Skip to main content

Advertisement

Log in

Effect on intestinal microbiota, bioaccumulation, and oxidative stress of Carassius auratus gibelio under waterborne cadmium exposure

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

Cadmium (Cd) is a hazardous pollutant known to exert various toxic effects and other sublethal effects on aquatic organisms, and induce a variety of adverse effects on human health, and can be commonly found in environment. The aim of this study was to explore the effects of waterborne Cd exposure on the intestinal microbiota, and Cd accumulation and oxidative response in Carassius auratus gibelio (C. gibelio). The fish were exposed to waterborne Cd at 0, 1, 2, and 4 mg/L for 30 days. Waterborne Cd exposure resulted marked alterations in the composition of microbiota. At the genus level, Bacteroides, Aeromonas, Akkermansia, Acinetobacter, Chryseobacterium, Shinella, Cetobacterium and Bacillus were significantly changed in Cd groups. The results obtained indicate that Cd exposure significantly increased the bioaccumulation level of Cd and profoundly affected antioxidant enzyme including superoxide dismutase (SOD), catalase (CAT), glutathione (GSH), total antioxidant (T-AOC), malonaldehyde (MDA), and glutathione-S-transferase (GST). The present findings may provide a new framework for the role of gut microbiota in the response to environmental chemical contamination and in the pathogenesis of body disorders.

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

Similar content being viewed by others

Data availability

Our experimental data are really available.

References

  • Adeyeye EI, Akinyugha NJ, Fesobi ME, Tenabe VO (1996) Determination of some metals in Clarias gariepinus (Cuvier and Vallenciennes), Cyprinus carpio (L.) and Oreochromis niloticus (L.) fishes in a polyculture fresh water pond and their environments. Aquaculture. 147:205–214

    Article  CAS  Google Scholar 

  • Asagba SO, Eriyamremu GE, Igberaese ME (2008) Bioaccumulation of cadmium and its biochemical effect on selected tissues of the catfish (Clarias gariepinus). Fish Physiol Biochem 34:61–69

    Article  CAS  Google Scholar 

  • Bengtsson BE (1974) The effects of zinc on the mortality and reproduction of the minnow, Phoxinus phoxinus L. Arch Environ Contamin & Toxicol 2, 342–355

  • Bogdan C, Röllinghoff M, Diefenbach A (2000) Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol 12:64–76

    Article  CAS  Google Scholar 

  • Cao L, Huang W, Liu J, Yin X, Dou S (2010) Accumulation and oxidative stress biomarkers in Japanese flounder larvae and juveniles under chronic cadmium exposure. Comp Biochem Physiol Part C Toxico Pharmacol 151:386–392

    Article  Google Scholar 

  • Chang X, Li H, Feng J, Chen Y, Nie G, Zhang J (2019) Effects of cadmium exposure on the composition and diversity of the intestinal microbial community of common carp (Cyprinus carpio L.). Ecotoxicol Environ Saf 171:92–98

    Article  CAS  Google Scholar 

  • Dai J et al (2018) Effect of lead on antioxidant ability and immune responses of crucian carp. Biol Trace Elem Res:1–8

  • Danyang et al (2018) The effect of cadmium exposure on diversity of intestinal microbial community of Rana chensinensis tadpoles. Ecotoxicol Environ Saf

  • Das S, et al. (2019) Effects of cadmium exposure on antioxidant enzymes and histological changes in the mud shrimp Austinogebia edulis (Crustacea: Decapoda). Environ Sci Pollut Res

  • Díaz-Jaramillo M et al (2017) Sublethal effects in Perinereis gualpensis (Polychaeta: Nereididae) exposed to mercury-pyrene sediment mixture observed in a multipolluted estuary. Ecotoxicology. 26:1–10

    Article  Google Scholar 

  • Drummond RA, et al. (2011) Some short-term indicators of sublethal effects of copper on brook trout, Salvelinus fontinalis Journal of the Fisheries Research Board of Canada 30, 698–701

  • Duan Y et al (2016) Effect of dietary poly-β-hydroxybutyrate (PHB) on growth performance, intestinal health status and body composition of Pacific white shrimp Litopenaeus vannamei (Boone, 1931). Fish Shellfish Immunol:520–528

  • Elgazzar A, et al. (2014) Physiological and oxidative stress biomarkers in the freshwater Nile Tilapia, Oreochromis niloticus L., exposed to sublethal doses of cadmium. Alexandria Journal of Veterinary Ences. 40, 29

  • Gómez GD, Balcázar JL (2010) A review on the interactions between gut microbiota and innate immunity of fish. FEMS Immunol Med Microbiol 52:145–154

    Article  Google Scholar 

  • Guardiola FA, Cuesta A, Meseguer J, Martínez S, Martínez-Sánchez MJ, Pérez-Sirvent C, Esteban MA (2013) Accumulation, histopathology and immunotoxicological effects of waterborne cadmium on gilthead seabream (Sparus aurata). Fish Shellfish Immun 35:792–800

    Article  CAS  Google Scholar 

  • Hamilton SJC, Mehrle PM (1986) Metallothionein in fish: review of its importance in assessing stress from metal contaminants

