Negative impacts of chronic dietary exposure to polyethylene microplastics on growth, gut microbiota, liver metabolism and gene expressions in genetically improved farmed tilapia (Oreochromis niloticus)

Microplastics (MPs) pollution has been recognized as a threat to sustainable fisheries due to the concerns of MPs contamination in fish feed production and susceptibility to ingestion of MPs from the aquaculture environment. Here, we report a comprehensive investigation about the impacts of dietary...

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Veröffentlicht in:The Science of the total environment 2022-06, p.156571, Article 156571
Hauptverfasser: Lu, Xing, Zhang, Jie-Xin, Zhang, Lang, Wu, Di, Tian, Juan, Yu, Li-Juan, He, Li, Zhong, Shan, Du, Hao, Deng, Dong-Fang, Ding, Yong-Zhen, Wen, Hua, Jiang, Ming
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creator Lu, Xing
Zhang, Jie-Xin
Zhang, Lang
Wu, Di
Tian, Juan
Yu, Li-Juan
He, Li
Zhong, Shan
Du, Hao
Deng, Dong-Fang
Ding, Yong-Zhen
Wen, Hua
Jiang, Ming
description Microplastics (MPs) pollution has been recognized as a threat to sustainable fisheries due to the concerns of MPs contamination in fish feed production and susceptibility to ingestion of MPs from the aquaculture environment. Here, we report a comprehensive investigation about the impacts of dietary exposure to polyethylene microplastics (PE-MPs) for 9 weeks on growth performance, gut microbiota, liver metabolism, and gene expressions in brain and liver of the genetically improved farmed tilapia (GIFT, Oreochromis niloticus). Dietary exposure to two kinds of PE-MPs with different median size (27 μm and 63 μm, respectively) concentration-dependently decreased weight gain (WG), while increased feed conversion ratio (FCR) and hepatosomatic index (HSI) of the tilapia. Dietary administration of PE-MPs also significantly reduced the activities of intestinal protease and amylase. PE-MPs particles of the larger size groups (63 μm) were mainly detected in feces, but those of the smaller ones (27 μm) tended to be accumulated in intestine. PE-MPs ingestion altered the gut microbiota composition, and Fusobacteria, Verrucomicrobia and Firmicutes were the overrepresented bacterial taxa. Metabolomic assays of liver samples in fish fed the diets containing 8 % of 27 μm and 63 μm PE-MPs revealed the particle size-specific variations in composition of differential metabolites, and pathways such as amino acid and glycerophospholipid metabolism were affected by dietary PE-MPs exposure. Gene expressions of brain and liver samples were analyzed by RNA-seq. Photoperiodism and circadian rhythm were the representative biological processes enriched for the differentially expressed genes (DEGs) identified from the brain. Citrate cycle (TCA cycle) was the most enriched pathway revealed by a joint transcriptomic and metabolic pathway analysis for the liver, followed by propanoate and pyruvate metabolism. Furthermore, an integration analysis of the gut microbiome and liver transcriptome data identified significant associations between several pathogenic bacteria taxa and immune pathways. Our data systematically cataloged the adverse impacts of chronic exposure to PE-MPs on physiology and metabolism of GIFT tilapia. [Display omitted] •Chronic dietary exposure to PE-MPs depressed growth and intestinal digested enzymes in GIFT tilapia.•Exposed to PE-MPs increased Fusobacteria and decreased Verrucomicrobia abundance in tilapia gut.•PE-MPs-regulated genes involved in circadian rhythm were id
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Here, we report a comprehensive investigation about the impacts of dietary exposure to polyethylene microplastics (PE-MPs) for 9 weeks on growth performance, gut microbiota, liver metabolism, and gene expressions in brain and liver of the genetically improved farmed tilapia (GIFT, Oreochromis niloticus). Dietary exposure to two kinds of PE-MPs with different median size (27 μm and 63 μm, respectively) concentration-dependently decreased weight gain (WG), while increased feed conversion ratio (FCR) and hepatosomatic index (HSI) of the tilapia. Dietary administration of PE-MPs also significantly reduced the activities of intestinal protease and amylase. PE-MPs particles of the larger size groups (63 μm) were mainly detected in feces, but those of the smaller ones (27 μm) tended to be accumulated in intestine. PE-MPs ingestion altered the gut microbiota composition, and Fusobacteria, Verrucomicrobia and Firmicutes were the overrepresented bacterial taxa. Metabolomic assays of liver samples in fish fed the diets containing 8 % of 27 μm and 63 μm PE-MPs revealed the particle size-specific variations in composition of differential metabolites, and pathways such as amino acid and glycerophospholipid metabolism were affected by dietary PE-MPs exposure. Gene expressions of brain and liver samples were analyzed by RNA-seq. Photoperiodism and circadian rhythm