Micro/Nano-Plastics Cause Neurobehavioral Toxicity in Discus Fish (Symphysodon aequifasciatus): Insight from Brain-Gut-Microbiota Axis
Abstract
Numerous studies have investigated neurobehavioral toxicity of microplastics, but no studies have illustrated mechanism via brain-gut axis. Here, juvenile discus fish (Symphysodon aequifasciatus) were exposed for 96 h to microfibers (900 µm, fiber, MFs) or nanoplastics (~88 nm, bead, NPs) with three concentrations (0, 20 and 200 µg/L). Accumulation in fish gut was independent of plastics type and concentration. MFs reduced growth performance while NPs weakened swimming and predatory performance of post-exposed discus. For brain cholinesterase activity, acetylcholinesterase was activated by NPs while NPs/MFs exposure inhibited butyrylcholinesterase. Concentrations of neurotransmitters (acetylcholine, dopamine and γ-aminobutyric acid) increased in brain but decreased in gut after NPs or MFs exposure. For gut microbiota, increased richness under MFs exposure was observed. At phylum level, Proteobacteria proportion was lower in NPs but higher in MFs. Abundance of Clostridia and Fusobacteriia (Bacillus), potentially secreting neurotransmitters, increased in NPs but decreased in MFs. Brain transcriptomics revealed seven upregulated and four downregulated genes concerning neural-activities. Pathways of neuroactive ligand-receptor interaction and serotonergic synapse were enriched in both MFs and NPs, but dopaminergic synapse pathway was enriched only in MFs. These results established a novel mechanism by which microplastics might cause behavioral toxicities via brain-gut-microbiota axis.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
MPs can induce toxic effects on organisms, affecting normal functioning, and may cause organ-specific toxicities such as neuronal, digestive, reproductive, and developmental toxicity.
“MPs can induce toxic effects on organisms, affecting normal functioning, and may cause several organ-specific toxicities, such as neuronal, digestive, reproductive, and developmental toxicity [17,18,19,20,21,22,23].”
From Is Wild Marine Biota Affected by Microplastics? (2022) · cites this paper as [17]
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
A new and rapid colorimetric determination of acetylcholinesterase activity
Ellman, G. L., Courtney, K. D., Andres, V., & Featherstone, R. M. (1961) · Biochemical Pharmacology · doi:10.1016/0006-2952(61)90145-9 · Cited by 27,221 · see citing works
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., et al. (2009) · Clinical Chemistry · doi:10.1373/clinchem.2008.112797 · Cited by 16,303 · see citing works
Lost at sea: where is all the plastic?
Thompson, R. C., Olsen, Y., Mitchell, R. P., Davis, A., Rowland, S. J., John, A. W. G., McGonigle, D., & Russell, A. E. (2004) · Science · doi:10.1126/science.1094559 · Cited by 7,765 · see citing works
Proteobacteria: Microbial signature of dysbiosis in gut microbiota
Shin, N.-R., Whon, T. W., & Bae, J.-W. (2015) · Trends in Biotechnology · doi:10.1016/j.tibtech.2015.06.011 · Cited by 3,954 · see citing works
Hartmann, N. B., Hüffer, T., Thompson, R. C., Hassellöv, M., Verschoor, A., Daugaard, A. E., Rist, S., Karlsson, T., Brennholt, N., Cole, M., et al. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.8b05297 · Cited by 2,881 · see citing works
Lu, Y., Zhang, Y., Deng, Y., Jiang, W., Zhao, Y., Geng, J., Ding, L., & Ren, H. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.6b00183 · Cited by 2,125 · see citing works
Neurotoxins Affecting Neuroexocytosis
Schiavo, G., Matteoli, M., & Montecucco, C. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.2.717 · Cited by 1,266 · see citing works