    Google Scholar 

  • Han XY, Xu ZR, Wang YZ, Huang QC (2006) Effect of cadmium on lipid peroxidation and activities of antioxidant enzymes in growing pigs. Biol Trace Elem Res 110:251–263

    Article  CAS  Google Scholar 

  • Hansen JA, Welsh PG, Lipton J, Suedkamp MJ (2002) The effects of long-term cadmium exposure on the growth and survival of juvenile bull trout (Salvelinus confluentus). Aquat Toxicol 58:165–174

    Article  CAS  Google Scholar 

  • Hilmy AM, Shabana MB, Daabees AY (1985) Bioaccumulation of cadmium: toxicity in Mugil cephalus. Comp Biochem Phys Part C Comp Pharmacol 81:139–144

    Article  CAS  Google Scholar 

  • J.A et al (2002) The effects of long-term cadmium exposure on the growth and survival of juvenile bull trout (Salvelinus confluentus). Aquat Toxicol

  • Javed M (2015) Chronic dual exposure (waterborne+dietary) effects of cadmium, zinc and copper on growth and their bioaccumulation in Cirrhina mrigala. Pak Vet J 35:143–146

    CAS  Google Scholar 

  • Kim JH, Kang JC (2014) The selenium accumulation and its effect on growth, and haematological parameters in red sea bream, Pagrus major , exposed to waterborne selenium. Ecotoxicol Environ Saf 104:96–102

    Article  CAS  Google Scholar 

  • Kraemer LD, Campbell PGC, Hare L (2005) Dynamics of Cd, Cu and Zn accumulation in organs and sub-cellular fractions in field transplanted juvenile yellow perch (Perca flavescens). Environ Pollut 138:324–337

    Article  CAS  Google Scholar 

  • Li T, Long M, Gatesoupe FJ, Zhang Q, Li A, Gong X (2015) Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb Ecol 69:25–36

    Article  CAS  Google Scholar 

  • Liu SM et al (2014) Removal of Cu, Ni, Zn, Cd and Pb in artificial acid mine drainage by modified oxygen releasing compounds. Appl Mech Mater 535:758–763

    Article  Google Scholar 

  • Liu K, Chi S, Liu H, Dong X, Yang Q, Zhang S, Tan B (2015) Toxic effects of two sources of dietborne cadmium on the juvenile cobia, Rachycentron canadum L and tissue-specific accumulation of related minerals. Aquat Toxicol 165:120–128

    Article  CAS  Google Scholar 

  • Marchesi JR, Adams DH, Fava F, Hermes GDA, Hirschfield GM, Hold G, Quraishi MN, Kinross J, Smidt H, Tuohy KM, Thomas LV, Zoetendal EG, Hart A (2016) The gut microbiota and host health: a new clinical frontier. Gut. 65:330–339

    Article  Google Scholar 

  • Mu WN, Li ZH, Zhong LQ, Wu YH (2016) Effect of tributyltin, cadmium, and their combination on physiological responses in juvenile grass carp. J Aquat Anim Health 28:181–186

    Article  CAS  Google Scholar 

  • Namba A, Mano N, Hirose H (2007) Phylogenetic analysis of intestinal bacteria and their adhesive capability in relation to the intestinal mucus of carp. J Appl Microbiol 102:1307–1317

    Article  CAS  Google Scholar 

  • Navarrete P, Fuentes P, de la Fuente L, Barros L, Magne F, Opazo R, Ibacache C, Espejo R, Romero J (2013) Short term effects of dietary soybean meal and lactic acid bacteria on the intestinal morphology and microbiota of Atlantic salmon (Salmo salar). Aquac Nutr 19:827–836

    Article  CAS  Google Scholar 

  • Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41:1553–1573

    Article  Google Scholar 

  • Papadimitriou E, Loumbourdis NS (2002) Exposure of the frog Rana ridibunda to copper: impact on two biomarkers, lipid peroxidation, and glutathione. Bull Environ Contam Toxicol 69:885–891

    Article  CAS  Google Scholar 

  • Papineni RVL, Umar S (2013) Spot light on intestinal microbiota. Transl Cancer Res 2:359–369

    CAS  Google Scholar 

  • Pavlov DF, Chuiko GM, Pavlov DD (2014) Growth of Mozambique tilapia (Oreochromis mossambicus Peters) chronically exposed to cadmium, naphthalene, and DDVP. Inland Water Biol 7:97–100

    Article  Google Scholar 

  • Pei Z et al (2015) Comparative study on the effect of dietary lipid level on growth and feed utilization for gibel carp (Carassius auratus gibelio) and Chinese longsnout catfish (Leiocassis longirostris Gunther). Aquac Nutr 10:209–216

    Article  Google Scholar 

  • Pérez T, Balcázar JL, Ruiz-Zarzuela I, Halaihel N, Vendrell D, de Blas I, Múzquiz JL (2010) Host-microbiota interactions within the fish intestinal ecosystem. Mucosal Immunol 3:355–360

