Skip to main content
Log in

Histopathological examination and transcriptome analyses to assess the acute toxic effects of arsenite exposure on rare minnows (Gobiocypris rarus)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Arsenic is ubiquitously present in the aquatic environment. We investigated the acute toxic effects of arsenite [As(III)] exposure on rare minnows (Gobiocypris rarus) in vivo. The 96-h LC50 value for exposure to As(III) was 13.73 mg/L. As(III) bioaccumulation in different tissues was measured using inductively-coupled plasma mass spectrometry, and the extent of As(III) accumulation was, from greatest to least, liver > intestine > gills > muscle > kidney > testis > brain. Histological examination revealed that in As(III)-treated fish, numerous cellular and tissue alterations were present in the gill, liver, and intestine tissues. Moreover, transmission electron microscopy showed ultrastructural alterations in hepatocytes. We also performed transcriptome analyses to investigate As(III)-induced toxicity response in the liver of As(III)-treated fish; various oxidative-related genes were differentially expressed, and their expression levels were further validated using qPCR. This study is one of the many steps we aim to take on the way to promote the rare minnow to an international standard laboratory animal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahmeda MK, Habibullah-Al-Mamuna M, Parvina E, Akterb MS, Khan MS (2013) Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, tilapia (Oreochromis mossambicus). Exp Toxicol Pathol 65:903–909

    Article  CAS  Google Scholar 

  • Akter MS, Ahmed MK, Akhand MAA, Islam MM (2008) Acute toxicity of arsenic and mercuryto fresh water climbing perch, Anabas testudineus (Bloch). World J Zool 3(1):13–8

    Google Scholar 

  • Arriaza B, Amarasiriwardena D, Cornejo L, Standen V, Byrne S, Bartkus L et al. (2010) Exploring chronic arsenic poisoning in pre-Columbian Chilean mummies. J Archaeol Sci 37:1274–1278. https://doi.org/10.1016/j.jas.2009.12.030

    Article  Google Scholar 

  • Athikesavan S, Vincent S, Ambrose T, Velmurugan B (2004) Nickel induced histopathological changes in the different tissues of freshwater fish, Hypophthalmichthys molitrix (Valenciennes). J Environ Biol 27(2):391–395

    Google Scholar 

  • Bambino K, Zhang C, Austin C, Amarasiriwardena C, Arora M, Chu J et al. (2018) Inorganic arsenic causes fatty liver and interacts with ethanol to cause alcoholic liver disease in zebrafish. Dis Model Mech 11(2):dmm031575. https://doi.org/10.1242/dmm.031575

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W, Burkhardtholm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34

    Article  Google Scholar 

  • Bhowmik AK, Alamdar A, Katsoyiannis I, Shen H, Ali N, Ali SM et al. (2015) Mapping human health risks from exposure to trace metal contamination of drinking water sources in Pakistan. Sci Total Environ 538:306–316

    Article  CAS  Google Scholar 

  • Chen R, Hou R, Hong X, Yan S, Zha J (2019) Organophosphate flame retardants (OPFRs) induce genotoxicity in vivo: a survey on apoptosis, DNA methylation, DNA oxidative damage, liver metabolites, and transcriptomics. Environ Int 130:104914

    Article  CAS  Google Scholar 

  • Chen CJ, Chiou HY, Chiang MH, Lin LJ, Tai TY (1996) Dose-response relationship between ischemic heart disease mortality and long-term arsenic exposure. Arterioscler Thromb Vasc Biol 16:504–510

    Article  CAS  Google Scholar 

  • Chen Y, Ahsan H (2004) Cancer burden from arsenic in drinking water in Bangladesh. Am J Public Health 94:741–744

    Article  Google Scholar 

  • Chou BYH, Liao CM, Lin MC, Cheng HH (2006) Toxicokinetics/toxicodynamics of arsenic forfarmed juvenile milkfish Chanos chanos and human consumption risk in BFD-endemic area of Taiwan. Environ Int 32:552–560

