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Tributyl phosphate can inhibit the feeding behavior of rotifers by altering the axoneme structure, neuronal coordination and energy supply required for motile cilia

Organophosphorus flame retardants (OPFRs) are frequently detected in aquatic environments and can potentially amplify the food chain, posing a potential risk to organisms. Marine invertebrates have primitive nervous systems to regulate behavior, but how they respond to OPFRs that are potentially neu...

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Published in:Journal of hazardous materials 2023-10, Vol.459, p.132224-132224, Article 132224
Main Authors: Zhang, Xin, Tang, Xuexi, Yang, Yingying, Tong, Xin, Hu, Hanwen, Zhang, Xinxin
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cited_by cdi_FETCH-LOGICAL-c365t-a8b853139fb771e3b5140d2bea24487025cf1019aa725a2851f6547ca08483ac3
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creator Zhang, Xin
Tang, Xuexi
Yang, Yingying
Tong, Xin
Hu, Hanwen
Zhang, Xinxin
description Organophosphorus flame retardants (OPFRs) are frequently detected in aquatic environments and can potentially amplify the food chain, posing a potential risk to organisms. Marine invertebrates have primitive nervous systems to regulate behavior, but how they respond to OPFRs that are potentially neurotoxic substances is unclear. This study assessed changes in the feeding behavior of rotifer Brachionus plicatilis exposed to alkyl OPFRs tributyl phosphate (TnBP) (0.376 nM, 3.76 and 22.53 µM) to elucidate the mechanism of behavioral toxicity. TnBP at 22.53 μM reduced the ingestion and filtration rates of rotifers for Chlorella vulgaris and Phaeocystis globosa in a 24-h test and altered rotifer-P. globosa population dynamics in 15-d coculture. Ciliary beat frequency was also reduced, and the expression of genes encoding the cilia axoneme was downregulated. TnBP could inhibit rotifer acetylcholinesterase activity by binding this protein and reduce the expression of the exocytotic membrane protein syntaxin-4, suggesting a disorder in nervous regulation of cilia beat. Moreover, TnBP induced abnormal shape and dysfunction of mitochondria, which caused insufficient energy required for ciliary movement. This study revealed diverse neurotoxicity mechanisms of TnBP, particularly as a potentially competing acetylcholinesterase ligand for aquatic invertebrates. Our research also provides a meaningful reference for OPFR-induced behavioral toxicity assessments. [Display omitted] •TnBP at environmental level reduced the control ability of rotifers over P. globosa.•The downregulation of some axonemal genes led to a slow CBF of rotifer.•TnBP could bind to the pocket of rotifer AChE protein and inhibited its activity.•TnBP inhibited the SNARE expression of B. plicatilis.•TnBP interfered with the mitochondrial dynamics and autophagy of rotifer.
doi_str_mv 10.1016/j.jhazmat.2023.132224
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Marine invertebrates have primitive nervous systems to regulate behavior, but how they respond to OPFRs that are potentially neurotoxic substances is unclear. This study assessed changes in the feeding behavior of rotifer Brachionus plicatilis exposed to alkyl OPFRs tributyl phosphate (TnBP) (0.376 nM, 3.76 and 22.53 µM) to elucidate the mechanism of behavioral toxicity. TnBP at 22.53 μM reduced the ingestion and filtration rates of rotifers for Chlorella vulgaris and Phaeocystis globosa in a 24-h test and altered rotifer-P. globosa population dynamics in 15-d coculture. Ciliary beat frequency was also reduced, and the expression of genes encoding the cilia axoneme was downregulated. TnBP could inhibit rotifer acetylcholinesterase activity by binding this protein and reduce the expression of the exocytotic membrane protein syntaxin-4, suggesting a disorder in nervous regulation of cilia beat. 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[Display omitted] •TnBP at environmental level reduced the control ability of rotifers over P. globosa.•The downregulation of some axonemal genes led to a slow CBF of rotifer.•TnBP could bind to the pocket of rotifer AChE protein and inhibited its activity.•TnBP inhibited the SNARE expression of B. plicatilis.•TnBP interfered with the mitochondrial dynamics and autophagy of rotifer.</description><identifier>ISSN: 0304-3894</identifier><identifier>EISSN: 1873-3336</identifier><identifier>DOI: 10.1016/j.jhazmat.2023.132224</identifier><identifier>PMID: 37557041</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Cilia ; Feeding suppression ; Marine zooplankton ; Neurotoxicity ; Organophosphorus flame retardant</subject><ispartof>Journal of hazardous materials, 2023-10, Vol.459, p.132224-132224, Article 132224</ispartof><rights>2023</rights><rights>Copyright © 2023. 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subjects Cilia
Feeding suppression
Marine zooplankton
Neurotoxicity
Organophosphorus flame retardant
title Tributyl phosphate can inhibit the feeding behavior of rotifers by altering the axoneme structure, neuronal coordination and energy supply required for motile cilia
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