Abstract
Perfluorinated compounds (PFCs) are persistent organic contaminants that are highly toxic to the environment and bioaccumulate, but their ecotoxic effects on aquatic plants remain unclear. In this study, the submerged plant Vallisneria natans was treated with short-term (7 days) and long-term (21 days) exposures to perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) at concentrations of 0, 0.01, 0.1, 1.0, 5.0, and 10 mg/L, respectively. The results showed that both high concentrations of PFOA and PFOS inhibited the growth of V. natans and triggered the increase in photosynthetic pigment content in leaves. The oxidative damage occurred mainly in leaves, but both leaves and roots gradually built up tolerance during the stress process without serious membrane damage. Both leaves and roots replied to short-term stress by activating superoxide dismutase (SOD), catalase (CAT) and polyphenol oxidase (PPO), while peroxidase (POD) was involved under high concentration stress with increasing exposure time. Leaves showed a dose–effect relationship in integrated biomarker response (IBR) values under short-term exposure, and the sensitivity of roots and leaves to PFOS was higher than that of PFOA. Our findings help to increase knowledge of the toxic effects of PFCs and have important reference value for risk assessment and environmental remediation of PFCs in the aquatic ecosystem.
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References
Bai G, Zhang Y, Yan P et al (2020) Spatial and seasonal variation of water parameters, sediment properties, and submerged macrophytes after ecological restoration in a long-term (6 year) study in Hangzhou west lake in China: Submerged macrophyte distribution influenced by environmental variables. Water Res 186:116379. https://doi.org/10.1016/j.watres.2020.116379
Bhaduri AM, Fulekar MH (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Biotechnol 11:55–69. https://doi.org/10.1007/s11157-011-9251-x
Boudreau TM, Sibley PK, Mabury SA et al (2003) Laboratory evaluation of the toxicity of perfluorooctane sulfonate (PFOS) on Selenastrum capricornutum, Chlorella vulgaris, Lemna gibba, Daphnia magna, and Daphnia pulicaria. Arch Environ Contam Toxicol 44:307–313. https://doi.org/10.1007/s00244-002-2102-6
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Cang J, Zhao H (2013) Experimental course of plant physiology. Higher Education Press
Chen C, Fang Y, Cui X, Zhou D (2022) Effects of trace PFOA on microbial community and metabolisms: microbial selectivity, regulations and risks. Water Res 226:119273. https://doi.org/10.1016/j.watres.2022.119273
Deng G, Li M, Li H et al (2014) Exposure to cadmium causes declines in growth and photosynthesis in the endangered aquatic fern (Ceratopteris pteridoides). Aquat Bot 112:23–32. https://doi.org/10.1016/j.aquabot.2013.07.003
Dreyer A, Matthias V, Weinberg I, Ebinghaus R (2010) Wet deposition of poly- and perfluorinated compounds in Northern Germany. Environ Pollut 158:1221–1227. https://doi.org/10.1016/j.envpol.2010.01.030
Du D, Lu Y, Zhou Y et al (2021) Bioaccumulation, trophic transfer and biomagnification of perfluoroalkyl acids (PFAAs) in the marine food web of the South China Sea. J Hazard Mater 405:124681. https://doi.org/10.1016/j.jhazmat.2020.124681
Eriksson U, Haglund P, Kärrman A (2017) Contribution of precursor compounds to the release of per- and polyfluoroalkyl substances (PFASs) from waste water treatment plants (WWTPs). J Environ Sci 61:80–90. https://doi.org/10.1016/j.jes.2017.05.004
Fan P, Liu C, Ke Z et al (2022) Growth and physiological responses in a submerged clonal aquatic plant and multiple-endpoint assessment under prolonged exposure to ciprofloxacin. Ecotoxicol Environ Saf 239:113690. https://doi.org/10.1016/j.ecoenv.2022.113690
Fan P, Yin J, Zhong G, Wu Z (2020) Ascorbic acid alleviation of manganese-induced toxicity in Vallisneria natans (Lour.) Hara. Environ Sci Pollut Res 27:32695–32706. https://doi.org/10.1007/s11356-020-09479-5
