Abstract
The contamination of toxic heavy metals in aquatic environments has garnered significant global attention due to its detrimental effects on marine organisms and human health. Hexavalent chromium is a typical environmental and occupational heavy metal pollutant, identified as carcinogenic heavy metal. This study aimed to assess the impact of different Cr (VI) concentrations (0.05–2.5 mg/L) on Urechis unicinctus (U. unicinctus) by investigating bioaccumulation, antioxidant defense system, expression of resistance-related genes, and histological issues. A clear concentration-effect relationship was observed in the bioaccumulation of Cr (VI) in muscle tissues of U. unicinctus. Moreover, exposure to Cr (VI) can alter the activities of lysozyme (LSZ), catalase (CAT), and superoxide dismutase (SOD) to enhance cellular defense mechanisms in U. unicinctus. Likewise, maintained the normal protein structure and functional stability by regulating protein folding. The heat shock cognitive protein (HSC70) gene showed an upward and then downward trend after Cr (VI) exposure. At 12 h, the HSC70 gene expression reached the maximum values of 4.75 and 4.61-fold in the 0.1 and 1.5 mg/L groups, respectively. The organism produced a large number of free radicals, and elevated level of metallothionein (MT) was used to scavenge free radicals and alleviate oxidative stress. Additionally, histopathological examination revealed disorganization in the midgut, atrophic changes in intestinal connective tissue, uneven distribution in respiratory tissues, and irregular shape with a significant reduction in epithelial cells within the gastric cavity. These findings can serve as a valuable reference for elucidating the toxicity mechanisms of heavy metals towards marine benthic organisms and enhancing water environment monitoring strategies.
Similar content being viewed by others
Data availability
The authors confirm that the data supporting the findings of this study are available within the article.
References
Abalaka SE, Enem SI, Idoko IS, Sani NA, Tenuche OZ, Ejeh SA et al (2020) Heavy metals bioaccumulation and health risks with associated histopathological changes in clarias gariepinus from the kado fish market, Abuja Nigeria. J Health Poll 10(26):200602. https://doi.org/10.5696/2156-9614-10.26.200602
Aigbe UO, Osibote OA (2020) A review of hexavalent chromium removal from aqueous solutions by sorption technique using nanomaterials. J Environ Chem Eng 8(6):104503. https://doi.org/10.1016/j.jece.2020.104503
Balali-Mood M, Naseri K, Tahergorabi Z, Khazdair MR, Sadeghi M (2021) Toxic mechanisms of five heavy metals: mercury, lead, chromium, cadmium, and arsenic. Front Pharmacol 12:643972. https://doi.org/10.3389/fphar.2021.643972
Boudou A, Ribeyre F (2018) Fish biological model for experimental studies in ecotoxicology. In: Aquatic ecotoxicology: fundamental concepts and methodologies, 2nd edn. CRC Press, France, pp 127–162
Cainelli G, Cardillo G (2012) Chromium oxidations in organic chemistry, 1st edn. Springer Verlag, New York, pp 1–211
Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198(1):116–126. https://doi.org/10.1111/j.0105-2896.2004.00116.x
Chen H, Zhang M, Wu G, Chen L, Pan D (2010) Accumulation and release characteristics of Eriocheir sinensis for pb and cd. Acta Hydrobiol Sin 34:828–836. https://doi.org/10.3724/SP.J.1035.2010.00828