    Article  CAS  Google Scholar 

  • Consea A, Gotz S, Garcia-Gomez J, Terol J, Talon M, Robles M (2005) BLAST2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  Google Scholar 

  • Datta S, Ghosh D, Saha DR, Bhattacharaya S, Mazumder S (2009) Chronic exposure to low concentration of arsenic is immunotoxic to fish: role of head kidney macrophages as biomarkers of arsenic toxicity to Clarias batrachus. Aquat Toxicol 92:86–94

    Article  CAS  Google Scholar 

  • Duker AA, Carranza EJ, Hale M (2005) Arsenic geochemistry and health. Environ Int 31:631–641

    Article  CAS  Google Scholar 

  • Dutton J, Fisher NS (2011) Bioaccumulation of As, Cd, Cr, Hg (II), and MeHg in killifish (Fundulus heteroclitus) from amphipod and worm prey. Sci Total Environ 409:3438–3447

    Article  CAS  Google Scholar 

  • Dwivedi N, Mehta A, Yadav A, Binukumar BK, Gill KD, Flora SJS (2011) MiADMSA reverses impaired mitochondrial energy metabolism and neuronal apoptotic cell death after arsenic exposure in rats. Toxicol Appl Pharmacol 256:241–248

    Article  CAS  Google Scholar 

  • Gao XM, Zhou Y, Zhang DD, Hou CC, Zhu JQ (2019) Multiple vitellogenin genes (vtgs) in large yellow croaker (Larimichthys crocea): molecular characterization and expression pattern analysis during ovarian development. Fish Physiol Biochem 45(3):829–848. https://doi.org/10.1007/s10695-018-0569-y

    Article  CAS  Google Scholar 

  • Gebel T (2000) Confounding variables in the environmental toxicology of arsenic. Toxicology 144:155–162

    Article  CAS  Google Scholar 

  • Ghosh S, Dungdung SR, Chowdhury ST, Mandal AK, Sarkar S, Ghosh D et al. (2011) Encapsulation of the flavonoid quercetin with an arsenic chelator into nanocapsules enables the simultaneous delivery of hydrophobic and hydrophilic drugs with a synergistic effect against chronic arsenic accumulation and oxidative stress. Free Radic Biol Med 51:1893–1902

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I et al. (2011) Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • He J, Charlet L (2013) A review of arsenic presence in China drinking water. J Hydrol 492:79–88

    Article  CAS  Google Scholar 

  • Hong X, Chen R, Hou R, Yuan L, Zha J (2018) Triphenyl phosphate (TPHP)-induced neurotoxicity in adult male chinese rare minnows (Gobiocypris rarus). Environ Sci Technol 52(20):11895–11903

    CAS  Google Scholar 

  • Hua D, Wang J, Yu D, Liu J (2017) Lanthanum exerts acute toxicity and histopathological changes in gill and liver tissue of rare minnow (Gobiocypris rarus). Ecotoxicology 26(9):1207–1215

    Article  CAS  Google Scholar 

  • Jain C, Ali I (2000) Arsenic: occurrence, toxicity and spesiation techniques. Water Res 34:4304–4312

    Article  CAS  Google Scholar 

  • Kaczor M, Sura P, Bronowicka-Adamska P, Wrobel M (2013) Exposure to lead in water and cysteine non-oxidative metabolism in Pelophylax ridibundus tissues. Aquat Toxicol 127:72–77. https://doi.org/10.1016/j.aquatox.2012.03.014

    Article  CAS  Google Scholar 

  • Kadeyala PK, Sannadi S, Gottipolu RR (2013) Alterations in apoptotic caspases and antioxidant enzymes in arsenic exposed rat brain regions: reversal effect of essential metals and a chelating agent. Environ Toxicol Pharmacol 36:1150–1166

    Article  CAS  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M et al. (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484. https://doi.org/10.1093/nar/gkm882

    Article  CAS  Google Scholar 

  • Kannan K, Jain SK (2000) Oxidative stress and apoptosis. Pathophysiology 7:153–163