Faverney CR, Devaux A, Lafaurie M et al (2001) Toxic effects of wastewaters collected at upstream and downstream sites of a purification station in cultures of rainbow trout hepatocytes. Arch Environ Contam Toxicol 41:129–141. https://doi.org/10.1007/s002440010230
Filipovic M, Berger U, McLachlan MS (2013) Mass balance of perfluoroalkyl acids in the Baltic Sea. Environ Sci Technol 47:4088–4095. https://doi.org/10.1021/es400174y
Gao J (2006) Experimental guidance for plant physiology. Higher Education Press
Gasparotto J, Chaves PR, Da Boit Martinello K, et al. (2018) Obese rats are more vulnerable to inflammation, genotoxicity and oxidative stress induced by coal dust inhalation than non-obese rats. Ecotoxicology and environmental safety 165:. https://doi.org/10.1016/j.ecoenv.2018.08.097
Gasparotto J, Chaves PR, Da Boit Martinello K, et al. (2019) Obesity associated with coal ash inhalation triggers systemic inflammation and oxidative damage in the hippocampus of rats. Food chem toxicol : int j publ Br Ind Biol Res Assoc 133:. https://doi.org/10.1016/j.fct.2019.110766
Grandjean P, Budtz-Jørgensen E (2013) Immunotoxicity of perfluorinated alkylates: calculation of benchmark doses based on serum concentrations in children. Environ Health 12:35. https://doi.org/10.1186/1476-069X-12-35
Gredilla A, Fdez-Ortiz De Vallejuelo S, Gomez-Nubla L, et al. (2017) Are children playgrounds safe play areas? Inorganic analysis and lead isotope ratios for contamination assessment in recreational (brazilian) parks. Environ Sci Pollut Res Int 24:. https://doi.org/10.1007/s11356-017-9831-6
Han H, Wu H, Zhi Y et al (2023) Impacts of bisphenol A on growth and reproductive traits of submerged macrophyte Vallisneria natans. Environ Sci Pollut Res 30:46383–46393. https://doi.org/10.1007/s11356-023-25521-8
Hu Z, Cui Y, Li M, Yu J (2015) Physiological effect of Vallisneria natans under different concentrations of nitrogen, phosphorus and chloramphenicol. Environmental Science 36:3248–3254. https://doi.org/10.13227/j.hjkx.2015.09.016
Hua Z, Li X, Zhang J, Gu L (2022) Removal potential of multiple perfluoroalkyl acids (PFAAs) by submerged macrophytes in aquatic environments: tolerance of Vallisneria natans and PFAA removal in submerged macrophyte-microbiota systems. J Hazard Mater 424:127695. https://doi.org/10.1016/j.jhazmat.2021.127695
Islam R, Kumar S, Karmoker J et al (2018) Bioaccumulation and adverse effects of persistent organic pollutants (POPs) on ecosystems and human exposure: a review study on Bangladesh perspectives. Environ Technol Innov 12:115–131. https://doi.org/10.1016/j.eti.2018.08.002
Jampeetong A, Brix H (2009) Oxygen stress in Salvinia natans: interactive effects of oxygen availability and nitrogen source. Environ Exp Bot 66:153–159. https://doi.org/10.1016/j.envexpbot.2009.01.006
Jeong T-Y, Yuk M-S, Jeon J, Kim SD (2016) Multigenerational effect of perfluorooctane sulfonate (PFOS) on the individual fitness and population growth of Daphnia magna. Sci Total Environ 569–570:1553–1560. https://doi.org/10.1016/j.scitotenv.2016.06.249
Ji Y, Yao Z, Zhang J et al (2018) Integrated biomarker responses of the submerged macrophyte Vallisneria spiralis via hydrological processes from Lake Poyang. China R Soc Open Sci 5:180729. https://doi.org/10.1098/rsos.180729
Kim J-H, Kim W-K (2016) Use of the integrated biomarker response to measure the effect of short-term exposure to dibenz[a, h]anthracene in common carp (Cyprinus carpio). Bull Environ Contam Toxicol 96:496–501. https://doi.org/10.1007/s00128-015-1726-y
Kong X, Wang T, Zhang X et al (2015) Ecological effects on aquatic plants induced by perfluorinated compounds II - bioaccumulation and physiological response of Ceratophyllum demersum in PFOS polluted water. Asian J Ecotoxicol 10:445–453
Kosaka N, Iguchi H, Ochiya T (2010) Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci 101:2087–2092. https://doi.org/10.1111/j.1349-7006.2010.01650.x