were the representative biological processes enriched for the differentially expressed genes (DEGs) identified from the brain. Citrate cycle (TCA cycle) was the most enriched pathway revealed by a joint transcriptomic and metabolic pathway analysis for the liver, followed by propanoate and pyruvate metabolism. Furthermore, an integration analysis of the gut microbiome and liver transcriptome data identified significant associations between several pathogenic bacteria taxa and immune pathways. Our data systematically cataloged the adverse impacts of chronic exposure to PE-MPs on physiology and metabolism of GIFT tilapia. [Display omitted] •Chronic dietary exposure to PE-MPs depressed growth and intestinal digested enzymes in GIFT tilapia.•Exposed to PE-MPs increased Fusobacteria and decreased Verrucomicrobia abundance in tilapia gut.•PE-MPs-regulated genes involved in circadian rhythm were identified in tilapia brain.•PE-MPs ingestion disturbed liver citrate cycle at both transcriptome and metabolome level.•Correlations were identified between pathogenic gut bacteria and liver immune pathways.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2022.156571</identifier><identifier>PMID: 35688245</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Dietary exposure ; Gene expressions ; Growth ; Gut microbiota ; Metabolism ; Polyethylene microplastics ; Tilapia</subject><ispartof>The Science of the total environment, 2022-06, p.156571, Article 156571</ispartof><rights>2021</rights><rights>Copyright © 2021. 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Metabolomic assays of liver samples in fish fed the diets containing 8 % of 27 μm and 63 μm PE-MPs revealed the particle size-specific variations in composition of differential metabolites, and pathways such as amino acid and glycerophospholipid metabolism were affected by dietary PE-MPs exposure. Gene expressions of brain and liver samples were analyzed by RNA-seq. Photoperiodism and circadian rhythm were the representative biological processes enriched for the differentially expressed genes (DEGs) identified from the brain. Citrate cycle (TCA cycle) was the most enriched pathway revealed by a joint transcriptomic and metabolic pathway analysis for the liver, followed by propanoate and pyruvate metabolism. Furthermore, an integration analysis of the gut microbiome and liver transcriptome data identified significant associations between several pathogenic bacteria taxa and immune pathways. Our data systematically cataloged the adverse impacts of chronic exposure to PE-MPs on physiology and metabolism of GIFT tilapia. [Display omitted] •Chronic dietary exposure to PE-MPs depressed growth and intestinal digested enzymes in GIFT tilapia.•Exposed to PE-MPs increased Fusobacteria and decreased Verrucomicrobia abundance in tilapia gut.•PE-MPs-regulated genes involved in circadian rhythm were identified in tilapia brain.•PE-MPs ingestion disturbed liver citrate cycle at both transcriptome and metabolome level.•Correlations were identified between pathogenic gut bacteria and liver immune pathways.</description><subject>Dietary exposure</subject><subject>Gene expressions</subject><subject>Growth</subject><subject>Gut microbiota</subject><subject>Metabolism</subject><subject>Polyethylene microplastics</subject><subject>Tilapia</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNo9kcGO0zAQhi0EYsvCK8AcQdoW26kT57hawYK0Yi97txxn0k7lxJHtFvqKPBXOFvBlZHvmm1__z9gHwTeCi_rzYZMc5ZBxOm0kl3IjVK0a8YKthG7ateCyfslWnG_1uq3b5oq9SenAy2m0eM2uKlVrLbdqxX7_wJ3NdEKgcbYuJwgDuH0MEznoCbONZ8Bfc0jHiJADzMGfMe_PHieEkVwMs7cpkyuTE-xi-Jn3N7A75stnRyHbG_BlQ4Sx4LrgKY1gpx52C6KwI6ZEYUpA0_NbgVnvz4uiGE7Yw2DjWEomb2ey8PExYlg0jpRgIh_KwDF9esteDdYnfPe3XrOnr1-e7r6tHx7vv9_dPqxRC1XsaLgSsueD7sTWDoNyonK6XHDQfWN13UqlBt6gVa2wle6dkEJ3UtYVl-iqa_b-gp2PXVFl5khjMcn887Q03F4asIg4EUZTssLJYU8RXTZ9ICO4WXI0B_M_R7PkaC45Vn8A7W2Zew</recordid><startdate>20220607</startdate><enddate>20220607</enddate><creator>Lu, Xing</creator><creator>Zhang, Jie-Xin</creator><creator>Zhang, Lang</creator><creator>Wu, Di</creator><creator>Tian, Juan</creator><creator>Yu, Li-Juan</creator><creator>He, Li</creator><creator>Zhong, Shan</creator><creator>Du, Hao</creator><creator>Deng, Dong-Fang</creator><creator>Ding, Yong-Zhen</creator><creator>Wen, Hua</creator><creator>Jiang, Ming</creator><general>Elsevier B.V</general><scope>NPM</scope></search><sort><creationdate>20220607</creationdate><title>Negative impacts of chronic dietary exposure to polyethylene microplastics on growth, gut microbiota, liver metabolism and gene expressions in genetically improved farmed tilapia (Oreochromis niloticus)</title><author>Lu, Xing ; Zhang, Jie-Xin ; Zhang, Lang ; Wu, Di ; Tian, Juan ; Yu, Li-Juan ; He, Li ; Zhong, Shan ; Du, Hao ; Deng, Dong-Fang ; Ding, Yong-Zhen ; Wen, Hua ; Jiang, Ming</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-e815-9670512d0f8b14aff5c13c88b1ef8d7a869255f07ea591a38dc1218b226302ec3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Dietary