Jeong, C.-B., Won, E.-J., Kang, H.-M., Lee, M.-C., Hwang, D.-S., Hwang, U.-K., Zhou, B., Souissi, S., Lee, S.-J., & Lee, J.-S. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.6b01441 · Cited by 1,233 · see citing works
Molecular and cellular biology of cholinesterases
Massoulié, J., Pezzementi, L., Bon, S., Krejci, E., & Vallette, F.-M. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90040-y · Cited by 1,214 · see citing works
Low numbers of microplastics detected in drinking water from ground water sources
Mintenig, S. M., Löder, M. G. J., Primpke, S., & Gerdts, G. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.08.178 · Cited by 997 · see citing works
Qiao, R., Sheng, C., Lu, Y., Zhang, Y., Ren, H., & Lemos, B. (2019) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2019.01.245 · Cited by 971 · see citing works
Barboza, L. G. A., Lopes, C., Oliveira, P., Bessa, F., Otero, V., Henriques, B., Raimundo, J., Caetano, M., Vale, C., & Guilhermino, L. (2020) · Science of The Total Environment · doi:10.1016/j.scitotenv.2019.134625 · Cited by 951 · see citing works
García‐Segura, L. M., Azcoitia, Í., & DonCarlos, L. L. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00025-3 · Cited by 938 · see citing works
Qiao, R., Deng, Y., Zhang, S., Wolosker, M. B., Zhu, Q., Ren, H., & Zhang, Y. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.07.065 · Cited by 926 · see citing works
Barboza, L. G. A., Vieira, L. R., Branco, V., Figueiredo, N., Carvalho, F., Carvalho, C., & Guilhermino, L. (2018) · Aquatic Toxicology · doi:10.1016/j.aquatox.2017.12.008 · Cited by 766 · see citing works
Microplastic risk assessment in surface waters: A case study in the Changjiang Estuary, China
Xu, P., Peng, G., Su, L., Gao, Y., Gao, L., & Li, D. (2018) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2018.06.020 · Cited by 745 · see citing works
Tanaka, K., & Takada, H. (2016) · Scientific Reports · doi:10.1038/srep34351 · Cited by 737 · see citing works
Microplastic in three urban estuaries, China
Zhao, S., Zhu, L., & Li, D. (2015) · Environmental Pollution · doi:10.1016/j.envpol.2015.08.027 · Cited by 722 · see citing works
Selective enrichment of bacterial pathogens by microplastic biofilm
Wu, X., Pan, J., Li, M., Li, Y., Bartlam, M. G., & Wang, Y. (2019) · Water Research · doi:10.1016/j.watres.2019.114979 · Cited by 719 · see citing works
Yu, P., Liu, Z., Wu, D., Chen, M., Lv, W., & Zhao, Y. (2018) · Aquatic Toxicology · doi:10.1016/j.aquatox.2018.04.015 · Cited by 610 · see citing works
Hidayaturrahman, H., & Lee, T.-G. (2019) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2019.06.071 · Cited by 597 · see citing works
Comparison of microplastic pollution in different water bodies from urban creeks to coastal waters
Luo, W., Su, L., Craig, N. J., Du, F., Wu, C., & Shi, H. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.11.081 · Cited by 504 · see citing works
Wan, Z., Wang, C., Zhou, J., Shen, M., Wang, X., Fu, Z., & Jin, Y. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.11.070 · Cited by 503 · see citing works
Sarasamma, S., Audira, G., Siregar, P., Malhotra, N., Lai, Y., Liang, S., Chen, J., Chen, K. H. ‐., & Hsiao, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041410 · Cited by 462 · see citing works
Dehler, C. E., Secombes, C. J., & Martín, S. (2016) · Aquaculture · doi:10.1016/j.aquaculture.2016.07.017 · Cited by 452 · see citing works
Wen, B., Jin, S.-R., Chen, Z., Gao, J., Liu, Y.-N., Liu, J.-H., & Feng, X.-S. (2018) · Environmental Pollution · doi:10.1016/j.envpol.2018.09.029 · Cited by 429 · see citing works
Self-citationYunes, R. А., Poluektova, E. U., Dyachkova, M. S., Klimina, K. M., Kovtun, A. S., Averina, O. V., Orlova, V. S., & Даниленко, В. Н. (2016) · Anaerobe · doi:10.1016/j.anaerobe.2016.10.011 · Cited by 376 · see citing works
