Probing PFOA-induced Metabolic Disorders in Tilapia Through Fish Skin Mucus

Abstract

The study of the metabolic toxicity of perfluorooctanoic acid (PFOA) is of great importance in assessing its potential impact on aquatic organisms and the aquatic environment, and provides a fundamental scientific basis for environmental protection and sustainable development. In this study, an electrospray ionization (ESI) source capable of direct analysis of solution samples was combined with a high-resolution Orbitrap Fusion Tribrid mass spectrometer to investigate the metabolic perturbations induced by different concentrations of perfluorooctanoic acid (PFOA) and their correlations in skin mucus and liver tissue of tilapia. Seven common metabolites were found in mucus and liver, and nitrogen metabolism pathways were disturbed in all of them. The up-regulation of glutamate in mucus may reflect an increased demand for amino acids and energy, whereas the down-regulation of glutamate in the liver may lead to dysregulation of nitrogen metabolism, protein synthesis and amino acid metabolism. Enrichment analyses suggest a dysregulation of nitrogen metabolism pathways, which may lead to impaired maintenance of tissue function and dysregulated energy metabolism in tilapia.

Keywords

Perfluorooctanoic acid (PFOA) / Electrospray ionization-mass spectrometry (ESI-MS) / Fish skin mucus / Nitrogen metabolism / Biological Sciences / Biochemistry and Cell Biology

References

[1] VierkeL, StaudeC, Biegel-EnglerA, DrostW, SchulteCEnviron. Sci. Eur., 2012, 24: 11.

[2] PrevedourosK, CousinsI T, BuckR C, KorzeniowskiS HEnviron. Sci. Technol., 2006, 40: 32.

[3] MahinroostaR, SenevirathnaLJ. Environ. Manage., 2020, 255: 109896.

[4] WeiY, Chan LeoL, WangD, ZhangH, WangJ, DaiJJ. Proteome Res., 2008, 7: 1729.

[5] WangZ, DeWittJ C, HigginsC P, CousinsI TEnviron. Sci. Technol., 2017, 51: 2508.

[6] HuangC, ZhangY, ZhangQ, HeD, DongS, XiaoXTalanta, 2024, 280: 126693.

[7] ZhengL, ZhengY, LiuY, LongSTalanta, 2019, 194: 1.

[8] ChenH, MunozG, DuyS V, ZhangL, YaoY, ZhaoZ, YiL, LiuM, SunH, LiuJ, SauvéSEnviron. Sci. Technol., 2020, 54: 14254.

[9] FangS, ChenX, ZhaoS, ZhangY, JiangW, YangL, ZhuLEnviron. Sci. Technol., 2014, 48: 2173.

[10] DuD, LuY, ZhouY, LiQ, ZhangM, HanG, CuiH, JeppesenEJ. Hazard. Mater., 2021, 405: 124681.

[11] LeeJ W, ChoiK, ParkK, SeongC, YuS D, KimPSci. Total Environ., 2020, 707: 135334.

[12] LiuJ, LuH, NingY, HuaX, PanW, GuY, DongD, LiangDAnalyst, 2022, 147: 3930.

[13] FangZ, LiY, LiY, YangD, ZhangH, JonesK C, GuC, LuoJEnviron. Sci. Technol., 2021, 55: 9548.

[14] GallowayJ E, MorenoA V P, LindstromA B, StrynarM J, NewtonS, MayA A, WeaversL KEnviron. Sci. Technol., 2020, 54: 7175.

[15] DunnW B, BaileyN J C, JohnsonH EThe Analyst, 2005, 130: 606.

[16] SaitoK, MatsudaFAnnu. Rev. Plant Biol., 2010, 61: 463.

[17] Fernández-AlacidL, SanahujaI, Ordóñez-GrandeB, Sánchez-NuñoS, HerreraM, IbarzAAquaculture, 2019, 499: 185.

[18] ZacconeG, FasuloS, LicataA, Lo CascioPBasic Appl. Histochem., 1985, 29: 135

[19] ReverterM, Tapissier-BontempsN, LecchiniD, BanaigsB, SasalPFishes, 2018, 3: 41.

[20] LuY, ZhangY, DengY, JiangW, ZhaoY, GengJ, DingL, RenHEnviron. Sci. Technol., 2016, 50: 4054.

[21] E. D. R., SkeltonD M, DavisJ M, VilleneuveD L, CavallinJ E, SchroederA, JensenK M, AnkleyG T, ColletteT WEnviron. Sci. Technol., 2015, 49: 3091.

[22] WuX, YangS-A, KanY, LiM, DongJ, QiuT, GuY, ZhaoY, LiangDAnal. Chem., 2024, 96: 9416.

[23] LazadoC C, SkovP VFishes, 2019, 4: 57.

[24] HintonD E, SegnerH, BraunbeckTTarget Organ Toxicity in Marine and Freshwater Teleosts: Organs, 2017Boca RatonCRC Press224.

[25] WolfJ C, WolfeM JToxicol. Pathol., 2005, 33: 75.

