Abstract
Microplastics (MPs) are widespread in aquatic environments. They could induce intestinal toxicity in the fish. However, research on the metabolic toxicity of polystyrene microplastics (PS-MPs) with different particle sizes to the zebrafish intestine is still limited. Here, metabolomics using ultra-performance liquid chromatography–tandem mass spectrometry (UHPLC-MS/MS) was applied to characterize the metabolic disorders in zebrafish intestine after exposure to 500 μg/L PS-MPs with different sizes (100 nm, 5 μm, and 200 μm) for 21 days. Results showed that the 100 nm PS-MPs group increased glutathione content. A total of 35, 165, and 87 metabolites were significantly altered in zebrafish intestines of 100 nm, 5 μm, and 200 μm groups under positive ion mode, respectively. In comparison, 31, 115, and 45 metabolites were changed in the 100 nm, 5 μm, and 200 μm groups under negative ion mode, respectively. Metabolic pathway analysis indicated that carbohydrate metabolism, amino acid metabolism, and nucleotide metabolism were changed in all three groups. The greatest changes were found in the 5 μm group. Moreover, treatment with micro-sized PS-MP groups specifically changed lipid metabolism, which might be related to pathogenic bacteria (Streptococcus and Moraxella). In the 100 nm PS-MP group, S-adenosyl-l-methionine (SAM) was found to be markedly related to the intestinal microbiota. SAM level was significantly increased, which might account for the elevated glutathione content. To sum up, the mechanisms of nano-sized MPs (oxidative stress) and micro-sized MPs (lipid metabolism disorder) were distinct. This study provides novel insight into the toxicity mechanism of MPs in the zebrafish intestine.
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References
Alomar C, Deudero S (2017) Evidence of microplastic ingestion in the shark Galeus melastomus Rafinesque, 1810 in the continental shelf off the western Mediterranean Sea. Environ Pollut 223:223–229. https://doi.org/10.1016/j.envpol.2017.01.015
Ariav Y, Ch’ng JH, Christofk HR, Ron-Harel N, Erez A (2021) Targeting nucleotide metabolism as the nexus of viral infections, cancer, and the immune response. Sci Adv 7:eabg616. https://doi.org/10.1126/sciadv.abg6165
Chen H, Wang Z, Cai H, Zhou C (2016) Progress in the microbial production of S-adenosyl-L-methionine. World J Microbiol Biotechnol 32:153. https://doi.org/10.1007/s11274-016-2102-8
Chen Q, Yin D, Jia Y, Schiwy S, Legradi J, Yang S, Hollert H (2017) Enhanced uptake of BPA in the presence of nanoplastics can lead to neurotoxic effects in adult zebrafish. Sci Total Environ 609:1312–1321. https://doi.org/10.1016/j.scitotenv.2017.07.144
Chen Q, Lackmann C, Wang W, Seiler T-B, Hollert H, Shi H (2020) Microplastics lead to hyperactive swimming behaviour in adult zebrafish. Aquat Toxicol 224:105521. https://doi.org/10.1016/j.aquatox.2020.105521
Chen Z, Han S, Zhou D, Zhou S, Jia G (2019) Effects of oral exposure to titanium dioxide nanoparticles on gut microbiota and gut-associated metabolism in vivo. Nanoscale 11:22398–22412. https://doi.org/10.1039/c9nr07580a
Cheng W, Li X, Zhou Y, Yu H, Xie Y, Guo H, Wang H, Li Y, Feng Y, Wang Y (2022) Polystyrene microplastics induce hepatotoxicity and disrupt lipid metabolism in the liver organoids. Sci Total Environ 806:150328. https://doi.org/10.1016/j.scitotenv.2021.150328
