Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio)
Abstract Background Many studies have investigated how nanoplastics (NPs) exposure mediates nerve and intestinal toxicity through a dysregulated brain-gut axis interaction, but there are few studies aimed at alleviating those effects. To determine whether and how vitamin D can impact that toxicity,...
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Format: | Article |
Language: | English |
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BMC
2023-11-01
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Series: | Microbiome |
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Online Access: | https://doi.org/10.1186/s40168-023-01680-1 |
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author | Miaomiao Teng Yunxia Li Xiaoli Zhao Jason C. White Lihui Zhao Jiaqi Sun Wentao Zhu Fengchang Wu |
author_facet | Miaomiao Teng Yunxia Li Xiaoli Zhao Jason C. White Lihui Zhao Jiaqi Sun Wentao Zhu Fengchang Wu |
author_sort | Miaomiao Teng |
collection | DOAJ |
description | Abstract Background Many studies have investigated how nanoplastics (NPs) exposure mediates nerve and intestinal toxicity through a dysregulated brain-gut axis interaction, but there are few studies aimed at alleviating those effects. To determine whether and how vitamin D can impact that toxicity, fish were supplemented with a vitamin D-low diet and vitamin D-high diet. Results Transmission electron microscopy (TEM) showed that polystyrene nanoplastics (PS-NPs) accumulated in zebrafish brain and intestine, resulting in brain blood–brain barrier basement membrane damage and the vacuolization of intestinal goblet cells and mitochondria. A high concentration of vitamin D reduced the accumulation of PS-NPs in zebrafish brain tissues by 20% and intestinal tissues by 58.8% and 52.2%, respectively, and alleviated the pathological damage induced by PS-NPs. Adequate vitamin D significantly increased the content of serotonin (5-HT) and reduced the anxiety-like behavior of zebrafish caused by PS-NPs exposure. Virus metagenome showed that PS-NPs exposure affected the composition and abundance of zebrafish intestinal viruses. Differentially expressed viruses in the vitamin D-low and vitamin D-high group affected the secretion of brain neurotransmitters in zebrafish. Virus AF191073 was negatively correlated with neurotransmitter 5-HT, whereas KT319643 was positively correlated with malondialdehyde (MDA) content and the expression of cytochrome 1a1 (cyp1a1) and cytochrome 1b1 (cyp1b1) in the intestine. This suggests that AF191073 and KT319643 may be key viruses that mediate the vitamin D reduction in neurotoxicity and immunotoxicity induced by PS-NPs. Conclusion Vitamin D can alleviate neurotoxicity and immunotoxicity induced by PS-NPs exposure by directionally altering the gut virome. These findings highlight the potential of vitamin D to alleviate the brain-gut-virome disorder caused by PS-NPs exposure and suggest potential therapeutic strategies to reduce the risk of NPs toxicity in aquaculture, that is, adding adequate vitamin D to diet. Video Abstract |
first_indexed | 2024-03-09T05:32:56Z |
format | Article |
id | doaj.art-1dcdaecb567842cb8a9f49edbbf8503b |
institution | Directory Open Access Journal |
issn | 2049-2618 |
language | English |
last_indexed | 2024-03-09T05:32:56Z |
publishDate | 2023-11-01 |
publisher | BMC |
record_format | Article |
series | Microbiome |
spelling | doaj.art-1dcdaecb567842cb8a9f49edbbf8503b2023-12-03T12:30:24ZengBMCMicrobiome2049-26182023-11-0111111510.1186/s40168-023-01680-1Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio)Miaomiao Teng0Yunxia Li1Xiaoli Zhao2Jason C. White3Lihui Zhao4Jiaqi Sun5Wentao Zhu6Fengchang Wu7State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental SciencesState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental SciencesState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental SciencesThe Connecticut Agricultural Experiment StationState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental SciencesSchool of Energy and Environmental Engineering, University of Science and Technology BeijingDepartment of Applied Chemistry, Innovation Center of Pesticide Research, College of Science, China Agricultural UniversityState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental SciencesAbstract Background Many studies have investigated how nanoplastics (NPs) exposure mediates nerve and intestinal toxicity through a dysregulated brain-gut axis interaction, but there are few studies aimed at alleviating those effects. To determine whether and how vitamin D can impact that toxicity, fish were supplemented with a vitamin D-low diet and vitamin D-high diet. Results Transmission electron microscopy (TEM) showed that polystyrene nanoplastics (PS-NPs) accumulated in zebrafish brain and intestine, resulting in brain blood–brain barrier basement membrane damage and the vacuolization of intestinal goblet cells and mitochondria. A high concentration of vitamin D reduced the accumulation of PS-NPs in zebrafish brain tissues by 20% and intestinal tissues by 58.8% and 52.2%, respectively, and alleviated the pathological damage induced by PS-NPs. Adequate vitamin D significantly increased the content of serotonin (5-HT) and reduced the anxiety-like behavior of zebrafish caused by PS-NPs exposure. Virus metagenome showed that PS-NPs exposure affected the composition and abundance of zebrafish intestinal viruses. Differentially expressed viruses in the vitamin D-low and vitamin D-high group affected the secretion of brain neurotransmitters in zebrafish. Virus AF191073 was negatively correlated with neurotransmitter 5-HT, whereas KT319643 was positively correlated with malondialdehyde (MDA) content and the expression of cytochrome 1a1 (cyp1a1) and cytochrome 1b1 (cyp1b1) in the intestine. This suggests that AF191073 and KT319643 may be key viruses that mediate the vitamin D reduction in neurotoxicity and immunotoxicity induced by PS-NPs. Conclusion Vitamin D can alleviate neurotoxicity and immunotoxicity induced by PS-NPs exposure by directionally altering the gut virome. These findings highlight the potential of vitamin D to alleviate the brain-gut-virome disorder caused by PS-NPs exposure and suggest potential therapeutic strategies to reduce the risk of NPs toxicity in aquaculture, that is, adding adequate vitamin D to diet. Video Abstracthttps://doi.org/10.1186/s40168-023-01680-1Polystyrene nanoplasticsVitamin DBrainVirusesZebrafish |
spellingShingle | Miaomiao Teng Yunxia Li Xiaoli Zhao Jason C. White Lihui Zhao Jiaqi Sun Wentao Zhu Fengchang Wu Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio) Microbiome Polystyrene nanoplastics Vitamin D Brain Viruses Zebrafish |
title | Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio) |
title_full | Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio) |
title_fullStr | Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio) |
title_full_unstemmed | Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio) |
title_short | Vitamin D modulation of brain-gut-virome disorder caused by polystyrene nanoplastics exposure in zebrafish (Danio rerio) |
title_sort | vitamin d modulation of brain gut virome disorder caused by polystyrene nanoplastics exposure in zebrafish danio rerio |
topic | Polystyrene nanoplastics Vitamin D Brain Viruses Zebrafish |
url | https://doi.org/10.1186/s40168-023-01680-1 |
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