    Article  Google Scholar 

  • Ring E et al (2003) Electron microscopy of the intestinal microflora of fish. Aquaculture. 227:395–415

    Article  Google Scholar 

  • Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM, Guillemin K, Rawls JF (2011) Evidence for a core gut microbiota in the zebrafish. ISME J 5:1595–1608

    Article  CAS  Google Scholar 

  • Sarnat HB, Netsky MG (2002) When does a ganglion become a brain? Evolutionary origin of the central nervous system

  • Tan XY, et al. (2010) Effect of dietary cadmium level on the growth, body composition and several hepatic enzymatic activities of juvenile yellow catfish, Pelteobagrus fulvidraco Aquaculture Research 41, 1022–1029

  • Timbrell J (1991) Principles of biochemical toxicology. Principles of Biochemical Toxicology 520

  • Tongtong et al (2015) Comparative analysis of the intestinal bacterial communities in different species of carp by pyrosequencing. Microb Ecol

  • Wang H, Ji Y, Yin C, Deng M, Tang T, Deng B, Ren W, Deng J, Yin Y, Tan C (2018) Differential analysis of gut microbiota correlated with oxidative stress in sows with high or low litter performance during lactation. Front Microbiol 9:1665

  • Wang N et al (2019) Amelioration of Cd-induced bioaccumulation, oxidative stress and intestinal microbiota by Bacillus cereus in Carassius auratus gibelio. Chemosphere. 245:125613

    Article  Google Scholar 

  • Wang X, et al. (2020) Aberrant gut microbiota alters host metabolome and impacts renal failure in humans and rodents. Gut. gutjnl-2019-319766

  • Wimmer U, Wang Y, Georgiev O, Schaffner W (2005) Two major branches of anti-cadmium defense in the mouse: MTF-1/metallothioneins and glutathione. Nucleic Acids Res 33:5715–5727

    Article  CAS  Google Scholar 

  • Wu H, Xuan R, Li Y, Zhang X, Jing W, Wang L (2014) Biochemical, histological and ultrastructural alterations of the alimentary system in the freshwater crab Sinopotamon henanense subchronically exposed to cadmium. Ecotoxicology. 23:65–75

    Article  CAS  Google Scholar 

  • Xia L, Xiong D, Gu Z, Xu Z, Chen C, Xie J, Xu P (2008) Recovery of Acinetobacter baumannii from diseased channel catfish (Ictalurus punctatus) in China. Aquaculture. 284:285–288

    Article  Google Scholar 

  • Yin Y, Zhang P, Yue X, du X, Li W, Yin Y, Yi C, Li Y (2018) Effect of sub-chronic exposure to lead (Pb) and Bacillus subtilis on Carassius auratus gibelio: bioaccumulation, antioxidant responses and immune responses. Ecotoxicol Environ Saf 161:755–762

    Article  CAS  Google Scholar 

  • Yu-Sheng et al (2017) Bioaccumulation of lead and non-specific immune responses in white shrimp (Litopenaeus vannamei) to Pb exposure. Fish Shellfish Immun

  • Zhai Q et al (2016) Effect of dietary probiotic supplementation on intestinal microbiota and physiological conditions of Nile tilapia (Oreochromis niloticus) under waterborne cadmium exposure. Antonie Van Leeuwenhoek 110:1–13

    Google Scholar 

  • Zhai Q, Li T, Yu L, Xiao Y, Feng S, Wu J, Zhao J, Zhang H, Chen W (2017) Effects of subchronic oral toxic metal exposure on the intestinal microbiota of mice. Sci Bull 62:831–840

    Article  CAS  Google Scholar 

  • Zhang T, Zhang Y, Li DL, Xiao TY, Li J (2013) Exposure of silver carp (Hypophthalmichthys molitrix) to environmentally relevant levels of cadmium:hematology,muscle physiology,and implications for stock enhancement in the Xiangjiang River (Hunan,China). Science China 56:66–72

    Article  CAS  Google Scholar 

  • Zhang CN, Zhang JL, Ren HT, Zhou BH, Wu QJ, Sun P (2017) Effect of tributyltin on antioxidant ability and immune responses of zebrafish ( Danio rerio ). Ecotoxicol Environ Saf 138:1–8

    Article  Google Scholar 

Download references

Funding

The work was supported by the National Natural Sciences Foundational of China (no. 30972191) and the 948 Program from Ministry of Agriculture of China (no. 2014Z34).

Author information

Authors and Affiliations

Authors

Contributions

All authors participated in experiments, data processing, and paper writing. All authors agree to contribute to the journal without conflict of interest.

Corresponding author

Correspondence to Yuehong Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the Ethics Committee of Jilin Agricultural University with ID no. 20121008. All authors read this guide carefully. All subjects signed their informed consents before participation.

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

Wang, N., Guo, Z., Zhang, Y. et al. Effect on intestinal microbiota, bioaccumulation, and oxidative stress of Carassius auratus gibelio under waterborne cadmium exposure. Fish Physiol Biochem 46, 2299–2309 (2020). https://doi.org/10.1007/s10695-020-00870-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-020-00870-0

Keywords

Navigation