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Heavy metal bioaccumulation triggers oxystress, genotoxicity and immunomodulation in head kidney macrophages of Channa punctatus Bloch

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Abstract

Studies on heavy metal induced toxicity have been conducted in many water bodies across the globe and such effects have been evaluated in various fish species. The present study was designed to determine the load of some heavy metals in select sites in Southern Assam, India, along with estimating their concentration in tissues of Channa punctatus Bloch. inhabiting those niches. The effect of heavy metals in oxystress generation, genotoxicity and subsequent immune response in fish was also evaluated. In all of these sites, the concentration of Hg, Cd, Pb and Cr were above the permissible ranges while their concentrations were several folds higher in the piscine tissues due to bioaccumulation and possible biomagnification. Kidney showed the highest metal pollution index followed by liver and gills. Generation of ROS was significantly elevated and that in turn triggered oxystress, as is evident from enhanced lipid peroxidation, protein carbonylation and respiratory burst activity. These were in association with the compromised antioxidant enzyme levels with concomitant damage to DNA as evident from Comet parameters. The innate immune potential was significantly impaired as evident from the compromised cell adhesion, phagocytosis, intracellular killing activity in head kidney macrophages (HKM) along with decreased release of nitric oxide (NO) and myeloperoxidase (MPO). Immunosuppression was further validated at protein levels where compromised release of cytokines viz. TNF-α, IL-1β, IL-6, IL-10 and IL-12 and cell signaling molecules iNOS and NF-κβ were noted. Thus the present study indicates genotoxicity along with a compromise in immune status of Channa punctatus Bloch. living in a habitat laden with heavy metals.

Highlights

  • Heavy metal concentrations in select water bodies above the WHO, EPA, IS limits.

  • Accumulation of heavy metals in fish tissues are above the FAO set range.

  • MPI is maximum in the kidney followed by liver and gill of Channa punctatus.

  • Metal induced oxidative stress, genotoxicity and compromised innate immune potential.

  • Heavy metal induced decreased cytokine release and immunocompromised state.

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Acknowledgements

The authors gratefully acknowledge the Sophisticated Analytical Instrument Facility (SAIF), NEHU, Shillong, Meghalaya. This research was conducted in compliance with all relevant federal guidelines and institutional policies.

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Authors and Affiliations

  1. Immunobiology and Nanobiotechnology Laboratory, Department of Biotechnology, Assam University, Silchar, Assam, 788011, India

    Chohelee Choudhury, Rajkamal Das & Mahuya Sengupta

  2. Laboratory of Molecular and Cell Biology, Department of Life Science and Bioinformatics, Assam University, Silchar, 788011, India

    Sarbani Giri & Dharmeswar Barhoi

  3. Department of Economics, Assam University, Silchar, Assam, 788011, India

    Ritwik Mazumder

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  1. Chohelee Choudhury
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  2. Sarbani Giri
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  6. Mahuya Sengupta
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Contributions

CC carried out the whole experimental work and drafted the manuscript. RD helped in experimental work. DB and SG guided in comet analysis. RM helped in statistical analysis while MS helped in supervising the work, designing the experiments and evaluating the manuscript.

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Correspondence to Mahuya Sengupta.

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Choudhury, C., Giri, S., Mazumder, R. et al. Heavy metal bioaccumulation triggers oxystress, genotoxicity and immunomodulation in head kidney macrophages of Channa punctatus Bloch. Ecotoxicology 32, 553–568 (2023). https://doi.org/10.1007/s10646-023-02659-2

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