Cho Y, Shim WJ, Jang M, Han GM, Hong SH (2019) Abundance and characteristics of microplastics in market bivalves from South Korea. Environ Pollut 245:1107–1116. https://doi.org/10.1016/j.envpol.2018.11.091
Choi JS, Hong SH, Park J-W (2020) Evaluation of microplastic toxicity in accordance with different sizes and exposure times in the marine copepod Tigriopus japonicus. Mar Environ Res 153:104838. https://doi.org/10.1016/j.marenvres.2019.104838
Correa-Martinez CL, Rauwolf KK, Schuler F, Fueller M, Kampmeier S, Groll AH (2019) Moraxella nonliquefaciens bloodstream infection and sepsis in a pediatric cancer patient: case report and literature review. BMC Infect Dis 19:836. https://doi.org/10.1186/s12879-019-4489-y
Dai J, Lai L, Tang H, Wang W, Wang S, Lu C, Yao H, Fan H, Wu Z (2018) Streptococcus suis synthesizes deoxyadenosine and adenosine by 5’-nucleotidase to dampen host immune responses. Virulence 9:1509–1520. https://doi.org/10.1080/21505594.2018.1520544
Ding J, Zhang S, Razanajatovo RM, Zou H, Zhu W (2018) Accumulation, tissue distribution, and biochemical effects of polystyrene microplastics in the freshwater fish red tilapia (Oreochromis niloticus). Environ Pollut 238:1–9. https://doi.org/10.1016/j.envpol.2018.03.001
Fujita Y, Matsuoka H, Hirooka K (2007) Regulation of fatty acid metabolism in bacteria. Mol Microbiol 66:829–839. https://doi.org/10.1111/j.1365-2958.2007.05947.x
Gonzalez-Uarquin F, Rodehutscord M, Huber K (2020) Myo-inositol: its metabolism and potential implications for poultry nutrition–a review. Poult Sci 99:893–905. https://doi.org/10.1016/j.psj.2019.10.014
Granby K, Rainieri S, Rasmussen RR, Kotterman MJJ, Sloth JJ, Cederberg TL, Barranco A, Marques A, Larsen BK (2018) The influence of microplastics and halogenated contaminants in feed on toxicokinetics and gene expression in European seabass (Dicentrarchus labrax). Environ Res 164:430–443. https://doi.org/10.1016/j.envres.2018.02.035
Gray AD, Weinstein JE (2017) Size- and shape-dependent effects of microplastic particles on adult daggerblade grass shrimp (Palaemonetes pugio). Environ Toxicol Chem 36:3074–3080. https://doi.org/10.1002/etc.3881
Gu W, Liu S, Chen L, Liu Y, Gu C, Ren H-q, Wu B (2020) Single-cell RNA sequencing reveals size-dependent effects of polystyrene microplastics on immune and secretory cell populations from zebrafish intestine. Environ Sci Technol 54:3417–3427. https://doi.org/10.1021/acs.est.9b06386
Güven O, Gökdağ K, Jovanović B, Kıdeyş AE (2017) Microplastic litter composition of the Turkish territorial waters of the Mediterranean Sea, and its occurrence in the gastrointestinal tract of fish. Environ Pollut 223:286–294. https://doi.org/10.1016/j.envpol.2017.01.025
Haspel JA, Chettimada S, Shaik RS, Chu J-H, Raby BA, Cernadas M, Carey V, Process V, Hunninghake GM, Ifedigbo E, Lederer JA, Englert J, Pelton A, Coronata A, Fredenburgh LE, Choi AMK (2014) Circadian rhythm reprogramming during lung inflammation. Nat Commun 5:4753. https://doi.org/10.1038/ncomms5753
He M, Yan M, Chen X, Wang X, Gong H, Wang W, Wang J (2022) Bioavailability and toxicity of microplastics to zooplankton. Gondwana Res 108:120–126. https://doi.org/10.1016/j.gr.2021.07.021
Heischmann S, Quinn K, Cruickshank-Quinn C, Liang L-P, Reisdorph R, Reisdorph N, Patel M (2016) Exploratory metabolomics profiling in the kainic acid rat model reveals depletion of 25-hydroxyvitamin D3 during epileptogenesis. Sci Rep 6:31424. https://doi.org/10.1038/srep31424
