Enantioselective disruption of circadian rhythm behavior in goldfish (Carassius auratus) induced by chiral fungicide triadimefon at environmentally-relevant concentration

Linjia Liu; Liuqingqing Liu; Zixi Yuan; Wenting Zhao; Liyan Huang; Xianxiang Luo; Fengmin Li; Hao Zheng

doi:10.1016/j.jhazmat.2024.136891

Enantioselective disruption of circadian rhythm behavior in goldfish (Carassius auratus) induced by chiral fungicide triadimefon at environmentally-relevant concentration

J Hazard Mater. 2024 Dec 15:485:136891. doi: 10.1016/j.jhazmat.2024.136891. Online ahead of print.

Authors

Linjia Liu¹, Liuqingqing Liu², Zixi Yuan¹, Wenting Zhao¹, Liyan Huang¹, Xianxiang Luo³, Fengmin Li³, Hao Zheng⁴

Affiliations

¹ Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ocean University of China, Qingdao 266100, China.
² Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ocean University of China, Qingdao 266100, China. Electronic address: llqq@ouc.edu.cn.
³ Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ocean University of China, Qingdao 266100, China; Sanya Oceanographic Institution, Ocean University of China, Sanya 57200, China.
⁴ Institute of Coastal Environmental Pollution Control, College of Environmental Science and Engineering, Key Laboratory of Marine Environment and Ecology, Ocean University of China, Qingdao 266100, China; Sanya Oceanographic Institution, Ocean University of China, Sanya 57200, China. Electronic address: zhenghao2013@ouc.edu.cn.

PMID: 39708603
DOI: 10.1016/j.jhazmat.2024.136891

Abstract

The pollution of triadimefon (TDF) fungicides significantly hinders the "One Health" frame achievement. However, the enantioselective effects of chiral TDF on the circadian rhythm of fish remained unclear. Herein, TDF enantiomers (R(-)-TDF and S(+)-TDF) and racemic Rac-TDF were selected to investigate their enantioselective effects and mechanisms on circadian rhythm of goldfish (Carassius auratus) at an environmentally-relevant concentration (100 µg L⁻¹). S(+)-TDF reduced the diurnal-nocturnal differences in schooling behavior more strongly than R(-)-TDF, proving the enantioselectively weakened circadian rhythm of goldfish by TDF. S(+)-TDF more preferentially bioaccumulated in goldfish than R(-)-TDF, mainly contributed to the enantioselectively disrupted circadian rhythm. On one hand, TDF enantiomers in brains differentially inhibited neuronal activity, leading to cholinergic system dysfunction. On the other hand, TDF enantiomers in intestines differentially disrupted intestinal barriers, thus potentially dysregulating the "brain-gut" axis. Importantly, the commercial probiotics alleviated the behavioral disorder, indirectly confirming that the dysbiosis of intestinal bacteria contributed to the TDF-induced circadian rhythm disruption. These findings provide novel insights into the enantioselective disruption of fish circadian rhythm behaviors by chiral fungicides at enantiomer levels, and offer novel strategies for early assessing the ecological risks of chiral agrochemicals in aquatic ecosystems.

Keywords: Brain-gut axis; Chiral fungicides; Circadian rhythm; Enantiomers; Triadimefon.