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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Main Authors: Zeeshan Ali, Ijaz Khan, Muhammad Shahid Iqbal, Haitao Shi, Li Ding, Meiling Hong
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325000594
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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.
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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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