Lau C, Butenhoff JL, Rogers JM (2004) The developmental toxicity of perfluoroalkyl acids and their derivatives. Toxicol Appl Pharmacol 198:231–241. https://doi.org/10.1016/j.taap.2003.11.031
Lee JW, Choi K, Park K et al (2020) Adverse effects of perfluoroalkyl acids on fish and other aquatic organisms: a review. Sci Total Environ 707:135334. https://doi.org/10.1016/j.scitotenv.2019.135334
León-Mejía G, Machado MN, Okuro RT et al (2018) Intratracheal instillation of coal and coal fly ash particles in mice induces DNA damage and translocation of metals to extrapulmonary tissues. Sci Total Environ 625:589–599. https://doi.org/10.1016/j.scitotenv.2017.12.283
León-Mejía G, Silva LFO, Civeira MS, et al. (2016) Cytotoxicity and genotoxicity induced by coal and coal fly ash particles samples in V79 cells. Environ Sci Pollut Res Int 23:. https://doi.org/10.1007/s11356-016-7623-z
Li P, Sun J, Xie X et al (2021) Stress response and tolerance to perfluorooctane sulfonate (PFOS) in lettuce (Lactuca sativa). J Hazard Mater 404:124213. https://doi.org/10.1016/j.jhazmat.2020.124213
Li Y, Men B, He Y et al (2017) Effect of single-wall carbon nanotubes on bioconcentration and toxicity of perfluorooctane sulfonate in zebrafish (Danio rerio). Sci Total Environ 607–608:509–518. https://doi.org/10.1016/j.scitotenv.2017.06.140
Liu Y, Liu N, Zhou Y et al (2019) Growth and physiological responses in Myriophyllum spicatum L. exposed to linear alkylbenzene sulfonate. Enviro Toxic and Chemistry 38:2073–2081. https://doi.org/10.1002/etc.4475
Lu B, Qian J, Wang P et al (2020) Effect of perfluorooctanesulfonate (PFOS) on the rhizosphere soil nitrogen cycling of two riparian plants. Sci Total Environ 741:140494. https://doi.org/10.1016/j.scitotenv.2020.140494
Lu H, Ma Z, Zhang X (2018) Distribution characteristics of perfluorooctanoic acid (PFOA) in shallow groundwater of a fluorine industrial park in Shandong Province. IOP Conf Ser: Earth Environ Sci 189:032064. https://doi.org/10.1088/1755-1315/189/3/032064
Nordin AP, Da Silva J, De Souza CT, et al. (2018) In vitro genotoxic effect of secondary minerals crystallized in rocks from coal mine drainage. J Hazard Mater 346:. https://doi.org/10.1016/j.jhazmat.2017.12.026
Pérez F, Llorca M, Köck-Schulmeyer M et al (2014) Assessment of perfluoroalkyl substances in food items at global scale. Environ Res 135:181–189. https://doi.org/10.1016/j.envres.2014.08.004
Pi N, Ng JZ, Kelly BC (2017) Uptake and elimination kinetics of perfluoroalkyl substances in submerged and free-floating aquatic macrophytes: Results of mesocosm experiments with Echinodorus horemanii and Eichhornia crassipes. Water Res 117:167–174. https://doi.org/10.1016/j.watres.2017.04.003
Qian J, Lu B, Chen H et al (2019) Phytotoxicity and oxidative stress of perfluorooctanesulfonate to two riparian plants: Acorus calamus and Phragmites communis. Ecotoxicol Environ Saf 180:215–226. https://doi.org/10.1016/j.ecoenv.2019.04.078
Ramírez O, Sánchez De La Campa AM, Amato F et al (2019) Physicochemical characterization and sources of the thoracic fraction of road dust in a latin american megacity. Sci Total Environ 652:434–446. https://doi.org/10.1016/j.scitotenv.2018.10.214
Rodríguez-Varela M, Durán-Álvarez JC, Jiménez-Cisneros B et al (2021) Occurrence of perfluorinated carboxylic acids in Mexico City’s wastewater: a monitoring study in the sewerage and a mega wastewater treatment plant. Sci Total Environ 774:145060. https://doi.org/10.1016/j.scitotenv.2021.145060
Rojas JC, Sánchez NE, Schneider I et al (2019) Exposure to nanometric pollutants in primary schools: environmental implications. Urban Clim 27:412–419. https://doi.org/10.1016/j.uclim.2018.12.011
Satterfield CN, Bonnell AH (1955) Interferences in titanium sulfate method for hydrogen peroxide. Anal Chem 27:1174–1175. https://doi.org/10.1021/ac60103a042
Shen X, Hu Y (2006) Study on biological traits of submersed plant Vallisneria. Journal of Hefei Normal University 86–88. https://doi.org/10.3969/j.issn.1674-2273.2006.06.030
