The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach

Marine microplastics pollution is a major environmental concern in marine ecosystems worldwide, yet the biological impacts of microplastics on the coastal biota are not yet fully understood. We investigated the impact of suspended microplastics on the energy budget of the mussels Mytilus coruscus us...

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Main Authors: Yueyong Shang, Xinghuo Wang, Xueqing Chang, Inna M. Sokolova, Shuaishuai Wei, Wei Liu, James K. H. Fang, Menghong Hu, Wei Huang, Youji Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Marine Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2021.754789/full
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author Yueyong Shang
Yueyong Shang
Xinghuo Wang
Xinghuo Wang
Xueqing Chang
Xueqing Chang
Inna M. Sokolova
Inna M. Sokolova
Shuaishuai Wei
Shuaishuai Wei
Wei Liu
James K. H. Fang
Menghong Hu
Menghong Hu
Wei Huang
Wei Huang
Youji Wang
Youji Wang
Youji Wang
author_facet Yueyong Shang
Yueyong Shang
Xinghuo Wang
Xinghuo Wang
Xueqing Chang
Xueqing Chang
Inna M. Sokolova
Inna M. Sokolova
Shuaishuai Wei
Shuaishuai Wei
Wei Liu
James K. H. Fang
Menghong Hu
Menghong Hu
Wei Huang
Wei Huang
Youji Wang
Youji Wang
Youji Wang
author_sort Yueyong Shang
collection DOAJ
description Marine microplastics pollution is a major environmental concern in marine ecosystems worldwide, yet the biological impacts of microplastics on the coastal biota are not yet fully understood. We investigated the impact of suspended microplastics on the energy budget of the mussels Mytilus coruscus using the Cellular Energy Allocation (CEA) approach. The mussels were exposed to control conditions (no microplastics) or to one of the three concentrations of 2 μm polystyrene microspheres (10, 104, and 106 particles/L) for 14 days, followed by 7 days of recovery. Exposure to high concentrations of microplastics (104 or 106 particles/L) increased cellular energy demand (measured as the activity of the mitochondrial electron transport system, ETS) and depleted cellular energy stores (carbohydrates, lipids, and proteins) in the mussels whereas exposure to 10 particles/L had no effect. Carbohydrate levels decreased already after 7 days of microplastics exposure and were restored after 7 days of recovery. In contrast, the tissue levels of lipids and proteins declined more slowly (after 14 days of exposure) and did not fully recover after 7 days following the removal of microplastics. Therefore, the total energy content and the CEA declined after 7–14 days of exposure to high microplastics concentrations, and remained suppressed during 7 days of subsequent recovery. These findings demonstrate a negative impact of microplastics on energy metabolism at the cellular level that cannot be restored during a short time recovery. Given a close link of CEA with the organismal energy balance, suppression of CEA by microplastics exposure suggests that bioenergetics disturbances might lead to decreases in growth and productivity of mussels’ populations in environments with heavy microplastics loads.
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spelling doaj.art-fb69c9e210954b88baaf4a34d5a7e0fe2022-12-21T22:11:43ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452021-09-01810.3389/fmars.2021.754789754789The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation ApproachYueyong Shang0Yueyong Shang1Xinghuo Wang2Xinghuo Wang3Xueqing Chang4Xueqing Chang5Inna M. Sokolova6Inna M. Sokolova7Shuaishuai Wei8Shuaishuai Wei9Wei Liu10James K. H. Fang11Menghong Hu12Menghong Hu13Wei Huang14Wei Huang15Youji Wang16Youji Wang17Youji Wang18International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaDepartment of Marine Biology, Institute for Biological Sciences, University of Rostock, Rostock, GermanyDepartment of Maritime Systems, Interdisciplinary Faculty, University of Rostock, Rostock, GermanyInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaDepartment F.-A. Forel for Environmental and Aquatic Sciences, Environmental Biogeochemistry and Ecotoxicology, Faculty of Sciences, Earth and Environment Sciences, University of Geneva, Geneva, SwitzerlandDepartment of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Kowloon, Hong KongInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaState Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaKey Laboratory of Marine Ecosystem Dynamics, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaInternational Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai, ChinaState Key Laboratory of Satellite Ocean Environment Dynamics, Second Institute of Oceanography, Ministry of Natural Resources, Hangzhou, ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai, ChinaMarine microplastics pollution is a major environmental concern in marine ecosystems worldwide, yet the biological impacts of microplastics on the coastal biota are not yet fully understood. We investigated the impact of suspended microplastics on the energy budget of the mussels Mytilus coruscus using the Cellular Energy Allocation (CEA) approach. The mussels were exposed to control conditions (no microplastics) or to one of the three concentrations of 2 μm polystyrene microspheres (10, 104, and 106 particles/L) for 14 days, followed by 7 days of recovery. Exposure to high concentrations of microplastics (104 or 106 particles/L) increased cellular energy demand (measured as the activity of the mitochondrial electron transport system, ETS) and depleted cellular energy stores (carbohydrates, lipids, and proteins) in the mussels whereas exposure to 10 particles/L had no effect. Carbohydrate levels decreased already after 7 days of microplastics exposure and were restored after 7 days of recovery. In contrast, the tissue levels of lipids and proteins declined more slowly (after 14 days of exposure) and did not fully recover after 7 days following the removal of microplastics. Therefore, the total energy content and the CEA declined after 7–14 days of exposure to high microplastics concentrations, and remained suppressed during 7 days of subsequent recovery. These findings demonstrate a negative impact of microplastics on energy metabolism at the cellular level that cannot be restored during a short time recovery. Given a close link of CEA with the organismal energy balance, suppression of CEA by microplastics exposure suggests that bioenergetics disturbances might lead to decreases in growth and productivity of mussels’ populations in environments with heavy microplastics loads.https://www.frontiersin.org/articles/10.3389/fmars.2021.754789/fullmicroplasticenergy statuscellular energy allocationenergy metabolismmussel
spellingShingle Yueyong Shang
Yueyong Shang
Xinghuo Wang
Xinghuo Wang
Xueqing Chang
Xueqing Chang
Inna M. Sokolova
Inna M. Sokolova
Shuaishuai Wei
Shuaishuai Wei
Wei Liu
James K. H. Fang
Menghong Hu
Menghong Hu
Wei Huang
Wei Huang
Youji Wang
Youji Wang
Youji Wang
The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach
Frontiers in Marine Science
microplastic
energy status
cellular energy allocation
energy metabolism
mussel
title The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach
title_full The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach
title_fullStr The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach
title_full_unstemmed The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach
title_short The Effect of Microplastics on the Bioenergetics of the Mussel Mytilus coruscus Assessed by Cellular Energy Allocation Approach
title_sort effect of microplastics on the bioenergetics of the mussel mytilus coruscus assessed by cellular energy allocation approach
topic microplastic
energy status
cellular energy allocation
energy metabolism
mussel
url https://www.frontiersin.org/articles/10.3389/fmars.2021.754789/full
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