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Hypoxia-induced oxidative DNA damage links with higher level biological effects including specific growth rate in common carp, Cyprinus carpio L.

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Abstract

Both hypoxia and hyperoxia, albeit in different magnitude, are known stressors in the aquatic environment. Adopting an integrated approach, mirror carp (Cyprinus carpio L.), were exposed chronically (i.e. 30 days) to hypoxic (1.8 ± 1.1 mg O2 l−1) and hyperoxic (12.3 ± 0.5 mg O2 l−1) conditions and resultant biological responses or biomarkers were compared between these two treatments as well as with fish held under normoxic conditions (7.1 ± 1.04 mg O2 l−1). The biomarkers determined included the activities of glutathione peroxidase (GPx), measurement of oxidative DNA damage (using modified Comet assay employing bacterial enzymes: Fpg and Endo-III), haematological parameters, histopathological and ultrastructural examination of liver and gills. Specific growth rate (SGR) of the fish, as an important ecotoxicological parameter was also determined over the exposure period. The study suggested that while the levels of hepatic GPx were unaffected, there was a significant difference in activity in the blood plasma under different exposure conditions; the hyperoxic group showed increased GPx activity by approximately 37% compared to normoxic group and the hypoxic group showed a decrease by approximately 38% than the normoxic group. Interestingly, oxidative DNA damage was significantly higher in both hypoxic and hyperoxic by approximately 25% compared to normoxic conditions, Fpg showing enhanced level of damage compared to the Endo-III treatment (P < 0.001). The haematological parameters showed enhanced values under hypoxic conditions. Transmission electron microscopic (TEM) studies revealed damage to liver and gill tissues for both the treatments. Interestingly, SGR of fish was significantly lowered in hypoxic by approx. 30% compared to normoxic condition and this was found to be correlated with DNA damage (R = −0.82; P = 0.02). Taken together, these results indicate that prolonged exposure to both hypoxic and hyperoxic conditions induce oxidative stress responses at both DNA and tissue levels, and hypoxia can result in compensatory changes in haematological and growth parameters which could influence Darwinian fitness of the biota with wider ecological implications.

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Acknowledgments

SAM is funded by the Ministry of Higher Education and Scientific Research, Republic of Iraq. ANJ would like to acknowledge the support received from European Regional Development Fund, INTERREG IVA (Grant No. 4059). We are thankful to Professor Andrew Collins, University of Oslo, Norway, for providing bacterial enzymes used for the modified Comet assay. Thanks are also due to Mr. Peter Russell and Mr. Benjamin Eynon for technical assistance and to Mr. Glenn Harper for help in electron microscopic studies.

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  1. School of Biomedical & Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK

    Sanaa A. Mustafa, Sherain N. Al-Subiai, Simon J. Davies & Awadhesh N. Jha

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  1. Sanaa A. Mustafa
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  2. Sherain N. Al-Subiai
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  4. Awadhesh N. Jha
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Correspondence to Awadhesh N. Jha.

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Mustafa, S.A., Al-Subiai, S.N., Davies, S.J. et al. Hypoxia-induced oxidative DNA damage links with higher level biological effects including specific growth rate in common carp, Cyprinus carpio L.. Ecotoxicology 20, 1455–1466 (2011). https://doi.org/10.1007/s10646-011-0702-5

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