Shi Y, Pan Y, Wang J, Cai Y (2012) Distribution of perfluorinated compounds in water, sediment, biota and floating plants in Baiyangdian Lake, China. J Environ Monit 14:636–642. https://doi.org/10.1039/C1EM10772K
Wang JF, Feng YL (2004) The effect of light intensity on biomass allocation, leaf morphology and relative growth rate of two invasive plants. Chinese Journal of Plant Ecology 28:781–786. https://doi.org/10.17521/cjpe.2004.0102
Wang XH, Hong HS, Mu JL et al (2008) Polycyclic aromatic hydrocarbon (PAH) metabolites in marine fishes as a specific biomarker to indicate PAH pollution in the marine coastal environment. J Environ Sci Health, Part A 43:219–226. https://doi.org/10.1080/10934520701792662
Wang Y, Fu J, Wang T et al (2010) Distribution of perfluorooctane sulfonate and other perfluorochemicals in the ambient environment around a manufacturing facility in china. Environ Sci Technol 44:8062–8067. https://doi.org/10.1021/es101810h
Wang Z, Boucher JM, Scheringer M et al (2017) Toward a comprehensive global emission inventory of C 4 –C 10 perfluoroalkanesulfonic acids (PFSAs) and related precursors: focus on the life cycle of C 8 -based products and ongoing industrial transition. Environ Sci Technol 51:4482–4493. https://doi.org/10.1021/acs.est.6b06191
Wilcox J, Wang B, Rupp E et al (2015) Observations and assessment of fly ashes from high-sulfur bituminous coals and blends of high-sulfur bituminous and subbituminous coals: environmental processes recorded at the macro- and nanometer scale. Energy Fuels 29:7168–7177. https://doi.org/10.1021/acs.energyfuels.5b02033
Yang X, Ye C, Liu Y, Zhao F-J (2015) Accumulation and phytotoxicity of perfluorooctanoic acid in the model plant species Arabidopsis thaliana. Environ Pollut 206:560–566. https://doi.org/10.1016/j.envpol.2015.07.050
Zhang P, Sun L, Liu F et al (2022) Perfluorooctanoic acid and perfluorooctane sulfonic acid inhibit plant growth through the modulation of phytohormone signalling pathways: evidence from molecular and genetic analysis in Arabidopsis. Sci Total Environ 851:158287. https://doi.org/10.1016/j.scitotenv.2022.158287
Zhang W, Zhang Y, Taniyasu S et al (2013) Distribution and fate of perfluoroalkyl substances in municipal wastewater treatment plants in economically developed areas of China. Environ Pollut 176:10–17. https://doi.org/10.1016/j.envpol.2012.12.019
Zhang X, Lai T, Kong RY (2011) Biology of fluoro-organic compounds. In: Horváth IT (ed) Fluorous Chemistry. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 365–404
Zhao X-L, Li P, Qu C et al (2022) Phytotoxicity of environmental norfloxacin concentrations on the aquatic plant Spirodela polyrrhiza: evaluation of growth parameters, photosynthetic toxicity and biochemical traits. Comp Biochem Physiol c: Toxicol Pharmacol 258:109365. https://doi.org/10.1016/j.cbpc.2022.109365
Zhou L, Xia M, Wang L, Mao H (2016) Toxic effect of perfluorooctanoic acid (PFOA) on germination and seedling growth of wheat (Triticum aestivum L.). Chemosphere 159:420–425. https://doi.org/10.1016/j.chemosphere.2016.06.045
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This research was supported by the National Natural Science Foundation of China (No: 31270410 and 30670206).
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WZ: conceptualization, formal analysis, investigation, methodology. ZL: writing (original draft, review, and editing). ZK: writing (review and editing). ZW: supervision, writing (review and editing). All authors read and approved the final manuscript.
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Lin, Z., Zhou, W., Ke, Z. et al. Ecotoxicity of perfluorooctanoic acid and perfluorooctane sulfonate on aquatic plant Vallisneria natans. Environ Sci Pollut Res 31, 26646–26664 (2024). https://doi.org/10.1007/s11356-024-32705-3
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DOI: https://doi.org/10.1007/s11356-024-32705-3