Hubert L, Sutton VR, Garg U, Smith LD (2017) Disorders of purine and pyrimidine metabolism. Elsevier Inc 2:283–299
Jia J, Qin J, Yuan X, Liao Z, Huang J, Wang B, Sun C, Li W (2019) Microarray and metabolome analysis of hepatic response to fasting and subsequent refeeding in zebrafish (Danio rerio). BMC Genomics 20:919. https://doi.org/10.1186/s12864-019-6309-6
Jin Y, Xia J, Pan Z, Yang J, Wang W, Fu Z (2018) Polystyrene microplastics induce microbiota dysbiosis and inflammation in the gut of adult zebrafish. Environ Pollut 235:322–329. https://doi.org/10.1016/j.envpol.2017.12.088
Kang H-M, Byeon E, Jeong H, Kim M-S, Chen Q, Lee J-S (2021) Different effects of nano- and microplastics on oxidative status and gut microbiota in the marine medaka Oryzias melastigma. J Hazard Mater 405:124207. https://doi.org/10.1016/j.jhazmat.2020.124207
Khoubnasabjafari M, Ansarin K, Jouyban A (2015) Reliability of malondialdehyde as a biomarker of oxidative stress in psychological disorders. Bioimpacts 5:123–127
Le L, Liu M, Song Y, Lu S, Hu J, Cao C, Xie B, Shi H, He D (2018) Polystyrene (nano) microplastics cause size-dependent neurotoxicity, oxidative damage and other adverse effects in Caenorhabditis elegans. Environ Sci Nano 5:2009–2020. https://doi.org/10.1039/c8en00412a
Lei L, Wu S, Lu S, Liu M, Song Y, Fu Z, Shi H, Raley-Susman KM, He D (2018) Microplastic particles cause intestinal damage and other adverse effects in zebrafish Danio rerio and nematode Caenorhabditis elegans. Sci Total Environ 619:1–8. https://doi.org/10.1016/j.scitotenv.2017.11.103
Liu L, Wu Q, Miao X, Fan T, Meng Z, Chen X, Zhu W (2022) Study on toxicity effects of environmental pollutants based on metabolomics: a review. Chemosphere 286:131815. https://doi.org/10.1016/j.chemosphere.2021.131815
Liu S, Wang J, Zhu J, Wang J, Wang H, Zhan X (2021) The joint toxicity of polyethylene microplastic and phenanthrene to wheat seedlings. Chemosphere 282:130967. https://doi.org/10.1016/j.chemosphere.2021.130967
Liu Z, Yu P, Cai M, Wu D, Zhang M, Chen M, Zhao Y (2019) Effects of microplastics on the innate immunity and intestinal microflora of juvenile Eriocheir sinensis. Sci Total Environ 685:836–846. https://doi.org/10.1016/j.scitotenv.2019.06.265
Magera MJ, Gunawardena ND, Hahn SH, Tortorelli S, Mitchell GA, Goodman SI, Rinaldo P, Matern D (2006) Quantitative determination of succinylacetone in dried blood spots for newborn screening of tyrosinemia type I. Mol Genet Metab 88:16–21. https://doi.org/10.1016/j.ymgme.2005.12.005
Mates JM, Campos-Sandoval JA, de los Santos-Jimenez J, Marquez J, (2019) Dysregulation of glutaminase and glutamine synthetase in cancer. Cancer Lett 467:29–39. https://doi.org/10.1016/j.canlet.2019.09.011
Mattsson K, Ekvall MT, Hansson L-A, Linse S, Malmendal A, Cedervall T (2015) Altered behavior, physiology, and metabolism in fish exposed to polystyrene nanoparticles. Environ Sci Technol 49:553–561. https://doi.org/10.1021/es5053655
Miller EG, Porter JL, Binnie WH, Guo IY, Hasegawa S (2004) Further studies on the anticancer activity of citrus limonoids. J Agric Food Chem 52:4908–4912. https://doi.org/10.1021/jf049698g
Neis EPJG, Dejong CHC, Rensen SS (2015) The role of microbial amino acid metabolism in host metabolism. Nutrients 7:2930–2946. https://doi.org/10.3390/nu7042930
