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 in | Aquatic toxicology Vol. 260; p. 106585 |
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Main Authors | , , , , , , , , , , |
Format | Journal Article |
Language | English |
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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. |
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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 |
Author_xml | – sequence: 1 givenname: Wen surname: Sun fullname: Sun, Wen organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China – sequence: 2 givenname: Yao surname: Dang fullname: Dang, Yao organization: State Environmental Protection Key Laboratory of Environmental Pollution Health Risk Assessment, South China Institute of Environmental Sciences, Ministry of Ecology and Environment, Guangzhou 510655, China – sequence: 3 givenname: Lili surname: Dai fullname: Dai, Lili organization: Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430073, China – sequence: 4 givenname: Chunsheng surname: Liu fullname: Liu, Chunsheng organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China – sequence: 5 givenname: Jianghua surname: Wang fullname: Wang, Jianghua organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China – sequence: 6 givenname: Yongyong surname: Guo fullname: Guo, Yongyong organization: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430070, China – sequence: 7 givenname: Boya surname: Fan fullname: Fan, Boya organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China – sequence: 8 givenname: Juan surname: Kong fullname: Kong, Juan organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China – sequence: 9 givenname: Bingsheng surname: Zhou fullname: Zhou, Bingsheng organization: Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430070, China – sequence: 10 givenname: Xufa surname: Ma fullname: Ma, Xufa email: xufama@mail.hzau.edu.cn organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China – sequence: 11 givenname: Liqin orcidid: 0000-0002-5308-8494 surname: Yu fullname: Yu, Liqin email: yuliqin@mail.hzau.edu.cn organization: College of Fisheries, Huazhong Agricultural University, Wuhan 430070, China |
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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 5-HT 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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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 |
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