    Article  CAS  Google Scholar 

  • Kaoud HA, Zaki MM, El-Dahshan AR, Saeid S, EL Zorba HY (2011) Amelioration the toxic effects of cadmium-exposure in nile tilapia (Oreochromis niloticus) by using Lemnagibba L. Life Sci J 8:185–195

    Google Scholar 

  • Kim JS, Kim H, Yim B, Rhee JS, Won EJ, Lee YM (2018) Identification and molecular characterization of two Cu/Zn-SODs and Mn-SOD in the marine ciliate Euplotes crassus: modulation of enzyme activity and transcripts in response to copper and cadmium. Aquat Toxicol 199:296–304

    Article  CAS  Google Scholar 

  • Kowaltowskia AJ, Castilhob RF, Vercesi AE (2001) Mitochondrial permeability transition and oxidative stress. FEBS Lett 495(1–2):12–15

    Article  Google Scholar 

  • Kozul-Horvath CD, Zandbergen F, Jackson BP, Enelow RI, Hamilton JW (2012) Effects of low-dose drinking water arsenic on mouse fetal and postnatal growth and development. PLoS ONE 7:1–9

    Article  CAS  Google Scholar 

  • Kunito T, Kubota R, Fujihara J, Agusa T, Tanabe S (2008) Arsenic in marine mammals, seabirds, and sea turtles. Rev Environ Contam Toxicol 195:31–69

    CAS  Google Scholar 

  • Lam SH, Winata CL, Tong Y, Korzh S, Lim WS, Korzh V (2006) Transcriptome kinetics of arsenic-induced adaptive response in zebrafish liver. Physiol Genom 27:351–361

    Article  CAS  Google Scholar 

  • Lin W, Hou J, Guo H, Li L, Wang L, Zhang D et al. (2018) The synergistic effects of waterborne microcystin-LR and nitrite on hepatic pathological damage, lipid peroxidation and antioxidant responses of male zebrafish. Environ Pollut 235:197–206

    Article  CAS  Google Scholar 

  • Lu T, Liu J, LeCluyse E, Zhou Y, Cheng M, Waalkes M (2001) Application of cDNA microarray to the study of arsenic-induced liver diseases in the population of Guizhou, China. Toxicol Sci 59:185–192

    Article  CAS  Google Scholar 

  • Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42(4):630–648. https://doi.org/10.1139/f85-083

    Article  Google Scholar 

  • Mcclintock TR, Chen Y, Bundschuh J, Oliver JT, Navoni J, Olmos V et al. (2012) Science of the total environment arsenic exposure in Latin America: biomarkers, risk assessments and related health effects. Sci Total Environ 429:76–91. https://doi.org/10.1016/j.scitotenv.2011.08.051

    Article  CAS  Google Scholar 

  • McKim JM, Erickson RJ (1991) Environmental impacts on the physiological mechanisms controlling xenobiotic transfer across fish gills. Physiol Zool 64(1):39–67. https://doi.org/10.2307/30158513

    Article  Google Scholar 

  • Mrak T, Slejkovec Z, Jeran Z, Jaćimović R, Kastelec D (2008) Uptake and biotransformation of arsenate in the lichen Hypogymnia physodes (L.) Nyl. Environ Pollut 151:300–307

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lister A, Van der Kraak G, Lee LE, Van MT et al. (2006) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water. Ecotoxicol Environ Saf 63(3):365–377. https://doi.org/10.1016/j.ecoenv.2005.04.014

    Article  CAS  Google Scholar 

  • Nicolli HB, Bundschuh J, Blanco C, Tujchneider OC, Panarello HO, Dapeña C et al. (2012) Science of the total environment arsenic and associated trace-elements in groundwater from the Chaco-Pampean plain, Argentina: results from 100 years of research. Sci Total Environ 429:36–56. https://doi.org/10.1016/j.scitotenv.2012.04.048

