Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis)
Copper is used to treat algal blooms, macrophyte infestations and other environmental issues, but its rising ambient levels harm aquatic animals, especially their intestines. However, its impact on turtles' digestive health is not well understood, and the risks are unclear. This study investiga...
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Elsevier
2025-01-01
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author | Zeeshan Ali Ijaz Khan Muhammad Shahid Iqbal Haitao Shi Li Ding Meiling Hong |
author_facet | Zeeshan Ali Ijaz Khan Muhammad Shahid Iqbal Haitao Shi Li Ding Meiling Hong |
author_sort | Zeeshan Ali |
collection | DOAJ |
description | Copper is used to treat algal blooms, macrophyte infestations and other environmental issues, but its rising ambient levels harm aquatic animals, especially their intestines. However, its impact on turtles' digestive health is not well understood, and the risks are unclear. This study investigates the effects of copper on the intestinal health of Chinese stripe-necked turtle, focusing on histomorphology, mucosal barrier function, gene expression, and gut microbiota. Copper stress caused intestinal damage, characterized by shortened villi, inflammatory cell infiltration, and reduced epithelial layer thickness, as well as decreased acidic mucins, increased villi edema and inflammation. The mRNA expression level of bacteriostatic enzymes significantly reduced. Furthermore, This study found that copper exposure increases gut permeability by suppressing tight junction genes and triggers an inflammatory response in the gut, as indicated by elevated inflammatory cytokines. At the phylum level, Firmicutes exhibited a significant decrease, whereas Bacteroidota displayed a notable increase, and Fusobacteriota showed a substantial reduction in relative abundance in copper-treated groups. Similarly, at genus level Romboutsia, Cetobacterium decreased, while Turicibacter and Sarcina significantly increases in copper-treated groups compared to the control. This indicating the unique properties of copper including its essentiality, reactivity, and accumulation enables it to profoundly impact gut bacteria, altering both their composition and function. Copper's dual role as a nutrient and toxicant uniquely impacts gut microbes. Our findings suggest that copper stress compromises the intestinal physical, immune, chemical, and microbial barrier in M. sinensis, all of which contribute to the turtle’s poor health. |
format | Article |
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institution | Kabale University |
issn | 0147-6513 |
language | English |
publishDate | 2025-01-01 |
publisher | Elsevier |
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series | Ecotoxicology and Environmental Safety |
spelling | doaj-art-f0dcef2935de4b718bb3042e0cadc9302025-02-12T05:30:05ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01290117723Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis)Zeeshan Ali0Ijaz Khan1Muhammad Shahid Iqbal2Haitao Shi3Li Ding4Meiling Hong5Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, ChinaMinistry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, ChinaCorresponding authors.; Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, ChinaCorresponding authors.; Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, ChinaCopper is used to treat algal blooms, macrophyte infestations and other environmental issues, but its rising ambient levels harm aquatic animals, especially their intestines. However, its impact on turtles' digestive health is not well understood, and the risks are unclear. This study investigates the effects of copper on the intestinal health of Chinese stripe-necked turtle, focusing on histomorphology, mucosal barrier function, gene expression, and gut microbiota. Copper stress caused intestinal damage, characterized by shortened villi, inflammatory cell infiltration, and reduced epithelial layer thickness, as well as decreased acidic mucins, increased villi edema and inflammation. The mRNA expression level of bacteriostatic enzymes significantly reduced. Furthermore, This study found that copper exposure increases gut permeability by suppressing tight junction genes and triggers an inflammatory response in the gut, as indicated by elevated inflammatory cytokines. At the phylum level, Firmicutes exhibited a significant decrease, whereas Bacteroidota displayed a notable increase, and Fusobacteriota showed a substantial reduction in relative abundance in copper-treated groups. Similarly, at genus level Romboutsia, Cetobacterium decreased, while Turicibacter and Sarcina significantly increases in copper-treated groups compared to the control. This indicating the unique properties of copper including its essentiality, reactivity, and accumulation enables it to profoundly impact gut bacteria, altering both their composition and function. Copper's dual role as a nutrient and toxicant uniquely impacts gut microbes. Our findings suggest that copper stress compromises the intestinal physical, immune, chemical, and microbial barrier in M. sinensis, all of which contribute to the turtle’s poor health.http://www.sciencedirect.com/science/article/pii/S0147651325000594Chinese stripe-necked turtleHeavy metal toxicityBioaccumulationAntioxidant systemApoptosisIntestinal microbiome |
spellingShingle | Zeeshan Ali Ijaz Khan Muhammad Shahid Iqbal Haitao Shi Li Ding Meiling Hong Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis) Ecotoxicology and Environmental Safety Chinese stripe-necked turtle Heavy metal toxicity Bioaccumulation Antioxidant system Apoptosis Intestinal microbiome |
title | Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis) |
title_full | Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis) |
title_fullStr | Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis) |
title_full_unstemmed | Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis) |
title_short | Impact of copper stress in the intestinal barriers and gut microbiota of Chinese stripe-necked turtle (Mauremys sinensis) |
title_sort | impact of copper stress in the intestinal barriers and gut microbiota of chinese stripe necked turtle mauremys sinensis |
topic | Chinese stripe-necked turtle Heavy metal toxicity Bioaccumulation Antioxidant system Apoptosis Intestinal microbiome |
url | http://www.sciencedirect.com/science/article/pii/S0147651325000594 |
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