Tris(1,3-dichloro-2-propyl) phosphate causes female-biased growth inhibition in zebrafish: Linked with gut microbiota dysbiosis

•TDCIPP could selectively inhibited the growth of female zebrafish.•TDCIPP altered the microbial communities in the intestine of zebrafish.•TDCIPP induced an increase in α-diversity of the gut microbiome in male zebrafish.•TDCIPP induced histological injury and inflammation responses in female intes...

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Published inAquatic toxicology Vol. 260; p. 106585
Main Authors Sun, Wen, Dang, Yao, Dai, Lili, Liu, Chunsheng, Wang, Jianghua, Guo, Yongyong, Fan, Boya, Kong, Juan, Zhou, Bingsheng, Ma, Xufa, Yu, Liqin
Format Journal Article
LanguageEnglish
Published Netherlands Elsevier B.V 01.07.2023
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Abstract •TDCIPP could selectively inhibited the growth of female zebrafish.•TDCIPP altered the microbial communities in the intestine of zebrafish.•TDCIPP induced an increase in α-diversity of the gut microbiome in male zebrafish.•TDCIPP induced histological injury and inflammation responses in female intestine.•Abundances of pathogenic bacteria were negatively correlated with female growth. Tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) is ubiquitous in aquatic environment, but its effect on intestinal health of fish has yet not been investigated. In the present study, the AB strain zebrafish embryos were exposed to environmentally realistic concentrations (0, 30, 300, and 3000 ng·L−1) of TDCIPP for 90 days, after which the fish growth and physiological activities were evaluated, and the intestinal microbes were analyzed by 16S rRNA gene high-throughput sequencing. Our results manifested that the body length and body weight were significantly reduced in the female zebrafish but not in males. Further analyses revealed that TDCIPP resulted in notable histological injury of intestine, which was accompanied by impairment of epithelial barrier integrity (decreased tight junction protein 2), inflammation responses (increased interleukin 1β), and disruption of neurotransmission (increased serotonin) in female intestine. Male intestines maintained intact intestinal structure, and the remarkably increased activity of glutathione peroxidase (GPx) might protect the male zebrafish from inflammation and intestinal damage. Furthermore, 16S rRNA sequencing analysis showed that TDCIPP significantly altered the microbial communities in the intestine in a gender-specific manner, with a remarkable increase in alpha diversity of the gut microbiome in male zebrafish, which might be another mechanism for male fish to protect their intestines from damage by TDCIPP. Correlation analysis revealed that abnormal abundances of pathogenic bacteria (Chryseobacterium, Enterococcus, and Legionella) might be partially responsible for the impaired epithelial barrier integrity and inhibition in female zebrafish growth. Taken together, our study for the first time demonstrates the high susceptibility of intestinal health and gut microbiota of zebrafish to TDCIPP, especially for female zebrafish, which could be partially responsible for the female-biased growth inhibition.
AbstractList •TDCIPP could selectively inhibited the growth of female zebrafish.•TDCIPP altered the microbial communities in the intestine of zebrafish.•TDCIPP induced an increase in α-diversity of the gut microbiome in male zebrafish.•TDCIPP induced histological injury and inflammation responses in female intestine.•Abundances of pathogenic bacteria were negatively correlated with female growth. Tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) is ubiquitous in aquatic environment, but its effect on intestinal health of fish has yet not been investigated. In the present study, the AB strain zebrafish embryos were exposed to environmentally realistic concentrations (0, 30, 300, and 3000 ng·L−1) of TDCIPP for 90 days, after which the fish growth and physiological activities were evaluated, and the intestinal microbes were analyzed by 16S rRNA gene high-throughput sequencing. Our results manifested that the body length and body weight were significantly reduced in the female zebrafish but not in males. Further analyses revealed that TDCIPP resulted in notable histological injury of intestine, which was accompanied by impairment of epithelial barrier integrity (decreased tight junction protein 2), inflammation responses (increased interleukin 1β), and disruption of neurotransmission (increased serotonin) in female intestine. Male intestines maintained intact intestinal structure, and the remarkably increased activity of glutathione peroxidase (GPx) might protect the male zebrafish from inflammation and intestinal damage. Furthermore, 16S rRNA sequencing analysis showed that TDCIPP significantly altered the microbial communities in the intestine in a gender-specific manner, with a remarkable increase in alpha diversity of the gut microbiome in male zebrafish, which might be another mechanism for male fish to protect their intestines from damage by TDCIPP. Correlation analysis revealed that abnormal abundances of pathogenic bacteria (Chryseobacterium, Enterococcus, and Legionella) might be partially responsible for the impaired epithelial barrier integrity and inhibition in female zebrafish growth. Taken together, our study for the first time demonstrates the high susceptibility of intestinal health and gut microbiota of zebrafish to TDCIPP, especially for female zebrafish, which could be partially responsible for the female-biased growth inhibition.
Tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) is ubiquitous in aquatic environment, but its effect on intestinal health of fish has yet not been investigated. In the present study, the AB strain zebrafish embryos were exposed to environmentally realistic concentrations (0, 30, 300, and 3000 ng·L ) of TDCIPP for 90 days, after which the fish growth and physiological activities were evaluated, and the intestinal microbes were analyzed by 16S rRNA gene high-throughput sequencing. Our results manifested that the body length and body weight were significantly reduced in the female zebrafish but not in males. Further analyses revealed that TDCIPP resulted in notable histological injury of intestine, which was accompanied by impairment of epithelial barrier integrity (decreased tight junction protein 2), inflammation responses (increased interleukin 1β), and disruption of neurotransmission (increased serotonin) in female intestine. Male intestines maintained intact intestinal structure, and the remarkably increased activity of glutathione peroxidase (GPx) might protect the male zebrafish from inflammation and intestinal damage. Furthermore, 16S rRNA sequencing analysis showed that TDCIPP significantly altered the microbial communities in the intestine in a gender-specific manner, with a remarkable increase in alpha diversity of the gut microbiome in male zebrafish, which might be another mechanism for male fish to protect their intestines from damage by TDCIPP. Correlation analysis revealed that abnormal abundances of pathogenic bacteria (Chryseobacterium, Enterococcus, and Legionella) might be partially responsible for the impaired epithelial barrier integrity and inhibition in female zebrafish growth. Taken together, our study for the first time demonstrates the high susceptibility of intestinal health and gut microbiota of zebrafish to TDCIPP, especially for female zebrafish, which could be partially responsible for the female-biased growth inhibition.
ArticleNumber 106585
Author Dai, Lili
Guo, Yongyong
Dang, Yao
Fan, Boya
Zhou, Bingsheng
Wang, Jianghua
Liu, Chunsheng
Kong, Juan
Ma, Xufa
Yu, Liqin
Sun, Wen
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  surname: Zhou
  fullname: Zhou, Bingsheng
  organization: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430070, China
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  surname: Ma
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  email: xufama@mail.hzau.edu.cn
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  organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China
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CitedBy_id crossref_primary_10_1016_j_scitotenv_2024_174248
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Keywords Gut microbiota
TCP
DMSO
OTUs
OPFR
Zebrafish growth
PERMANOVA
TnBP
QA
QC
ANOVA
BSI
GSI
GSH
Intestinal health
HSI
TDCIPP
EROD
Environmental concentration
H&E
SOD
IL-1β
GPx
PCA
CAT
PCP
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TCEP
ELISA
TJP2
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Snippet •TDCIPP could selectively inhibited the growth of female zebrafish.•TDCIPP altered the microbial communities in the intestine of zebrafish.•TDCIPP induced an...
Tris(1,3-dichloro-2-propyl) phosphate (TDCIPP) is ubiquitous in aquatic environment, but its effect on intestinal health of fish has yet not been investigated....
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StartPage 106585
SubjectTerms Environmental concentration
Gut microbiota
Intestinal health
TDCIPP
Zebrafish growth
Title Tris(1,3-dichloro-2-propyl) phosphate causes female-biased growth inhibition in zebrafish: Linked with gut microbiota dysbiosis
URI https://dx.doi.org/10.1016/j.aquatox.2023.106585
https://www.ncbi.nlm.nih.gov/pubmed/37247575
https://search.proquest.com/docview/2820971882
Volume 260
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