Global distribution of microplastics and its impact on marine environment—a review
Nithin, A., Sundaramanickam, A., Surya, P., Sathish, M., & Janakiraman, S. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-09015-5 · Cited by 366 · see citing works
Materić, D., Kasper-Giebl, A., Kau, D., Anten, M., Greilinger, M., Ludewig, E., van Sebille, E., Röckmann, T., & Holzinger, R. (2020) · Environmental Science & Technology · doi:10.1021/acs.est.9b07540 · Cited by 363 · see citing works
Luís, L. G., Ferreira, P., Fonte, E., Oliveira, M., & Guilhermino, L. (2015) · Aquatic Toxicology · doi:10.1016/j.aquatox.2015.04.018 · Cited by 342 · see citing works
Ferreira, P., Fonte, E., Soares, M. E., Carvalho, F., & Guilhermino, L. (2016) · Aquatic Toxicology · doi:10.1016/j.aquatox.2015.11.011 · Cited by 325 · see citing works
Zhao, S., Wang, T., Zhu, L., Xu, P., Wang, X., Gao, L., & Li, D. (2019) · Water Research · doi:10.1016/j.watres.2019.06.019 · Cited by 311 · see citing works
Huang, J.-N., Wen, B., Zhu, J.-G., Zhang, Y.-S., Gao, J., & Chen, Z. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.138929 · Cited by 277 · see citing works
Self-citationLiu, Z., Huang, Y., Jiao, Y., Chen, Q., Wu, D., Yu, P., Li, Y., Cai, M., & Zhao, Y. (2020) · Aquatic Toxicology · doi:10.1016/j.aquatox.2020.105420 · Cited by 251 · see citing works
Cole, M., Liddle, C., Consolandi, G., Drago, C., Hird, C., Lindeque, P. K., & Galloway, T. S. (2020) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2020.111552 · Cited by 234 · see citing works
Wen, B., Zhang, N., Jin, S.-R., Chen, Z., Gao, J., Liu, Y., Liu, H.-P., & Xu, Z. (2017) · Aquatic Toxicology · doi:10.1016/j.aquatox.2017.12.010 · Cited by 226 · see citing works
Self-citationLi, Y., Liu, Z., Li, M., Jiang, Q., Wu, D., Huang, Y., Jiao, Y., Zhang, M., & Zhao, Y. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.122990 · Cited by 200 · see citing works
Microplastics Lead to Hyperactive Swimming Behaviour in Adult Zebrafish
Chen, Q., Lackmann, C., Wang, W., Seiler, T., Hollert, H., & Shi, H. (2020) · Aquatic Toxicology · doi:10.1016/j.aquatox.2020.105521 · Cited by 194 · see citing works
Microplastic-associated biofilms in lentic Italian ecosystems
Pippo, F. D., Venezia, C., Sighicelli, M., Pietrelli, L., Vito, S. D., Nuglio, S., & Rossetti, S. (2020) · Water Research · doi:10.1016/j.watres.2020.116429 · Cited by 188 · see citing works
Suman, T. Y., Jia, P., Li, W., Junaid, M., Xin, G.-Y., Wang, Y., & Pei, D. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123220 · Cited by 186 · see citing works
Liu, Z., Li, Y., Pérez, E., Jiang, Q., Chen, Q., Jiao, Y., Huang, Y., Yang, Y., & Zhao, Y. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123778 · Cited by 186 · see citing works
Bharath, K. M., Srinivasalu, S., Natesan, U., Ayyamperumal, R., Nirmal Kalam, S., Anbalagan, S., Sujatha, K., & Alagarasan, C. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.128502 · Cited by 178 · see citing works
Horzmann, K. A., & Freeman, J. L. (2016) · Toxics · doi:10.3390/toxics4030019 · Cited by 163 · see citing works
Ma, T., Jin, H., Kwok, L., Sun, Z., Liong, M., & Zhang, H. (2021) · Neurobiology of Stress · doi:10.1016/j.ynstr.2021.100294 · Cited by 153 · see citing works
Cao, G., Tao, F., Hu, Y., Li, Z., Zhang, Y., Deng, B., & Zhan, X. (2019) · Food & Function · doi:10.1039/c8fo02370k · Cited by 122 · see citing works
Chae, Y., Kim, D., Choi, M.-J., Cho, Y., & An, Y.-J. (2019) · Environment International · doi:10.1016/j.envint.2019.05.042 · Cited by 122 · see citing works