exposure</topic><topic>Gene expressions</topic><topic>Growth</topic><topic>Gut microbiota</topic><topic>Metabolism</topic><topic>Polyethylene microplastics</topic><topic>Tilapia</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lu, Xing</creatorcontrib><creatorcontrib>Zhang, Jie-Xin</creatorcontrib><creatorcontrib>Zhang, Lang</creatorcontrib><creatorcontrib>Wu, Di</creatorcontrib><creatorcontrib>Tian, Juan</creatorcontrib><creatorcontrib>Yu, Li-Juan</creatorcontrib><creatorcontrib>He, Li</creatorcontrib><creatorcontrib>Zhong, Shan</creatorcontrib><creatorcontrib>Du, Hao</creatorcontrib><creatorcontrib>Deng, Dong-Fang</creatorcontrib><creatorcontrib>Ding, Yong-Zhen</creatorcontrib><creatorcontrib>Wen, Hua</creatorcontrib><creatorcontrib>Jiang, Ming</creatorcontrib><collection>PubMed</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lu, Xing</au><au>Zhang, Jie-Xin</au><au>Zhang, Lang</au><au>Wu, Di</au><au>Tian, Juan</au><au>Yu, Li-Juan</au><au>He, Li</au><au>Zhong, Shan</au><au>Du, Hao</au><au>Deng, Dong-Fang</au><au>Ding, Yong-Zhen</au><au>Wen, Hua</au><au>Jiang, Ming</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Negative impacts of chronic dietary exposure to polyethylene microplastics on growth, gut microbiota, liver metabolism and gene expressions in genetically improved farmed tilapia (Oreochromis niloticus)</atitle><jtitle>The Science of the total environment</jtitle><addtitle>Sci Total Environ</addtitle><date>2022-06-07</date><risdate>2022</risdate><spage>156571</spage><pages>156571-</pages><artnum>156571</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Microplastics (MPs) pollution has been recognized as a threat to sustainable fisheries due to the concerns of MPs contamination in fish feed production and susceptibility to ingestion of MPs from the aquaculture environment. Here, we report a comprehensive investigation about the impacts of dietary exposure to polyethylene microplastics (PE-MPs) for 9 weeks on growth performance, gut microbiota, liver metabolism, and gene expressions in brain and liver of the genetically improved farmed tilapia (GIFT, Oreochromis niloticus). Dietary exposure to two kinds of PE-MPs with different median size (27 μm and 63 μm, respectively) concentration-dependently decreased weight gain (WG), while increased feed conversion ratio (FCR) and hepatosomatic index (HSI) of the tilapia. Dietary administration of PE-MPs also significantly reduced the activities of intestinal protease and amylase. PE-MPs particles of the larger size groups (63 μm) were mainly detected in feces, but those of the smaller ones (27 μm) tended to be accumulated in intestine. PE-MPs ingestion altered the gut microbiota composition, and Fusobacteria, Verrucomicrobia and Firmicutes were the overrepresented bacterial taxa. Metabolomic assays of liver samples in fish fed the diets containing 8 % of 27 μm and 63 μm PE-MPs revealed the particle size-specific variations in composition of differential metabolites, and pathways such as amino acid and glycerophospholipid metabolism were affected by dietary PE-MPs exposure. Gene expressions of brain and liver samples were analyzed by RNA-seq. Photoperiodism and circadian rhythm were the representative biological processes enriched for the differentially expressed genes (DEGs) identified from the brain. Citrate cycle (TCA cycle) was the most enriched pathway revealed by a joint transcriptomic and metabolic pathway analysis for the liver, followed by propanoate and pyruvate metabolism. Furthermore, an integration analysis of the gut microbiome and liver transcriptome data identified significant associations between several pathogenic bacteria taxa and immune pathways. Our data systematically cataloged the adverse impacts of chronic exposure to PE-MPs on physiology and metabolism of GIFT tilapia. [Display omitted] •Chronic dietary exposure to PE-MPs depressed growth and intestinal digested enzymes in GIFT tilapia.•Exposed to PE-MPs increased Fusobacteria and decreased Verrucomicrobia abundance in tilapia gut.•PE-MPs-regulated genes involved in circadian rhythm were identified in tilapia brain.•PE-MPs ingestion disturbed liver citrate cycle at both transcriptome and metabolome level.•Correlations were identified between pathogenic gut bacteria and liver immune pathways.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>35688245</pmid><doi>10.1016/j.scitotenv.2022.156571</doi></addata></record>
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source ScienceDirect Journals (5 years ago - present)
subjects Dietary exposure
Gene expressions
Growth
Gut microbiota
Metabolism
Polyethylene microplastics
Tilapia
title Negative impacts of chronic dietary exposure to polyethylene microplastics on growth, gut microbiota, liver metabolism and gene expressions in genetically improved farmed tilapia (Oreochromis niloticus)
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