Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination

Global-scale crop contamination with environmental estrogens has posed a huge risk to agri-food safety and human health. Laccase is regarded as an unexceptionable biocatalyst for regulating pollution and expediting humification, but the knowledge of estrogen bioremediation and C storage strengthened...

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Main Authors: Xuemin Qi, Ziyan Niu, Shenghua Xiao, Michael Gatheru Waigi, Hui Lin, Kai Sun
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412024001624
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author Xuemin Qi
Ziyan Niu
Shenghua Xiao
Michael Gatheru Waigi
Hui Lin
Kai Sun
author_facet Xuemin Qi
Ziyan Niu
Shenghua Xiao
Michael Gatheru Waigi
Hui Lin
Kai Sun
author_sort Xuemin Qi
collection DOAJ
description Global-scale crop contamination with environmental estrogens has posed a huge risk to agri-food safety and human health. Laccase is regarded as an unexceptionable biocatalyst for regulating pollution and expediting humification, but the knowledge of estrogen bioremediation and C storage strengthened by laccase-driven rhizosphere humification (LDRH) remains largely unknown. Herein, a greenhouse microcosm was performed to explore the migration and fate of 17β-estradiol (E2) in water-wheat (Triticum aestivum L.) matrices by LDRH. Compared to the non-added laccase, the pseudo-first-order decay rate constants of E2 in the rhizosphere solution after 10 and 50 μM exposures by LDRH increased from 0.03 and 0.02 h−1 to 0.36 and 0.09 h−1, respectively. Furthermore, LDRH conferred higher yield, polymerizability, O-containing groups, and functional-C signals in the humified precipitates, because it accelerated the formation of highly complex precipitates by radical-controlled continuous polymerization. In particular, not only did LDRH mitigate the phytotoxicity of E2, but it also diminished the metabolic load of E2 in wheat tissues. This was attributed to the rapid attenuation of E2 in the rhizosphere solution during LDRH, which limited E2 uptake and accumulation in each subcellular fraction of the wheat roots and shoots. Although several typical intermediate products such as estrone, estriol, and E2 oligomers were detected in roots, only small-molecule species were found in shoots, evidencing that the polymeric products of E2 were unable to be translocated acropetally due to the vast hydrophobicity and biounavailability. For the first time, our study highlights a novel, eco-friendly, and sustainable candidate for increasing the low-C treatment of organics in rhizosphere microenvironments and alleviating the potential risks of estrogenic contaminants in agroenvironments.
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spelling doaj.art-475a10ff2f47456690e0baa2b60dc9852024-03-23T06:22:25ZengElsevierEnvironment International0160-41202024-03-01185108576Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contaminationXuemin Qi0Ziyan Niu1Shenghua Xiao2Michael Gatheru Waigi3Hui Lin4Kai Sun5Anhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, ChinaAnhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, ChinaCollege of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, ChinaResearch Center for Eco-Environmental Engineering, Dongguan University of Technology, Dongguan 523808, ChinaAnhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, China; CAS Key Laboratory of Urban Pollutant Conversion, Department of Environmental Science and Engineering, University of Science and Technology of China, Hefei 230026, China; Corresponding author at: Anhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, College of Resources and Environment, Anhui Agricultural University, Hefei 230036, China.Global-scale crop contamination with environmental estrogens has posed a huge risk to agri-food safety and human health. Laccase is regarded as an unexceptionable biocatalyst for regulating pollution and expediting humification, but the knowledge of estrogen bioremediation and C storage strengthened by laccase-driven rhizosphere humification (LDRH) remains largely unknown. Herein, a greenhouse microcosm was performed to explore the migration and fate of 17β-estradiol (E2) in water-wheat (Triticum aestivum L.) matrices by LDRH. Compared to the non-added laccase, the pseudo-first-order decay rate constants of E2 in the rhizosphere solution after 10 and 50 μM exposures by LDRH increased from 0.03 and 0.02 h−1 to 0.36 and 0.09 h−1, respectively. Furthermore, LDRH conferred higher yield, polymerizability, O-containing groups, and functional-C signals in the humified precipitates, because it accelerated the formation of highly complex precipitates by radical-controlled continuous polymerization. In particular, not only did LDRH mitigate the phytotoxicity of E2, but it also diminished the metabolic load of E2 in wheat tissues. This was attributed to the rapid attenuation of E2 in the rhizosphere solution during LDRH, which limited E2 uptake and accumulation in each subcellular fraction of the wheat roots and shoots. Although several typical intermediate products such as estrone, estriol, and E2 oligomers were detected in roots, only small-molecule species were found in shoots, evidencing that the polymeric products of E2 were unable to be translocated acropetally due to the vast hydrophobicity and biounavailability. For the first time, our study highlights a novel, eco-friendly, and sustainable candidate for increasing the low-C treatment of organics in rhizosphere microenvironments and alleviating the potential risks of estrogenic contaminants in agroenvironments.http://www.sciencedirect.com/science/article/pii/S0160412024001624Environmental estrogensLaccase-driven rhizosphere humificationC storageWheat seedlingsUptake and transportation
spellingShingle Xuemin Qi
Ziyan Niu
Shenghua Xiao
Michael Gatheru Waigi
Hui Lin
Kai Sun
Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination
Environment International
Environmental estrogens
Laccase-driven rhizosphere humification
C storage
Wheat seedlings
Uptake and transportation
title Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination
title_full Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination
title_fullStr Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination
title_full_unstemmed Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination
title_short Novel insights into the mechanism of laccase-driven rhizosphere humification for alleviating wheat 17β-estradiol contamination
title_sort novel insights into the mechanism of laccase driven rhizosphere humification for alleviating wheat 17β estradiol contamination
topic Environmental estrogens
Laccase-driven rhizosphere humification
C storage
Wheat seedlings
Uptake and transportation
url http://www.sciencedirect.com/science/article/pii/S0160412024001624
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