TY - JOUR
T1 - Transcriptomic analysis reveals the endocrine toxicity of tributyltin and triphenyltin on the whelk Reishia clavigera and mechanisms of imposex formation
AU - Chi-Ho Ip, Jack
AU - T. Y. Leung, Priscilla
AU - K. Y. Ho, Kevin
AU - Qiu, Jian Wen
AU - M. Y. Leung, Kenneth
N1 - This work was substantially supported by the Research Grants Council of the Hong Kong SAR Government via two grants of the General Research Fund (Project no.: HKU 771212 M and 11307121). PTY Leung was supported by the State Key Laboratory of Marine Pollution (SKLMP), City University of Hong Kong. SKLMP receives regular research funding from Innovation and Technology Commission (ITC) of the HKSAR Government.
Copyright © 2024 The Authors. Published by Elsevier Ltd.. All rights reserved.
PY - 2024/8
Y1 - 2024/8
N2 - Organotin compounds (OTs) are endocrine disruptors that induce imposex in hundreds of gastropods, but little is known about their underlying molecular mechanisms. This study aimed to investigate the endocrine toxicity and molecular responses to tributyltin (TBT) and triphenyltin (TPT) exposure in the whelk Reishia clavigera, which often serves as a biomonitor for OT contamination. Over a 120-day exposure to environmentally relevant concentrations of TBT (1000 ng L-1) and TPT (500 ng L-1), we observed a significant increase in penis length in both male and female whelks. Notably, TPT exhibited a stronger potency in inducing pseudo-penis development and female sterility, even at a half dose of TBT. Bioaccumulation analysis also revealed higher persistence and accumulation of TPT in whelk tissues compared to TBT. Differential expression analysis identified a substantial number of differentially expressed genes (DEGs), with TPT exposure eliciting more DEGs than TBT. Our results demonstrated that OTs induced xenobiotic metabolism and metabolic dysregulation in the digestive gland, impaired multiple cellular functions and triggered neurotoxicity in the nervous system, and disrupted lipid homeostasis and oxidative stress in the gonads. Furthermore, imposex was possibly associated with disturbances in retinoic acid metabolism, nuclear receptor signaling, and neuropeptide activity. When compared to TBT, TPT exhibited a more pronounced endocrine-disrupting effect, attributable to its higher bioaccumulation and substantial interruption of transcriptional regulation, OT detoxification, and biosynthesis of retinoic acids in R. clavigera. Our results, therefore, highlight the importance of considering the differences in bioaccumulation and molecular toxicity between TBT and TPT in future risk assessments of these contaminants. Overall, our study provided molecular insights into the toxicity and transcriptome profiles in R. clavigera exposed to TBT and TPT, shedding light on the endocrine-disrupting effects and reproductive impairment in female gastropods.
AB - Organotin compounds (OTs) are endocrine disruptors that induce imposex in hundreds of gastropods, but little is known about their underlying molecular mechanisms. This study aimed to investigate the endocrine toxicity and molecular responses to tributyltin (TBT) and triphenyltin (TPT) exposure in the whelk Reishia clavigera, which often serves as a biomonitor for OT contamination. Over a 120-day exposure to environmentally relevant concentrations of TBT (1000 ng L-1) and TPT (500 ng L-1), we observed a significant increase in penis length in both male and female whelks. Notably, TPT exhibited a stronger potency in inducing pseudo-penis development and female sterility, even at a half dose of TBT. Bioaccumulation analysis also revealed higher persistence and accumulation of TPT in whelk tissues compared to TBT. Differential expression analysis identified a substantial number of differentially expressed genes (DEGs), with TPT exposure eliciting more DEGs than TBT. Our results demonstrated that OTs induced xenobiotic metabolism and metabolic dysregulation in the digestive gland, impaired multiple cellular functions and triggered neurotoxicity in the nervous system, and disrupted lipid homeostasis and oxidative stress in the gonads. Furthermore, imposex was possibly associated with disturbances in retinoic acid metabolism, nuclear receptor signaling, and neuropeptide activity. When compared to TBT, TPT exhibited a more pronounced endocrine-disrupting effect, attributable to its higher bioaccumulation and substantial interruption of transcriptional regulation, OT detoxification, and biosynthesis of retinoic acids in R. clavigera. Our results, therefore, highlight the importance of considering the differences in bioaccumulation and molecular toxicity between TBT and TPT in future risk assessments of these contaminants. Overall, our study provided molecular insights into the toxicity and transcriptome profiles in R. clavigera exposed to TBT and TPT, shedding light on the endocrine-disrupting effects and reproductive impairment in female gastropods.
KW - Biocide
KW - Imposex mechanisms
KW - Neogastropods
KW - Organotin
KW - Reproductive impairment
KW - Transcriptome
UR - http://www.scopus.com/inward/record.url?scp=85197403653&partnerID=8YFLogxK
U2 - 10.1016/j.envint.2024.108867
DO - 10.1016/j.envint.2024.108867
M3 - Journal article
C2 - 38968833
AN - SCOPUS:85197403653
SN - 0160-4120
VL - 190
JO - Environment International
JF - Environment International
M1 - 108867
ER -