    Article  CAS  Google Scholar 

  • Nordstrom DK (2002) Worldwide occurrences of arsenic in ground water. Science 296:2143–2145

    Article  CAS  Google Scholar 

  • OECD (1995) Guidance document for the development of OECD guidelines for testing of chemicals. Organisation for Economic Co-operation and Development. https://www.oecd-ilibrary.org/docserver/9789264077928-en.pdf?expires=1569775678&id=id&accname=guest&checksum=AD1AEC921E4FC88E0A53AA98BF18B21C (Accessed 10 May 2002)

  • Pan YX, Luo Z, Zhuo MQ, Wei CC, Chen GH, Song YF (2018) Oxidative stress and mitochondrial dysfunction mediated Cd-induced hepatic lipid accumulation in zebrafish Danio rerio. Aquat Toxicol 199:12–20

    Article  CAS  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S et al. (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  CAS  Google Scholar 

  • Poleksic V, Lenhardt M, Jaric I, Djordjevic D, Gacic Z, Cvijanovic G et al. (2010) Liver, gills, and skin histopathology and heavy metal content of the Danube sterlet (Acipenser ruthenus Linnaeus, 1758). Environ Toxicol Chem 29(3):515–521. https://doi.org/10.1002/etc.82

    Article  CAS  Google Scholar 

  • Quinlivan VH, Farber SA (2017) Lipid uptake, metabolism, and transport in the larval zebrafish. Front Endocrinol 8:319

    Article  Google Scholar 

  • Rauen U, Petrat F, Sustmann R, Groot H (2004) Iron-induced mitochondrial permeabiltiy transition in cultured hepatocytes. J Hepatol 40(4):607–615. https://doi.org/10.1016/j.jhep.2003.12.021

    Article  CAS  Google Scholar 

  • Shahid N, Zia Z, Shahid M, Bakhat H, Anwar S, Shah GM et al. (2015) Assessing drinking water quality in Punjab, Pakistan. Pol J Environ Stud 24:2597–2606

    Article  CAS  Google Scholar 

  • Sharma VK, Sohn M (2009) Aquatic arsenic: toxicity, speciation, transformations, and remediation. Environ Int 35:743–759

    Article  CAS  Google Scholar 

  • Shiomi K, Suglyama Y, Shimakura K, Nagashima Y (1996) Retention and biotransformation of arsenic compounds administered intraperitoneally to carp. Fish Sci 62:261–266

    Article  CAS  Google Scholar 

  • Speare DJ, Ferguson HW (2006) Gills and pseudobranchs, systemic pathology of fish: a text and atlas of normal tissues in teleosts and their responses in disease, 2nd edn. Scotian Press, London, p 24–63. http://www.scotianpress.com

  • Srivastava P, Yadav RS, Chandravanshi LP, Shukla RK, Dhuriya YK, Chauhan LKS et al. (2014) Unraveling the mechanism of neuroprotection of curcumin in arsenic induced cholinergic dysfunctions in rats. Toxicol Appl Pharmacol 279:428–440

    Article  CAS  Google Scholar 

  • Subramanian V (2004) Water quality in South Asia. Asian J Water Environ Pollut 1(1–2):41–54

    CAS  Google Scholar 

  • Sun S, Ge X, Xuan F, Zhu J, Yu N (2014) Nitrite-induced hepatotoxicity in bluntsnout bream (Megalobrama amblycephala): the mechanistic insight from transcriptome to physiology analysis Toxicol Appl Pharmacol 37:55–65

    Google Scholar 

  • Tchounwou P, Patlolla A, Centeno J (2003) Carcinogenic and systemic health effects associated with arsenic exposure-a critical review. Toxicol Pathol 31:575–588

    CAS  Google Scholar 

  • Tisler T, Zagorc-Koncan J (2002) Acute and chronic toxicity of arsenic to some aquatic organisms. Bull Environ Contam Toxicol 69:421–429