Nelms SE, Barnett J, Brownlow A, Davison NJ, Deaville R, Galloway TS, Lindeque PK, Santillo D, Godley BJ (2019) Microplastics in marine mammals stranded around the British coast: ubiquitous but transitory? Sci Rep 9:1075. https://doi.org/10.1038/s41598-018-37428-3
Niu J, Gao B, Wu W, Peng W, Xu D (2022) Occurrence, stability and source identification of small size microplastics in the Jiayan reservoir China. Sci Total Environ 807:150832. https://doi.org/10.1016/j.scitotenv.2021.150832
Qiao R, Deng Y, Zhang S, Wolosker MB, Zhu Q, Ren H, Zhang Y (2019a) Accumulation of different shapes of microplastics initiates intestinal injury and gut microbiota dysbiosis in the gut of zebrafish. Chemosphere 236:124334. https://doi.org/10.1016/j.chemosphere.2019.07.065
Qiao R, Sheng C, Lu Y, Zhang Y, Ren H, Lemos B (2019b) Microplastics induce intestinal inflammation, oxidative stress, and disorders of metabolome and microbiome in zebrafish. Sci Total Environ 662:246–253. https://doi.org/10.1016/j.scitotenv.2019.01.245
Ren C, Hu X, Li X, Zhou Q (2016) Ultra-trace graphene oxide in a water environment triggers Parkinson’s disease-like symptoms and metabolic disturbance in zebrafish larvae. Biomaterials 93:83–94. https://doi.org/10.1016/j.biomaterials.2016.03.036
Renzi M, Grazioli E, Blaskovic A (2019) Effects of different microplastic types and surfactant-microplastic mixtures under fasting and feeding conditions: a case study on Daphnia magna. Bull Environ Contam Toxicol 103:367–373. https://doi.org/10.1007/s00128-019-02678-y
Rist S, Baun A, Hartmann NB (2017) Ingestion of micro- and nanoplastics in Daphnia magna – quantification of body burdens and assessment of feeding rates and reproduction. Environ Pollut 228:398–407. https://doi.org/10.1016/j.envpol.2017.05.048
Sreekumar A et al (2009) Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 457:910–914. https://doi.org/10.1038/nature07762
Sun Z, Li J, Wang W, Liu Y, Liu J, Jiang H, Lu Q, Ding P, Shi R, Zhao X, Yuan W, Tan X, Shi X, Xing Y, Mao T (2021) Qingchang wenzhong decoction accelerates intestinal mucosal healing through modulation of dysregulated gut microbiome, intestinal barrier and immune responses in mice. Front Pharmacol 12:738152. https://doi.org/10.3389/fphar.2021.738152
Usman S, Abdull Razis AF, Shaari K, Amal MNA, Saad MZ, Mat Isa N, Nazarudin MF (2021) Polystyrene microplastics exposure: an insight into multiple organ histological alterations, oxidative stress and neurotoxicity in Javanese Medaka Fish (Oryzias javanicus Bleeker, 1854). Int J Environ Res Public Health 18.https://doi.org/10.3390/ijerph18189449
Wenderska IB, Chong M, McNulty J, Wright GD, Burrows LL (2011) Palmitoyl-dl-carnitine is a multitarget inhibitor of Pseudomonas aeruginosa biofilm development. ChemBioChem 12:2759–2766. https://doi.org/10.1002/cbic.201100500
Woermann K, Lucio M, Forcisi S, Heinzmann SS, Kenar E, Franken H, Rosenbaum L, Schmitt-Kopplin P, Kohlbacher O, Zell A, Haering HU, Lehmann R (2012) Metabolomics in diabetes research. Diabetologe 8:42-+. https://doi.org/10.1007/s11428-011-0778-9
Xiong X, Chen X, Zhang K, Mei Z, Hao Y, Zheng J, Wu C, Wang K, Ruan Y, Lam PKS, Wang D (2018) Microplastics in the intestinal tracts of East Asian finless porpoises (Neophocaena asiaeorientalis sunameri) from Yellow Sea and Bohai Sea of China. Mar Pollut Bull 136:55–60. https://doi.org/10.1016/j.marpolbul.2018.09.006