Chen L, Ma L, Bai Q, Zhu X, Zhang J, Wei Q, Li D, Gao C, Li J, Zhang Z (2014) Heavy metal-induced metallothionein expression is regulated by specific protein phosphatase 2A complexes. J Biol Chem 289(32):22413–22426. https://doi.org/10.1074/jbc.M114.548677
Chen QY, DesMarais T, Costa M (2019) Metals and mechanisms of carcinogenesis. Annu Rev Pharmacol Toxicol 59:537–554. https://doi.org/10.1146/annurev-pharmtox-010818-021031
Chen W, Zhang S, Sun Y, Tian B, Song L, Xu Y, Liu T (2021) Effects of substrate on the physiological characteristics and intestinal microbiota of echiura worm (Urechis unicinctus) juveniles. Aquaculture 530:735710. https://doi.org/10.1016/j.aquaculture.2020.735710
Cheng YH, Lai CM, Lin KS, Wang SSS (2017) Effects of metal oxide nanoparticles on the structure and activity of lysozyme. Colloids Surfaces B Biointerf 151:344–353
Colovic MB, Vasic VM, Djuric DM, Krstic DZ (2018) Sulphur-containing amino acids: protective role against free radicals and heavy metals. Curr Med Chem 25(3):324–335. https://doi.org/10.2174/0929867324666170609075434
Edwards KC (2021) Chromium (III) interaction with transferrin and transferrin receptor. University of Alabama Libraries, Tuscaloosa, Alabama, pp 1–157
El-Sappah AH, Seif MM, Abdel-Kader HH, Soaud SA, Elhamid MAA, Abdelghaffar AM, El-Sappah HH, Sarwar H, Yadav V, Maitra P (2022) Genotoxicity and trace elements contents analysis in Nile tilapia (Oreochromis niloticus) indicated the levels of aquatic contamination at three egyptian areas. Front Veterin Sci 9:170. https://doi.org/10.3389/fvets.2022.818866
Fang YZ, Yang S, Wu G (2002) Free radicals, antioxidants, and nutrition. Nutrition 18(10):872–879. https://doi.org/10.1016/S0899-9007(02)00916-4
Gao Y, Xia J (2011) Chromium contamination accident in China: viewing environment policy of China. ACS Publications. https://doi.org/10.1021/es203101f
Gong J, Zhao R, Deng J, Zhao Y, Zuo J, Huang L, Jing M (2018) Genetic diversity and population structure of penis fish (Urechis unicinctus) based on mitochondrial and nuclear gene markers. Mitochondrial DNA Part A 29(8):1261–1268. https://doi.org/10.1080/24701394.2018.1444039
Gong Y, Chai M, Ding H et al (2020) Bioaccumulation and human health risk of shellfish contamination to heavy metals and as in most rapid urbanized Shenzhen, China. Environ Sci Pollut Res 27:2096–2106. https://doi.org/10.1007/s11356-019-06580-2
Gunarto G, Tampangalo BR, Muliani M (2021) The application of erythromycin, elbayou, and Rica-1 probiotic in the rearing of Scylla paramamosain mud crab larvae development into the crablet stage. Thalassas An Int J Mar Sci 37(2):465–475. https://doi.org/10.1007/s41208-021-00327-y
He F, Liu Q, Jing M, Wan J, Huo C, Zong W, Tang J, Liu R (2021) Toxic mechanism on phenanthrene-induced cytotoxicity, oxidative stress and activity changes of superoxide dismutase and catalase in earthworm (Eisenia foetida): a combined molecular and cellular study. J Hazard Mater 418:126302. https://doi.org/10.1016/j.jhazmat.2021.126302
Ibrahim KS (2011) Isolation and pathological study of branchiomycosis from the commercial pond of common carp (Cyprinus Carpio) fish, in governorate of Duhok/Iraq. Iraqi J Vet Med 35(1):1–9
Ighodaro O, Akinloye O (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54(4):287–293. https://doi.org/10.1016/j.ajme.2017.09.001
