affiliations

¹ Biodiversity Research Center, Academia Sinica, Taipei, 115, Taiwan.
² Department of Microbiology, Soochow University, Taipei, 111, Taiwan.
³ Graduate Institute of Environmental Engineering, National Central University, Taoyuan, 320, Taiwan; Department of Chemical and Materials Engineering, National Central University, Taoyuan, 320, Taiwan.
⁴ Condensed Molecular Materials Laboratory, RIKEN, Saitama, 351-0198, Japan.
⁵ Environmental Molecular Biology Laboratory, RIKEN, Saitama, 351-0198, Japan.
⁶ Environmental Biotechnology Program, Life Sciences Department, College of Graduate Studies, Arabian Gulf University, Manama, Bahrain.
⁷ Graduate Institute of Biotechnology, National Chung Hsing University, Taichung 402, Taiwan.
⁸ Department of Microbiology, Soochow University, Taipei, 111, Taiwan. Electronic address: yilungchen@scu.edu.tw.
⁹ Biodiversity Research Center, Academia Sinica, Taipei, 115, Taiwan; Department of Agricultural Chemistry, National Taiwan University, Taipei 106, Taiwan. Electronic address: yinru915@gate.sinica.edu.tw.

PMID: 37391160
DOI: 10.1016/j.scitotenv.2023.165152

Abstract

Steroidal estrogens are ubiquitous contaminants that have garnered attention worldwide due to their endocrine-disrupting and carcinogenic activities at sub-nanomolar concentrations. Microbial degradation is one of the main mechanisms through which estrogens can be removed from the environment. Numerous bacteria have been isolated and identified as estrogen degraders; however, little is known about their contribution to environmental estrogen removal. Here, our global metagenomic analysis indicated that estrogen degradation genes are widely distributed among bacteria, especially among aquatic actinobacterial and proteobacterial species. Thus, by using the Rhodococcus sp. strain B50 as the model organism, we identified three actinobacteria-specific estrogen degradation genes, namely aedGHJ, by performing gene disruption experiments and metabolite profile analysis. Among these genes, the product of aedJ was discovered to mediate the conjugation of coenzyme A with a unique actinobacterial C₁₇ estrogenic metabolite, 5-oxo-4-norestrogenic acid. However, proteobacteria were found to exclusively adopt an α-oxoacid ferredoxin oxidoreductase (i.e., the product of edcC) to degrade a proteobacterial C₁₈ estrogenic metabolite, namely 3-oxo-4,5-seco-estrogenic acid. We employed actinobacterial aedJ and proteobacterial edcC as specific biomarkers for quantitative polymerase chain reaction (qPCR) to elucidate the potential of microbes for estrogen biodegradation in contaminated ecosystems. The results indicated that aedJ was more abundant than edcC in most environmental samples. Our results greatly expand the understanding of environmental estrogen degradation. Moreover, our study suggests that qPCR-based functional assays are a simple, cost-effective, and rapid approach for holistically evaluating estrogen biodegradation in the environment.

Keywords: Actinobacteria; Coenzyme A ligase; Endocrine-disrupting chemicals; Estrogen biodegradation; Proteobacteria; α-oxoacid ferredoxin oxidoreductase.

MeSH terms

Bacteria / metabolism
Biodegradation, Environmental
Ecosystem*
Estrogens* / metabolism
Estrone / metabolism
Proteobacteria / genetics

Substances

Estrogens
Estrone