Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective

Microplastics have emerged as a significant global concern, particularly in marine ecosystems. While extensive research has focused on the toxicological effects of microplastics on marine animals and/or their associated microorganisms as two separate entities, the holistic perspective of the adaptab...

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Main Authors: Xing-Lu Chen, Lin-Jun Wu, Li-Li Miao, Lei Li, Long-Mei Qiu, Hui-Qiang Zhu, Xi-Rui Si, Hong-Fei Li, Qiao-Ling Zhao, Peng-Zhi Qi, Ting-Ting Hou
Format: Article
Language:English
Published: Elsevier 2024-10-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324010376
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author Xing-Lu Chen
Lin-Jun Wu
Li-Li Miao
Lei Li
Long-Mei Qiu
Hui-Qiang Zhu
Xi-Rui Si
Hong-Fei Li
Qiao-Ling Zhao
Peng-Zhi Qi
Ting-Ting Hou
author_facet Xing-Lu Chen
Lin-Jun Wu
Li-Li Miao
Lei Li
Long-Mei Qiu
Hui-Qiang Zhu
Xi-Rui Si
Hong-Fei Li
Qiao-Ling Zhao
Peng-Zhi Qi
Ting-Ting Hou
author_sort Xing-Lu Chen
collection DOAJ
description Microplastics have emerged as a significant global concern, particularly in marine ecosystems. While extensive research has focused on the toxicological effects of microplastics on marine animals and/or their associated microorganisms as two separate entities, the holistic perspective of the adaptability and fitness of a marine animal metaorganism—comprising the animal host and its microbiome—remains largely unexplored. In this study, mussel metaorganisms subjected chronic PS-MPs exposure experienced acute mortality but rapidly adapted. We investigated the response of innate immunity, digestive enzymes and their associated microbiomes to chronic PS-MPs exposure. We found that PS-MPs directly and indirectly interacted with the host and microbe within the exposure system. The adaptation was a joint effort between the physiological adjustments of mussel host and genetic adaptation of its microbiome. The mussel hosts exhibited increased antioxidant activity, denser gill filaments and increased immune cells, enhancing their innate immunity. Concurrently, the gill microbiome and the digestive gland microbiome respective selectively enriched for plastic-degrading bacteria and particulate organic matter-utilizing bacteria, facilitating the microbiome’s adaptation. The microbial adaptation to chronic PS-MPs exposure altered the ecological roles of mussel microbiome, as evidenced by alterations in microbial interactions and nutrient cycling functions. These findings provided new insights into the ecotoxicological impact of microplastics on marine organisms from a metaorganism perspective.
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spelling doaj-art-6e3875acd8df4efb846bb6fe861cb4322025-08-20T01:54:44ZengElsevierEcotoxicology and Environmental Safety0147-65132024-10-0128411696110.1016/j.ecoenv.2024.116961Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspectiveXing-Lu Chen0Lin-Jun Wu1Li-Li Miao2Lei Li3Long-Mei Qiu4Hui-Qiang Zhu5Xi-Rui Si6Hong-Fei Li7Qiao-Ling Zhao8Peng-Zhi Qi9Ting-Ting Hou10National Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, ChinaState Key Laboratory of Microbial Resources, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, China; East China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Shanghai 200090, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, ChinaFishery College, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, ChinaZhoushan Institute for Food and Drug Control, Zhoushan, Zhejiang 316000, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, ChinaNational Engineering Research Center of Marine Facilities Aquaculture, Zhejiang Ocean University, Zhoushan, Zhejiang 316022, China; Corresponding author.Microplastics have emerged as a significant global concern, particularly in marine ecosystems. While extensive research has focused on the toxicological effects of microplastics on marine animals and/or their associated microorganisms as two separate entities, the holistic perspective of the adaptability and fitness of a marine animal metaorganism—comprising the animal host and its microbiome—remains largely unexplored. In this study, mussel metaorganisms subjected chronic PS-MPs exposure experienced acute mortality but rapidly adapted. We investigated the response of innate immunity, digestive enzymes and their associated microbiomes to chronic PS-MPs exposure. We found that PS-MPs directly and indirectly interacted with the host and microbe within the exposure system. The adaptation was a joint effort between the physiological adjustments of mussel host and genetic adaptation of its microbiome. The mussel hosts exhibited increased antioxidant activity, denser gill filaments and increased immune cells, enhancing their innate immunity. Concurrently, the gill microbiome and the digestive gland microbiome respective selectively enriched for plastic-degrading bacteria and particulate organic matter-utilizing bacteria, facilitating the microbiome’s adaptation. The microbial adaptation to chronic PS-MPs exposure altered the ecological roles of mussel microbiome, as evidenced by alterations in microbial interactions and nutrient cycling functions. These findings provided new insights into the ecotoxicological impact of microplastics on marine organisms from a metaorganism perspective.http://www.sciencedirect.com/science/article/pii/S0147651324010376MPsChronic exposureMetaorganismAdaptationMicrobiomeInnate immunity
spellingShingle Xing-Lu Chen
Lin-Jun Wu
Li-Li Miao
Lei Li
Long-Mei Qiu
Hui-Qiang Zhu
Xi-Rui Si
Hong-Fei Li
Qiao-Ling Zhao
Peng-Zhi Qi
Ting-Ting Hou
Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective
Ecotoxicology and Environmental Safety
MPs
Chronic exposure
Metaorganism
Adaptation
Microbiome
Innate immunity
title Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective
title_full Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective
title_fullStr Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective
title_full_unstemmed Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective
title_short Chronic polystyrene microplastics exposure-induced changes in thick-shell mussel (Mytilus coruscus) metaorganism: A holistic perspective
title_sort chronic polystyrene microplastics exposure induced changes in thick shell mussel mytilus coruscus metaorganism a holistic perspective
topic MPs
Chronic exposure
Metaorganism
Adaptation
Microbiome
Innate immunity
url http://www.sciencedirect.com/science/article/pii/S0147651324010376
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