[26] CattleyR C, CullenJ MFundamentals of Toxicologic Pathology, 2018ThirdLos AngelesSAGE Publications Inc.

[27] YuW, SunQ, QuL, LiuT, YiS, ZhangG, ChenH, LuoLFood Chem., 2024, 458: 140278.

[28] LuH, YeJ, WeiY, ZhangH, ChinginK, FrankevichV, ChenHChin. Chem. Lett., 2025, 36: 110077.

[29] HuangL, WangJ, JiangH, ChenL, ChenHChin. Chem. Lett., 2025, 36: 109896.

[30] ZhangX, LiuY, ZhangJ, HuZ, HuB, DingL, JiaL, ChenHTalanta, 2011, 85: 1665.

[31] SuR, YangT, ZhangX, LiN, ZhaiX, ChenHTRAC Trends Anal. Chem., 2023, 158: 116823.

[32] ZhangX, LiuJ, XiongJ, JiY, ZhangY, ChenH, YangS, ChenHInt. J. Mass Spectrom., 2018, 434: 100.

[33] GuyonR, RakotomangaM, AzzouziN, CoutanceauJ P, BonilloC, D’CottaH, PepeyE, SolerL, Rodier-GoudM, D’HontA, ConteM A, van BersN E, PenmanD J, HitteC, CrooijmansR P, KocherT D, Ozouf-CostazC, BaroillerJ F, GalibertFBMC Genomics, 2012, 13: 222.

[34] NingL-J, HeA-Y, LiJ-M, LuD-L, JiaoJ-G, LiL-Y, LiD-L, ZhangM-L, ChenL-Q, DuZ-YBiochim. Biophys. Acta: Mol. Cell Biol. Lipids, 2016, 1861: 1036.

[35] ElbahnasawyM A, El-NaggarH A, Abd-El RahmanI E, KalabaM H, MoghannemS A, Al-OtibiF, AlahmadiR M, AbdelzaherO F, MabroukM M, GewidaA G A, AbdEl-KaderM F, HasaballahA ISeparations, 2023, 10: 173.

[36] GaoF, LuM, WangZ, LiuZ, KeX, ZhangD, CaoJInt. J. Biol. Macromol., 2023, 225: 27.

[37] NakharuthaiC, BoonanuntanasarnS, KaewdaJ, ManassilaPAnimals, 2023, 13: 986.

[38] ShijaV M, AmoahK, CaiJFishes, 2023, 8: 366.

[39] YostawonkulJ, KambleM T, SakunaK, MadyodS, SukkarunP, MedheS V, RodkhumC, PiraratN, SewakaMAnimals, 2023, 13: 1798.

[40] CaoL, YinG, DuJ, JiaR, GaoJ, ShaoN, LiQ, ZhuH, ZhengY, NieZ, DingW, XuGAnimals, 2023, 13: 341.

[41] LiZ-H, XingS, LiP, HeS, CaoZ, WangX, CaoX, LiuB, YouHAquat. Toxicol., 2023, 257: 106441.

[42] HuX, MengL-J, LiuH-D, GuoY-S, LiuW-C, TanH-X, LuoG-ZSci. Total Environ., 2023, 901: 165921.

[43] El-SayedA-F M, FitzsimmonsKRev. Aquac., 2023, 15: 6.

[44] GherbawyY A, ThabetM A, SultanSInt. Microbiol., 2024, 27: 559.

[45] LiuJ, LuH, NingY, HuaX, PanW, GuY, DongD, LiangDAnalyst, 2022, 147: 3930.

[46] WuX, LiM, YangS, DongJ, PanW, NingY, HuaX, DongD, LiangDAnal. Chem., 2023, 95: 7863.

[47] FukudaT, MajumderK, ZhangH, MatsuiT, MineYJ. Funct. Foods, 2017, 28: 235.

[48] BraunM H, SteeleS L, EkkerM, PerryS FAm. J. Physiol. Renal Physiol., 2009, 296: F994.

[49] ChadwickT D, WrightP AJ. Exp. Biol., 1999, 202: 2653.

[50] Essex-FraserP A, SteeleS L, BernierN J, MurrayB W, StevensE D, WrightP AJ. Biol. Chem., 2005, 280: 20268.

[51] TerjesenB FBergen Univ. (Norway). Dept. of ZMangor-JensenA, FyhnH JFish Physiol. Biochem., 1998, 18: 189.

[52] ZimmerA M, WoodC MJ. Exp. Biol., 2015, 218: 1467

[53] ZimmerA M, WrightP A, WoodC MProc. R. Soc. B Biol. Sci., 2014, 281: 20141422.

[54] BrosnanJ T, BrosnanM EAmino Acids, 2013, 45: 413.

[55] AlbarracínS L, BaldeónM E, SangronisE, PetruschinaA C, ReyesF G RArch. Latinoam. Nutr., 2016, 66: 101

RIGHTS & PERMISSIONS

Jilin University, The Editorial Department of Chemical Research in Chinese Universities and Springer-Verlag GmbH