Biotransformation of bisphenol A in vivo and in vitro by laccase-producing Trametes hirsuta La-7: Kinetics, products, and mechanisms

Jie Liu; Kai Sun; Rui Zhu; Xun Wang; Michael Gatheru Waigi; Shunyao Li

doi:10.1016/j.envpol.2023.121155

Biotransformation of bisphenol A in vivo and in vitro by laccase-producing Trametes hirsuta La-7: Kinetics, products, and mechanisms

Environ Pollut. 2023 Mar 15:321:121155. doi: 10.1016/j.envpol.2023.121155. Epub 2023 Jan 25.

Authors

Jie Liu¹, Kai Sun², Rui Zhu¹, Xun Wang¹, Michael Gatheru Waigi³, Shunyao Li⁴

Affiliations

¹ Anhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei, 230036, Anhui, China.
² Anhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei, 230036, Anhui, China; CAS Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei, 230026, Anhui, China. Electronic address: sunkai@ahau.edu.cn.
³ College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, Jiangsu, China.
⁴ Laboratory of Wetland Protection and Ecological Restoration, Anhui University, Hefei, 230601, Anhui, China.

PMID: 36709035
DOI: 10.1016/j.envpol.2023.121155

Abstract

Bisphenol A (BPA) is a ubiquitous endocrine disruptor that poses adverse human health risks. Herein, biotransformation kinetics, products, and mechanisms of BPA undergoing a laccase-producing Trametes hirsuta La-7 metabolism were for the first time reported. Strain La-7 could completely biotransform ≤0.5 mmol·L^-1 BPA within 6 d in vivo. Notably, its extracellular crude laccase solution (ECLS) and intracellular homogenized mycelium (HM) only required 6 h to convert 85.71% and 84.24% of 0.5 mmol·L^-1 BPA in vitro, respectively. The removal of BPA was noticeably hampered by adding a cytochrome P-450 inhibitor (piperonyl butoxide) in HM, disclosing that cytochrome P-450 monooxygenase participated in BPA oxidation and metabolism. BPA intermediates were elaborately identified by high-resolution mass spectrometry (HRMS) combined with ¹³C stable isotope ratios (BPA: ¹³C₁₂-BPA = 0.25: 0.25, molar concentration). Based on the accurate molecular mass, isotope labeling difference, and relative intensity ratio of product peaks, 6 versatile metabolic mechanisms of BPA, including polymerization, hydroxylation, dehydration, bond cleavage, dehydrogenation, and carboxylation in vivo and in vitro, were confirmed. Germination index values revealed that inoculating strain La-7 in a BPA-contaminated medium presented no phytotoxicity to the germinated radish (Raphanus sativus L.) seeds. In vivo, Mg²⁺, Fe²⁺, Fe³⁺, and Mn²⁺ were conducive to BPA removal, but Cd²⁺ and Hg²⁺ significantly obstructed BPA elimination. Additionally, strain La-7 also exhibited high-efficiency metabolic ability toward estrone (E1), 17β-estradiol (E2), and 17α-ethinylestradiol (EE2), with more than 96.13%, 96.65%, and 100% of E1, E2, and EE2 having been converted, respectively. Our findings provide an environmentally powerful laccase-producing fungus to decontaminate endocrine disruptor-contaminated water matrices by radical polymerization and oxidative decomposition.

Keywords: BPA biotransformation; HRMS combined With (13)C(12)-labeling; Laccase-producing strain La-7; Metabolic mechanisms; Phytotoxicity.

MeSH terms

Benzhydryl Compounds / metabolism
Benzhydryl Compounds / toxicity
Biotransformation
Endocrine Disruptors* / metabolism
Endocrine Disruptors* / toxicity
Humans
Laccase* / metabolism
Trametes / metabolism

Substances

bisphenol A
Laccase
Endocrine Disruptors
Benzhydryl Compounds

Supplementary concepts

Trametes hirsuta