Impellitteri F, Curpăn AS, Plăvan G, Ciobica A, Faggio C (2022) Hemocytes: a useful tool for assessing the toxicity of microplastics, heavy metals, and pesticides on aquatic invertebrates. Int J Environ Res Public Health 19(24):16830. https://doi.org/10.3390/ijerph192416830
Jing M, Song W, Liu R (2016) Binding of copper to lysozyme: spectroscopic, isothermal titration calorimetry and molecular docking studies. Spectrochim Acta Part A Mol Biomol Spectrosc 164:103–109
Juárez-Rebollar D, Rios C, Nava-Ruíz C, Méndez-Armenta M (2017) Metallothionein in brain disorders. Oxidative Med Cell Longev 2017:5828056. https://doi.org/10.1155/2017/5828056
Julian D, Passman WE, Arp AJ (1996) Water lung and body wall contributions to respiration in an echiuran worm. Respir Physiol 106(2):187–198. https://doi.org/10.1016/S0034-5687(96)00073-4
Kadim MK, Risjani Y (2022) Biomarker for monitoring heavy metal pollution in aquatic environment: an overview toward molecular perspectives. Emerg Contam 8:195–205. https://doi.org/10.1016/j.emcon.2022.02.003
Khangarot BS, Rathore RS, Tripathi DM (1999) Effects of chromium on humoral and cell-mediated immune responses and host resistance to disease in a freshwater catfish, saccobranchus fossilis (Bloch). Ecotoxicol Environ Safety 43(1):11–20. https://doi.org/10.1006/eesa.1998.1722
Kumar P, Sivaperumal P, Manigandan V et al (2021) Assessment of potential human health risk due to heavy metal contamination in edible finfish and shellfish collected around ennore coast, India. Environ Sci Pollut Res 28:8151–8167. https://doi.org/10.1007/s11356-020-10764-6
Lacalle RG, Aparicio JD, Artetxe U, Urionabarrenetxea E, Polti MA, Soto M, Garbisu C, Becerril JM (2020) Gentle remediation options for soil with mixed chromium (VI) and lindane pollution: biostimulation, bioaugmentation, phytoremediation and vermiremediation. Heliyon 6(8):e04550. https://doi.org/10.1016/j.heliyon.2020.e04550
Lei SY, Lu MM, Ding LF, Zhu JQ (2013) The morphology of the digestive tract of Phascoloma esculenta. J Biol 30(2):33–36
Lejri R, Younes SB, Ellafi A, Bouallegue A, Moussaoui Y, Chaieb M, Mekki A (2022) Physico-chemical, microbial and toxicity assessment of industrial effluents from the southern tunisian tannery. J Water Process Eng 47:102686. https://doi.org/10.1016/j.jwpe.2022.102686
Li L, Chen H, Bi R, Xie L (2015) Bioaccumulation, subcellular distribution, and acute effects of chromium in japanese medaka (Oryzias latipes). Environ Toxicol Chem 34(11):2611–2617. https://doi.org/10.1002/etc.3112
Li J, Lu J, Asakiya C, Huang K, Zhou X, Liu Q, He X (2022) Extraction and identification of three new Urechis unicinctus visceral peptides and their antioxidant activity. Mar Drugs 20(5):293. https://doi.org/10.3390/md20050293
Liu X, Zhang Z, Ma X, Li X, Zhou D, Gao B, Bai Y (2016) Sulfide exposure results in enhanced sqr transcription through upregulating the expression and activation of HSF1 in echiuran worm Urechis unicinctus. Aquatic Toxicol 170:229–239. https://doi.org/10.1016/j.aquatox.2015.11.021
Liu D, Liu H, Wang S, Chen J, Xia Y (2018) The toxicity of ionic liquid 1-decylpyridinium bromide to the algae Scenedesmus obliquus: growth inhibition, phototoxicity, and oxidative stress. Sci Total Environ 622:1572–1580. https://doi.org/10.1016/j.scitotenv.2017.10.021
Liu F, Li XN, Ji Y, Liu C, Sun T, Zhao Y, Nicolage CG, Dediu L (2019) The biological characteristics and utilization of Urechis unicinctus. AgroLife Sci J 8:146–152
