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Pollution impact on metal and biomarker responses in intestinal cytosol of freshwater fish

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Abstract

In the present study, essential and nonessential metal content and biomarker responses were investigated in the intestine of fish collected from the areas polluted by mining. Our objective was to determine metal and biomarker levels in tissue responsible for dietary intake, which is rarely studied in water pollution research. The study was conducted in the Bregalnica River, reference location, and in the Zletovska and Kriva Rivers (the Republic of North Macedonia), which are directly influenced by the active mines Zletovo and Toranica, respectively. Biological responses were analyzed in Vardar chub (Squalius vardarensis; Karaman, 1928), using for the first time intestinal cytosol as a potentially toxic cell fraction, since metal sensitivity is mostly associated with cytosol. Cytosolic metal levels were higher in fish under the influence of mining (Tl, Li, Cs, Mo, Sr, Cd, Rb, and Cu in the Zletovska River and Cr, Pb, and Se in the Kriva River compared to the Bregalnica River in both seasons). The same trend was evident for total proteins, biomarkers of general stress, and metallothioneins, biomarkers of metal exposure, indicating cellular disturbances in the intestine, the primary site of dietary metal uptake. The association of cytosolic Cu and Cd at all locations pointed to similar pathways and homeostasis of these metallothionein-binding metals. Comparison with other indicator tissues showed that metal concentrations were higher in the intestine of fish from mining-affected areas than in the liver and gills. In general, these results indicated the importance of dietary metal pathways, and cytosolic metal fraction in assessing pollution impacts in freshwater ecosystems.

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The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

The authors are grateful to Dr. Nevenka Mikac for the opportunity to perform metal measurements on HR ICP-MS.

Funding

This research was funded by the Ministry of Science, Education and Sport of the Republic of Croatia (projects No. 098–0982934-2721 and 098–1782739-2749). The sampling was carried out as a part of two Croatian-Macedonian bilateral projects: “The assessment of availability and effects of metals on fish in the rivers under the impact of mining activities” and “Bacterial and parasitical communities of chub as indicators of the status of environment exposed to mining activities.”

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Authors and Affiliations

  1. Division for Marine and Environmental Research, Ruđer Bošković Institute, Bijenička Cesta 54, 10000, Zagreb, Croatia

    Vlatka Filipović Marijić, Nesrete Krasnići, Damir Valić, Damir Kapetanović, Irena Vardić Smrzlić & Zrinka Dragun

  2. Institute of Science and Technology Austria, Am Campus 1, 3400, Klosterneuburg, Austria

    Nesrete Krasnići

  3. Department for Cytology, Histology, and Embryology, Faculty of Natural Sciences and Mathematics, Ss Cyril and Methodius University, Arhimedova 3, Skopje, 1000, Republic of North Macedonia

    Maja Jordanova & Katerina Rebok

  4. Department for Ecology, Hydrometeorological Service, 18 Skupi, Skopje, 1000, Republic of North Macedonia

    Sheriban Ramani

  5. Institute of Animal Science, Bul. Ilinden, 92A, Skopje, 1000, Republic of North Macedonia

    Vasil Kostov & Rodne Nastova

Authors
  1. Vlatka Filipović Marijić
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  2. Nesrete Krasnići
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Contributions

Vlatka Filipović Marijić: conceptualization, validation, formal analysis, investigation, writing—original draft, writing—review and editing, and visualization. Nesrete Krasnići: formal analysis and investigation. Damir Valić: formal analysis and investigation. Damir Kapetanović: formal analysis and investigation. Irena Vardić Smrzlić: investigation. Maja Jordanova: formal analysis and investigation. Katerina Rebok: formal analysis and investigation. Sheriban Ramani: formal analysis and investigation. Vasil Kostov: formal analysis and investigation. Rodne Nastova: investigation. Zrinka Dragun: conceptualization, formal analysis, investigation, writing—review and editing, and project administration. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Vlatka Filipović Marijić.

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Fish were sampled by electrofishing according to the standard CEN EN 14011:2003 and anesthetized and sacrificed according to the Ordinance on the protection of animals used for scientific purposes. Laboratory for Biological Effects of Metals is a laboratory for fish sacrifice and work with fish bodies, organs and tissues, authorized by the Ministry of Agriculture, Veterinary and Food Safety Department (license number: HR-POK-025).

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Filipović Marijić, V., Krasnići, N., Valić, D. et al. Pollution impact on metal and biomarker responses in intestinal cytosol of freshwater fish. Environ Sci Pollut Res 30, 63510–63521 (2023). https://doi.org/10.1007/s11356-023-26844-2

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