    Article  CAS  Google Scholar 

  • USEPA (2007) Arsenic frequently asked questions by the agency for toxic substances and disease registry (ATSDR). CAS# 7440-38-2. United States Environmental Protection Agency (USEPA). https://www.epa.gov/sites/production/files/2015-04/documents/walter_atsdr_arsenic_faq.pdf. Accessed Aug 2007

  • Velmurugan B, Selvanayagam M, Cengiz EI, Unlu E (2009) Histopathological changes in the gill and liver tissues of freshwater fish, Cirrhinus mrigala exposed to dichlorvos. Braz Arch Biol Technol 52(5):1291–1296. https://doi.org/10.1590/S1516-89132009000500029

    Article  Google Scholar 

  • Waalkes MP, Ward JM, Liu J, Diwan BA (2003) Transplacental carcinogenicity of inorganic arsenic in the drinking water: induction of hepatic, ovarian, pulmonary, and adrenal tumors in mice. Toxicol Appl Pharmacol 186:7–17

    Article  CAS  Google Scholar 

  • Wang H, Liang Y, Li S, Chang J (2013a) Acute toxicity, respiratory reaction, and sensitivity of three cyprinid fish species caused by exposure to four heavy metals. PLoS ONE 8(6):e65282

    Article  CAS  Google Scholar 

  • Wang C, Zhang F, Cao W, Wang J (2013b) The identification of apolipoprotein CI in rare minnow (Gobiocypris rarus) and its expression following cadmium exposure. Environ Toxicol Pharmacol 35:419–426

    Article  CAS  Google Scholar 

  • Wang C, Zhang F, Cao W, Wang J (2014) The identification of metallothionein in rareminnow (Gobiocypris rarus) and its expressionfollowing heavy metal exposure. Environ Toxicol Pharmacol 37:1283–1291

    Article  CAS  Google Scholar 

  • Wang J, Cao W (2017) Gobiocypris rarus as a Chinese native model organism: history and current situation. Asian J Ecotoxicol 12:20–33

    Google Scholar 

  • Wasserman GA, Liu X, Parvez F, Ahsan H, Factor-Litvak P, van Geen A et al. (2004) Water arsenic exposure and children’s intellectual function in Araihazar, Bangladesh. Environ Health Perspect 112:1329–1333

    Article  CAS  Google Scholar 

  • WHO (2017) Guidelines for drinking-water quality. Fourth edition incorporating the first addendum. World Health Organization (WHO), Geneva, Switzerland

  • Xiong X, Luo S, Wu B, Wang J (2017) Comparative developmental toxicity and stress protein responses of dimethyl sulfoxide to rare minnow and zebrafish embryos/larvae. Zebrafish 14:60–68

    Article  CAS  Google Scholar 

  • Yan S, Wang M, Zha J, Zhu L, Li W, Luo Q et al. (2018) Environmentally relevant concentrations of carbamazepine caused endocrine-disrupting effects on nontarget organisms, Chinese Rare Minnows (Gobiocypris rarus). Environ Sci Technol 52(2):886–894

    Article  CAS  Google Scholar 

  • Zhou H, Guo LL, Lu L, Ge HH, Gao YG (2017) Needs and application of native model organisms for Chinese chemical management. Asian J Ecotoxicol 12:11–19

    Google Scholar 

Download references

Acknowledgements

We thank Dr Yuan Xiao (Institute of Hydrobiology, Chinese Academy of Sciences) for assistance with transmission electron microscopy analysis.

Funding

This study was funded by the Key Lab of Freshwater Biodiversity Conservation Ministry of Agriculture and Rural Affairs, Yangtze River Fisheries Research Institute, CAFS (Program SN: LFBC0903).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hong Cao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The present research did not involve human participants. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, L., Hu, X., Wang, N. et al. Histopathological examination and transcriptome analyses to assess the acute toxic effects of arsenite exposure on rare minnows (Gobiocypris rarus). Ecotoxicology 29, 613–624 (2020). https://doi.org/10.1007/s10646-020-02222-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-020-02222-3

Keywords

Navigation