Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior

Nanoplastics are being detected with increasing frequency in aquatic environments. Although evidence suggests that nanoplastics can cause overt toxicity to biota across different trophic levels, but there is little understanding of how materials such as differently charged polystyrene nanoplastics (...

Full description

Bibliographic Details
Main Authors: Miaomiao Teng, Xiaoli Zhao, Fengchang Wu, Chengju Wang, Chen Wang, Jason C. White, Wentian Zhao, Lingfeng Zhou, Sen Yan, Sinuo Tian
Format: Article
Language:English
Published: Elsevier 2022-05-01
Series:Environment International
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0160412022000800
_version_ 1818060427151540224
author Miaomiao Teng
Xiaoli Zhao
Fengchang Wu
Chengju Wang
Chen Wang
Jason C. White
Wentian Zhao
Lingfeng Zhou
Sen Yan
Sinuo Tian
author_facet Miaomiao Teng
Xiaoli Zhao
Fengchang Wu
Chengju Wang
Chen Wang
Jason C. White
Wentian Zhao
Lingfeng Zhou
Sen Yan
Sinuo Tian
author_sort Miaomiao Teng
collection DOAJ
description Nanoplastics are being detected with increasing frequency in aquatic environments. Although evidence suggests that nanoplastics can cause overt toxicity to biota across different trophic levels, but there is little understanding of how materials such as differently charged polystyrene nanoplastics (PS-NP) impact fish development and behavior. Following exposure to amino-modified (positive charge) PS-NP, fluorescence accumulation was observed in the zebrafish brain and gastrointestinal tract. Positively charged PS-NP induced stronger developmental toxicity (decreased spontaneous movement, heartbeat, hatching rate, and length) and cell apoptosis in the brain and induced greater neurobehavioral impairment as compared to carboxyl-modified (negative charge) PS-NP. These findings correlated well with fluorescence differences indicating PS-NP presence. Targeted neuro-metabolite analysis by UHPLC-MS/MS reveals that positively charged PS-NP decreased levels of glycine, cysteine, glutathione, and glutamic acid, while the increased levels of spermine, spermidine, and tyramine were induced by negatively charged PS-NP. Positively charged PS-NP interacted with the neurotransmitter receptor N-methyl-D-aspartate receptor 2B (NMDA2B), whereas negatively charged PS-NP impacted the G-protein-coupled receptor 1 (GPR1), each with different binding energies that led to behavioral differences. These findings reveal the charge-specific toxicity of nanoplastics to fish and provide new perspective for understanding PS-NP neurotoxicity that is needed to accurately assess potential environmental and health risks of these emerging contaminants.
first_indexed 2024-12-10T13:32:15Z
format Article
id doaj.art-43ea7ea1c998428caaeec889ae24f132
institution Directory Open Access Journal
issn 0160-4120
language English
last_indexed 2024-12-10T13:32:15Z
publishDate 2022-05-01
publisher Elsevier
record_format Article
series Environment International
spelling doaj.art-43ea7ea1c998428caaeec889ae24f1322022-12-22T01:46:55ZengElsevierEnvironment International0160-41202022-05-01163107154Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behaviorMiaomiao Teng0Xiaoli Zhao1Fengchang Wu2Chengju Wang3Chen Wang4Jason C. White5Wentian Zhao6Lingfeng Zhou7Sen Yan8Sinuo Tian9State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, ChinaState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China; Corresponding authors at: Anwai Dayang Fang 8#, Chaoyang District, Beijing, China.State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China; Corresponding authors at: Anwai Dayang Fang 8#, Chaoyang District, Beijing, China.Innovation Center of Pesticide Research, Department of Applied Chemistry, College of Science, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, ChinaThe Connecticut Agricultural Experiment Station, New Haven, Connecticut 06511, USAInnovation Center of Pesticide Research, Department of Applied Chemistry, College of Science, China Agricultural University, Beijing 100193, ChinaState Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, ChinaInnovation Center of Pesticide Research, Department of Applied Chemistry, College of Science, China Agricultural University, Beijing 100193, ChinaInnovation Center of Pesticide Research, Department of Applied Chemistry, College of Science, China Agricultural University, Beijing 100193, ChinaNanoplastics are being detected with increasing frequency in aquatic environments. Although evidence suggests that nanoplastics can cause overt toxicity to biota across different trophic levels, but there is little understanding of how materials such as differently charged polystyrene nanoplastics (PS-NP) impact fish development and behavior. Following exposure to amino-modified (positive charge) PS-NP, fluorescence accumulation was observed in the zebrafish brain and gastrointestinal tract. Positively charged PS-NP induced stronger developmental toxicity (decreased spontaneous movement, heartbeat, hatching rate, and length) and cell apoptosis in the brain and induced greater neurobehavioral impairment as compared to carboxyl-modified (negative charge) PS-NP. These findings correlated well with fluorescence differences indicating PS-NP presence. Targeted neuro-metabolite analysis by UHPLC-MS/MS reveals that positively charged PS-NP decreased levels of glycine, cysteine, glutathione, and glutamic acid, while the increased levels of spermine, spermidine, and tyramine were induced by negatively charged PS-NP. Positively charged PS-NP interacted with the neurotransmitter receptor N-methyl-D-aspartate receptor 2B (NMDA2B), whereas negatively charged PS-NP impacted the G-protein-coupled receptor 1 (GPR1), each with different binding energies that led to behavioral differences. These findings reveal the charge-specific toxicity of nanoplastics to fish and provide new perspective for understanding PS-NP neurotoxicity that is needed to accurately assess potential environmental and health risks of these emerging contaminants.http://www.sciencedirect.com/science/article/pii/S0160412022000800Differentially chargedPolystyrene nanoplasticsZebrafishBehavioral activityNeurotransmitters
spellingShingle Miaomiao Teng
Xiaoli Zhao
Fengchang Wu
Chengju Wang
Chen Wang
Jason C. White
Wentian Zhao
Lingfeng Zhou
Sen Yan
Sinuo Tian
Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior
Environment International
Differentially charged
Polystyrene nanoplastics
Zebrafish
Behavioral activity
Neurotransmitters
title Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior
title_full Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior
title_fullStr Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior
title_full_unstemmed Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior
title_short Charge-specific adverse effects of polystyrene nanoplastics on zebrafish (Danio rerio) development and behavior
title_sort charge specific adverse effects of polystyrene nanoplastics on zebrafish danio rerio development and behavior
topic Differentially charged
Polystyrene nanoplastics
Zebrafish
Behavioral activity
Neurotransmitters
url http://www.sciencedirect.com/science/article/pii/S0160412022000800
work_keys_str_mv AT miaomiaoteng chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT xiaolizhao chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT fengchangwu chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT chengjuwang chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT chenwang chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT jasoncwhite chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT wentianzhao chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT lingfengzhou chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT senyan chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior
AT sinuotian chargespecificadverseeffectsofpolystyrenenanoplasticsonzebrafishdanioreriodevelopmentandbehavior