Huang, J.-N., Wen, B., Meng, L.-J., Li, X., Mei-hui, W., Gao, J., & Chen, Z. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123044 · Cited by 118 · see citing works
Self-citationEstrela, F. N., Guimarães, A. T. B., Silva, F. G., da Luz, T. M., Silva, A. M., Pereira, P. S., & Malafaia, G. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123879 · Cited by 118 · see citing works
Chen, H., Hua, X., Li, H., Wang, C., Dang, Y., Ding, P., & Yu, Y. (2021) · Chemosphere · doi:10.1016/j.chemosphere.2021.129642 · Cited by 116 · see citing works
Wen, B., Liu, J.-H., Zhang, Y., Zhang, H.-R., Gao, J., & Chen, Z. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.140082 · Cited by 115 · see citing works
Self-citationZuo, J., Huo, T., Du, X., Yang, Q., Wu, Q., Shen, J., Liu, C., Hung, T., Yan, W., & Li, G. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.124677 · Cited by 97 · see citing works
Exposure to the fungicide propamocarb causes gut microbiota dysbiosis and metabolic disorder in mice
Wu, S., Jin, C., Wang, Y., Fu, Z., & Jin, Y. (2017) · Environmental Pollution · doi:10.1016/j.envpol.2017.10.129 · Cited by 91 · see citing works
Zhou, T., & Weis, J. S. (1998) · Aquatic Toxicology · doi:10.1016/s0166-445x(98)00052-6 · Cited by 89 · see citing works
Lin, X., Zhao, J., Zhang, W., He, L., Wang, L., Chang, D., Cui, L., Gao, Y., Li, B., Chen, C., et al. (2020) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.110130 · Cited by 89 · see citing works
Guimarães, A. T. B., Estrela, F. N., Rodrigues, A. S. D. L., Chagas, T. Q., Pereira, P. S., Silva, F. G., & Malafaia, G. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.123864 · Cited by 80 · see citing works
Acetylcholine receptors from human muscle as pharmacological targets for ALS therapy
Palma, E., Reyes‐Ruiz, J. M., Lopergolo, D., Roseti, C., Bertollini, C., Ruffolo, G., Cifelli, P., Onesti, E., Limatola, C., Miledi, R., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1600251113 · Cited by 70 · see citing works
Iroegbu, A. O. C., Sadiku, E. R., Ray, S. S., & Hamam, Y. (2020) · Environmental Science and Pollution Research · doi:10.1007/s11356-020-08194-5 · Cited by 64 · see citing works
Adverse effects of serotonin depletion in developing zebrafish
Airhart, M. J., Lee, D. H., Wilson, T. D., Miller, B. E., Miller, M. N., Skalko, R. G., & Monaco, P. J. (2011) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2011.08.008 · Cited by 60 · see citing works
Characterization of Serotonin Signaling Components in Patients with Inflammatory Bowel Disease
Shajib, M. S., Chauhan, U., Adeeb, S., et al. (2018) · Journal of the Canadian Association of Gastroenterology · doi:10.1093/jcag/gwy039 · Cited by 52 · see citing works
Maharaj, S., Ahmadie, N. E., Rheingold, S., et al. (2020) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2020.106917 · Cited by 37 · see citing works
Wang, H., Qin, X., Gui, Z., & Chu, W. (2020) · Microbial Pathogenesis · doi:10.1016/j.micpath.2020.104474 · Cited by 35 · see citing works
Ouyang, M., Liu, J.-H., Wen, B., Huang, J.-N., Feng, X.-S., Gao, J., & Chen, Z. (2020) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2020.124121 · Cited by 33 · see citing works
Self-citationMarkin, P. A., Alex Brito, O., Moskaleva, N. E., et al. (2021) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2021.100816 · Cited by 33 · see citing works
Sphingolipids as Regulators of Neuro-Inflammation and NADPH Oxidase 2
Arsenault, E. J., McGill, C. M., & Barth, B. M. (2021) · NeuroMolecular Medicine · doi:10.1007/s12017-021-08646-2 · Cited by 31 · see citing works
Fuertes, I., & Barata, C. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.127814 · Cited by 25 · see citing works
Is HCRTR2 a Genetic Risk Factor for Alzheimer's Disease?