Yang H, Xiong H, Mi K, Xue W, Wei W, Zhang Y (2020) Toxicity comparison of nano-sized and micron-sized microplastics to goldfish Carassius auratus larvae. J Hazard Mater 388:122058. https://doi.org/10.1016/j.jhazmat.2020.122058
Ye G, Zhang X, Liu X, Liao X, Zhang H, Yan C, Lin Y, Huang Q (2021) Polystyrene microplastics induce metabolic disturbances in marine medaka (Oryzias melastigmas) liver. Sci Total Environ 782:146885. https://doi.org/10.1016/j.scitotenv.2021.146885
Yu F, Yang C, Zhu Z, Bai X, Ma J (2019) Adsorption behavior of organic pollutants and metals on micro/nanoplastics in the aquatic environment. Sci Total Environ 694:133643. https://doi.org/10.1016/j.scitotenv.2019.133643
Yu Y, Chen H, Hua X, Dang Y, Han Y, Yu Z, Chen X, Ding P, Li H (2020) Polystyrene microplastics (PS-MPs) toxicity induced oxidative stress and intestinal injury in nematode Caenorhabditis elegans. Sci Total Environ 726.https://doi.org/10.1016/j.scitotenv.2020.138679
Zanandrea R, Wiprich MT, Altenhofen S, Rubensam G, dos Santos TM, Wyse ATS, Bonan CD (2020) Withdrawal effects following methionine exposure in adult zebrafish. Mol Neurobiol 57:3485–3497. https://doi.org/10.1007/s12035-020-01970-x
Zhang P, Fu L, Liu H, Huda N-U, Zhu X, Han D, Jin J, Yang Y, Kim Y-S, Xie S (2019) Effects of inosine 5’-monophosphate supplementation in high fishmeal and high soybean diets on growth, immune-related gene expression in gibel carp (Carassius auratus gibelio var. CAS III), and its challenge against Aeromonas hydrophila infection. Fish Shellfish Immunol 86:913–921. https://doi.org/10.1016/j.fsi.2018.12.016
Zhang X, Wen K, Ding D, Liu J, Lei Z, Chen X, Ye G, Zhang J, Shen H, Yan C, Dong S, Huang Q, Lin Y (2021) Size-dependent adverse effects of microplastics on intestinal microbiota and metabolic homeostasis in the marine medaka (Oryzias melastigma). Environ Int 151:106452. https://doi.org/10.1016/j.envint.2021.106452
Zhao Y, Qiao R, Zhang S, Wang G (2021) Metabolomic profiling reveals the intestinal toxicity of different length of microplastic fibers on zebrafish (Danio rerio). J Hazard Mater 403:123663. https://doi.org/10.1016/j.jhazmat.2020.123663
Zielonka M, Probst J, Carl M, Hoffmann GF, Koelker S, Okun JG (2019) Bioenergetic dysfunction in a zebrafish model of acute hyperammonemic decompensation. Exp Neurol 314:91–99. https://doi.org/10.1016/j.expneurol.2019.01.008
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This study was supported by the National Natural Science Foundation of China (21976087), the Natural Science Foundation of Jiangsu Province (BK20200011), the Fundamental Research Funds for the Central Universities (021114380170), and the Excellent Research Program of Nanjing University (ZYJH005).
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All authors contributed to the study conception. Material preparation, data collection, and analysis were performed by JY and WG. The first manuscript was written by JY. All authors modified the manuscript. The project administration and funding acquisition were provided by BW. All authors read and approved the final manuscript.
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Yu, J., Gu, W., Chen, L. et al. Comparison of metabolome profiles in zebrafish (Danio rerio) intestine induced by polystyrene microplastics with different sizes. Environ Sci Pollut Res 30, 22760–22771 (2023). https://doi.org/10.1007/s11356-022-23827-7
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DOI: https://doi.org/10.1007/s11356-022-23827-7