Loomis D, Guha N, Hall AL, Straif K (2018) Identifying occupational carcinogens: an update from the IARC monographs. Occup Environ Med 75(8):593–603. https://doi.org/10.1136/oemed-2017-104944
Lorenzon S, Francese M, Smith VJ, Ferrero EA (2001) Heavy metals affect the circulating haemocyte number in the shrimp Palaemon elegans. Fish Shellf Immunol 11(6):459–472. https://doi.org/10.1006/fsim.2000.0321
Ma X, Liu X, Zhou D, Bai Y, Gao B, Zhang Z, Qin Z (2016) The NF-κB pathway participates in the response to sulfide stress in Urechis unicinctus. Fish Shellf Immunol 58:229–238. https://doi.org/10.1016/j.fsi.2016.09.020
Madboli AENA, Seif MM (2021) Immunohistochemical, histopathological, and biochemical studies of the NF-ҡB P65 marker in rat ovaries experimentally intoxicated by cadmium and the protective effect of the purslane plant extract. Environ Sci Poll Res 28:17613–17626
Min EY, Ahn TY, Kang JC (2016) Bioaccumulation, alterations of metallothionein, and antioxidant enzymes in the mullet Mugil cephalus exposed to hexavalent chromium. Fish Aquatic Sci 19:19. https://doi.org/10.1186/s41240-016-0020-1
Mohan D, Pittman CU Jr, Steele PH (2006) Pyrolysis of wood/biomass for bio-oil: a critical review. Energy Fuels 20(3):848–889. https://doi.org/10.1021/ef0502397
Ngo HTT, Nguyen TD, Nguyen TTH, Le TT, Nguyen DQ (2022) Adverse effects of toxic metal pollution in rivers on the physiological health of fish. Toxics 10(9):528. https://doi.org/10.3390/toxics10090528
Pratush A, Kumar A, Hu Z (2018) Adverse effect of heavy metals (as, pb, hg, and cr) on health and their bioremediation strategies: a review. Int Microbiol 21:97–106. https://doi.org/10.1007/s10123-018-0012-3
Rahman Z, Singh VP (2019) The relative impact of toxic heavy metals (THMs)(arsenic (as), cadmium (Cd), chromium (cr (VI)), mercury (Hg), and lead (Pb)) on the total environment: an overview. Environ Monitor Assess 191:1–21. https://doi.org/10.1007/s10661-019-7528-7
Rajeshkumar S, Mini J, Munuswamy N (2013) Impact of heavy metals on antioxidant activity in different tissue of milk fish Chanos chanos. Int J Appl Biol Pharm Technol 4(1):272–279
Rong C, Sainan G, Jialang Z (2018) Effect of cadmium exposure on antioxidant and immune responses and the ameliorative role of blue LEDs pre-exposure in the liver and ovary of zebrafish. Asian J Ecotoxicol 1:169–178
Sarkar S, Yadav P, Trivedi R, Bansal AK, Bhatnagar D (1995) Cadmium-induced lipid peroxidation and the status of the antioxidant system in rat tissues. J Trace Elements Med Biol 9(3):144–149. https://doi.org/10.1016/S0946-672X(11)80038-6
Seif MM, Madboli AN, Marrez DA, Aboulthana WM (2019) Hepato-renal protective effects of egyptian purslane extract against experimental cadmium toxicity in rats with special emphasis on the functional and histopathological changes. Toxicol Rep 6:625–631
Seif M, Abd El-Aziz T, Sayed M, Wang Z (2021) Zingiber officinale ethanolic extract attenuates oxidative stress, steroidogenic gene expression alterations, and testicular histopathology induced by sodium arsenite in male rats. Environ Sci Poll Res 28:19783–19798
Shao M, Zhang Z, Kang K, Ma Z, Wang K (2003) Histology and cytology of digestive tract in Urechis unicoinctus von drasche. J Fish Sci China 10:265–268 (in Chinese)
Shekhawat K, Chatterjee S, Joshi B (2015) Chromium toxicity and its health hazards. Int J Adv Res 3(7):167–172