Gallone, S., Boschi, S., Rubino, E., et al. (2014) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000359964 · Cited by 23 · see citing works
Souza, J. G. D. S., Libeck, L. T., Virote, B. D. C. R., et al. (2020) · Aquaculture International · doi:10.1007/s10499-020-00516-1 · Cited by 18 · see citing works
Sousa, B., & Nunes, B. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.139372 · Cited by 17 · see citing works
DiCarlo, G. E., Mabry, S. J., Cao, X., McMillan, C., Woynaroski, T. G., Harrison, F. E., Reddy, I. A., Matthies, H. J. G., Flynn, C. R., Wallace, M. T., et al. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.655451 · Cited by 15 · see citing works
Yue, Z., Tian, E., Chen, Y., Luo, L., Yang, L., He, L., Li, L., & Wang, J. (2021) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2020.111875 · Cited by 14 · see citing works
Lemgruber, R. D. S. P., dos Anjos, N. A., Ghelfi, A., Fagundes, D. B., & Val, A. L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081083 · Cited by 12 · see citing works
A toxic diet: transfer of contaminants to offspring through a parental care mechanism
Maunder, R. J., Buckley, J., Val, A. L., et al. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.089102 · Cited by 10 · see citing works
Sine, H., Achbani, A., & Filali, K. (2021) · Archives of Environmental & Occupational Health · doi:10.1080/19338244.2021.1886034 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Is Wild Marine Biota Affected by Microplastics?
Porcino, N., Bottari, T., & Mancuso, M. (2022) · Animals · doi:10.3390/ani13010147 · Cited by 55 · see citing works
- Authors
- Huang, J.-N., Wen, B., Xu, L., Ma, H.-C., Li, X.-X., Gao, J.-Z., & Chen, Z.-Z.
- Affiliations
- Ministry of Agriculture and Rural Affairs (CN)
- Shanghai Ocean University (CN)
- Corresponding author
- Wen, Bin
- Chen, Zai-Zhong
- Venue
- Journal of Hazardous Materials
- Publisher
- Elsevier BV
- Published
- 2022-01
- Volume
- 421
- Pages
- 126830
- ISSN
- 0304-3894 (ISSN-L)
- OpenAlex
- W3188533108
- Cited by
- 202
- References
- 74
- Citations by year
- 2026: 38 · 2025: 40 · 2024: 46 · 2023: 40 · 2022: 34 · 2021: 4
- FWCI
- 7.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Journal of Hazardous Materials (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Environmental Science › Pollution › Microplastics and Plastic Pollution
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
- Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
- Keywords
- microplastics, nanoplastics, microfibers, neurobehavioral toxicity, Discus, Symphysodon aequifasciatus, brain-gut-microbiota axis, gut microbiota, neurotransmitters, acetylcholinesterase, butyrylcholinesterase, swimming performance, predatory behavior, growth performance, brain transcriptomics, serotonergic synapse, dopaminergic synapse, neuroactive ligand-receptor interaction
- MeSH terms
- Gastrointestinal Microbiome, Microplastics, Acetylcholinesterase, Animals, Brain, Butyrylcholinesterase, Plastics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
