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Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio

Aquatic organisms such as fish can accumulate high concentrations of arsenic (As), which has toxic effects on fish. However, whether the intestinal flora are involved in As damage to fish intestinal tissues and the underlying process are unclear. Common carp (Cyprinus carpio) were exposed to As (2.8...

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Autores principales: Shi, Xiaodan, Xu, Wei, Che, Xinghua, Cui, Jiawen, Shang, Xinchi, Teng, Xiaohua, Jia, Zhiying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10165157/
https://www.ncbi.nlm.nih.gov/pubmed/37168116
http://dx.doi.org/10.3389/fmicb.2023.1179397
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author Shi, Xiaodan
Xu, Wei
Che, Xinghua
Cui, Jiawen
Shang, Xinchi
Teng, Xiaohua
Jia, Zhiying
author_facet Shi, Xiaodan
Xu, Wei
Che, Xinghua
Cui, Jiawen
Shang, Xinchi
Teng, Xiaohua
Jia, Zhiying
author_sort Shi, Xiaodan
collection PubMed
description Aquatic organisms such as fish can accumulate high concentrations of arsenic (As), which has toxic effects on fish. However, whether the intestinal flora are involved in As damage to fish intestinal tissues and the underlying process are unclear. Common carp (Cyprinus carpio) were exposed to As (2.83 mg/L) in water for 30 days, and blood, muscle, intestine, and intestine samples were collected. Intestinal pathological sections were observed, and the lipopolysaccharide (LPS) levels in serum and the levels of As accumulation and tight junction-related factors in intestinal tissues were measured. The gut microbiota was analysed by 16S rRNA sequencing. The results showed that As treatment decreased the abundance of microbiota, increased the number of harmful bacteria, and decreased the number of beneficial bacteria in the intestine. In our experiment, the top 30 harmful and beneficial bacteria with the highest relative abundance were identified. Among the top 30 harmful and beneficial bacteria, As treatment resulted in a significant (P < 0.05) increase in harmful bacteria (such as Fusobacteriota, Bacteroidota (LPS-producing bacteria), Verrucomicrobiota, Bacteroides, Aeromonas, and Stenotrophomonas) and a significant (P < 0.05) decrease in beneficial bacteria (such as Actinobacteriota, Planctomycetota, Firmicutes, Reyranella, Akkermansia, and Pseudorhodobacter), which further demonstrated that As affects the abundance of intestinal flora. In addition, As exposure increased the LPS level in serum and the abundance of Bacteroidota (LPS-producing bacteria) in the intestine. Bacteroidota exhibits the six highest relative abundance at the phylum level, which indicates that LPS produced by Bacteroidota can increase the LPS level in serum. Additionally, the protein and gene levels of the tight junction markers ZO-1 and occludin in the intestine were reduced by As treatment, which further indicated that As exposure impaired the structural integrity of the intestine. In conclusion, the results obtained in our study indicate that the intestinal flora, LPS, and tight junctions participate in the impairment of the structural integrity of the common carp intestine resulting from As exposure.
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spelling pubmed-101651572023-05-09 Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio Shi, Xiaodan Xu, Wei Che, Xinghua Cui, Jiawen Shang, Xinchi Teng, Xiaohua Jia, Zhiying Front Microbiol Microbiology Aquatic organisms such as fish can accumulate high concentrations of arsenic (As), which has toxic effects on fish. However, whether the intestinal flora are involved in As damage to fish intestinal tissues and the underlying process are unclear. Common carp (Cyprinus carpio) were exposed to As (2.83 mg/L) in water for 30 days, and blood, muscle, intestine, and intestine samples were collected. Intestinal pathological sections were observed, and the lipopolysaccharide (LPS) levels in serum and the levels of As accumulation and tight junction-related factors in intestinal tissues were measured. The gut microbiota was analysed by 16S rRNA sequencing. The results showed that As treatment decreased the abundance of microbiota, increased the number of harmful bacteria, and decreased the number of beneficial bacteria in the intestine. In our experiment, the top 30 harmful and beneficial bacteria with the highest relative abundance were identified. Among the top 30 harmful and beneficial bacteria, As treatment resulted in a significant (P < 0.05) increase in harmful bacteria (such as Fusobacteriota, Bacteroidota (LPS-producing bacteria), Verrucomicrobiota, Bacteroides, Aeromonas, and Stenotrophomonas) and a significant (P < 0.05) decrease in beneficial bacteria (such as Actinobacteriota, Planctomycetota, Firmicutes, Reyranella, Akkermansia, and Pseudorhodobacter), which further demonstrated that As affects the abundance of intestinal flora. In addition, As exposure increased the LPS level in serum and the abundance of Bacteroidota (LPS-producing bacteria) in the intestine. Bacteroidota exhibits the six highest relative abundance at the phylum level, which indicates that LPS produced by Bacteroidota can increase the LPS level in serum. Additionally, the protein and gene levels of the tight junction markers ZO-1 and occludin in the intestine were reduced by As treatment, which further indicated that As exposure impaired the structural integrity of the intestine. In conclusion, the results obtained in our study indicate that the intestinal flora, LPS, and tight junctions participate in the impairment of the structural integrity of the common carp intestine resulting from As exposure. Frontiers Media S.A. 2023-04-24 /pmc/articles/PMC10165157/ /pubmed/37168116 http://dx.doi.org/10.3389/fmicb.2023.1179397 Text en Copyright © 2023 Shi, Xu, Che, Cui, Shang, Teng and Jia. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Shi, Xiaodan
Xu, Wei
Che, Xinghua
Cui, Jiawen
Shang, Xinchi
Teng, Xiaohua
Jia, Zhiying
Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio
title Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio
title_full Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio
title_fullStr Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio
title_full_unstemmed Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio
title_short Effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of Cyprinus carpio
title_sort effect of arsenic stress on the intestinal structural integrity and intestinal flora abundance of cyprinus carpio
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10165157/
https://www.ncbi.nlm.nih.gov/pubmed/37168116
http://dx.doi.org/10.3389/fmicb.2023.1179397
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