Sonone SS, Jadhav S, Sankhla MS, Kumar R (2020) Water contamination by heavy metals and their toxic effect on aquaculture and human health through food chain. Lett Appl NanoBioSci 10(2):2148–2166. https://doi.org/10.33263/LIANBS102.21482166
Stoepler TM, Castillo JC, Lill JT, Eleftherianos I (2012) A simple protocol for extracting hemocytes from wild caterpillars. JoVE (Journal of Visualized Experiments) 69:e4173. https://doi.org/10.3791/4173
Sung WS, Park SH, Lee DG (2008) Antimicrobial effect and membrane-active mechanism of urechistachykinins, neuropeptides derived from Urechis unicinctus. FEBS Letters 582(16):2463–2466. https://doi.org/10.1016/j.febslet.2008.06.015
TaghavizadehYazdi ME, Amiri MS, Nourbakhsh F, Rahnama M, Forouzanfar F, Mousavi SH (2021) Bio-indicators in cadmium toxicity: role of HSP27 and HSP70. Environ Sci Poll Res 28:26359–26379. https://doi.org/10.1007/s11356-021-13687-y
Wakeel A, Xu M, Gan Y (2020) Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and associated cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. Int J Mol Sci 21(3):728. https://doi.org/10.3390/ijms21030728
Wan J, Liu F, Wang G, Liang W, Peng C, Zhang W, Lin K, Yang J (2021) Exploring different mechanisms of biochars in removing hexavalent chromium: sorption, reduction and electron shuttle. Bioresource Technol 337:125382. https://doi.org/10.1016/j.biortech.2021.125382
Wang S, Zhang Z, Cui H, Kang KH, Ma Z (2010) The effect of toxic sulfide exposure on oxygen consumption and oxidation products in Urechis unicinctus (echiura: urechidae). J Ocean Univ China 9:157–161. https://doi.org/10.1007/s11802-010-0157-y
Wang LL, Xia B, Chen BJ, Li CH, Tang XX (2012) Effects of cadmium stress on antioxidant defense system of Patinopecten yessoensis. Mar Environ Sci 31:39–42. https://doi.org/10.3969/j.issn.1007-6336.2012.01.009 (In Chinese)
Wang J, Yang X, Wang J, Xu C, Zhang W, Liu R, Zong W (2016) Probing the binding interaction between cadmium (ii) chloride and lysozyme. New J Chem 40(4):3738–3746. https://doi.org/10.1039/C5NJ02911B
Wang C, Tang M, Chen Y, Liu D, Xie S, Zou J, Tang H, Li Q, Zhou A (2022) Expression of genes related to antioxidation, immunity, and heat stress in Gambusia affinis exposed to the heavy metals cu and zn. Ecotoxicol Environ Safe 247:114269. https://doi.org/10.1016/j.ecoenv.2022.114269
Wu Y (2005) Accumulation of copper in Chlamys farreri tissues and its effect on catalase activity. Chinese J Appl Environ Biol 11(5):559. https://doi.org/10.3321/j.issn:1006-687X.2005.05.009
Wu G, Yi Y (2015) Effects of dietary heavy metals on the immune and antioxidant systems of galleria mellonella larvae. Compar Biochem Physiol Part C Toxicol Pharmacol 167:131–139. https://doi.org/10.1016/j.cbpc.2014.10.004
Xiong JQ, Kim SJ, Kurade MB, Govindwar S, Abou-Shanab RA, Kim JR, Ron HS, Khan MA, Jeon BH (2019) Combined effects of sulfamethazine and sulfamethoxazole on a freshwater microalga, Scenedesmus obliquus: toxicity, biodegradation, and metabolic fate. J Hazard Mater 370:138–146. https://doi.org/10.1016/j.jhazmat.2018.07.049
Xu XH, Meng X, Gan HT (2019) Immune response, MT and HSP70 gene expression, and bioaccumulation induced by lead exposure of the marine crab Charybdis japonica. Aquat Toxicol 2019(210):98–105
Zahedi S, Mirvaghefi A, Rafati M, Mehrpoosh M (2013) Cadmium accumulation and biochemical parameters in juvenile persian sturgeon, Acipenser persicus, upon sublethal cadmium exposure. Comp Clin Pathol 22:805–813. https://doi.org/10.1007/s00580-012-1482-x
Zhang QD (2006) Effects of lignin on soil phosphate adsorption. J Agro-Environ Sci 25(1):152–155. https://doi.org/10.1111/j.1744-7917.2006.00098.x
Zhang Z, Shao M, Kang K, Jin Z (2003) Studies on the tolerating mechanism for sulfide in Urechis unicinctus (echiura: urechidae)-cytological observation on Urechis unicinctus in different hydrogen sulfide environment. Chin J Oceanol Limnol 21(1):86–90. https://doi.org/10.1007/BF02842765
Zhang TT, Xu YS, Wu TM (2012) Assessment of the content of lead in seafood from Hongsha Bay in Sanya. Food Ind 33(6):88–89
Zhang CM, Chen YH, Wu CW, Li XT (2013) Effects of Cr6+ on peripheral blood cell and antioxidant enzyme activity (SOD: CAT) of Nibea japonica. Oceanol. Limnol. Sin 44:332–336
Zhang M, Chen H, Wu G (2016) In vivo absorption and release characteristics of pb and cd in diet in Eriocheir sinensis. J Fish China 40(9):1431–1439
Zhang Y, Luo J, Zhu T, Yang Z, Jin M, Jiao L, Zhou Q (2022) Excessive dietary Cr6+ had no adverse effect on mud crab (scylla paramamosain) but provoke consumers health risk. Aquacult Rep 27:101397. https://doi.org/10.1016/j.aqrep.2022.101397
Zhu XY, Gan HT, Meng X, Yao HY, Xu GC, Xu JT, Liu TH, Cao LX, Xu XH (2019) Effects of cadmium on non-specific immunity and bioaccumulation of Urechis unicinctus. Asian J Ecotoxicol 1:106–115
Funding
This study was supported by grant from the Subei Science and Technology Special Project, Jiangsu Province Science and Technology Department (SZ-LYG202124, LYG-SZ201814); Priority Academic Program Development of Jiangsu Higher Education Institutions (CXKT2020); Lianyungang City Science and Technology Development Project (CN1411); Lianyungang City Huaguoshan Talents Plan (KK20100); Jiangsu Ocean University Graduate Research and Practice Innovation Program Project (KYCX2023-71; KYCX2023-105); A Project funded by the Priority Academic Program Development of Jiangsu Higher Education; Natural Science Foundation of the Jiangsu Higher Education Institutions of China (23KJB180005); and Natural Science Foundation of Jiangsu Province (BK20230690).
Author information
Authors and Affiliations
Contributions
SL: investigation, data curation, writing—original draft; LZ: investigation, data curation, writing—original draft; ZX, LW: data curation, writing—review and editing; SW: writing—review and editing; MS: validation, writing—review and editing; XX: supervision, validation, resources, project administration, funding acquisition.
Corresponding author
Ethics declarations
Ethical approval
The Animal Ethics Committee of Jiangsu Ocean University approved all experiments.
Consent to participate
Not applicable
Consent for publication
All authors review and approve the manuscript for publication.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Mohamed M. Abdel-Daim
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Xinghong Xu supervision
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, S., Zhu, L., Xu, Z. et al. Toxic effect of chromium on nonspecific immune, bioaccumulation, and tissue structure of Urechis unicinctus. Environ Sci Pollut Res 31, 23077–23090 (2024). https://doi.org/10.1007/s11356-024-32441-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-024-32441-8