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Hypoxia-mediated inhibition of cholesterol synthesis leads to disruption of nocturnal sex steroidogenesis in the gonad of koi carp, Cyprinus carpio

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Abstract

Reproductively mature koi carps (Cyprinus carpio) showed a prominent diurnal variation of sex steroids with sustained nocturnal rise. Exposure to chronic hypoxia (DO < 0.8 mg/l) disrupted nocturnal sex steroid production in koi carp gonads. Inhibition of sex steroidogenesis is linked to the down-regulation of HMG-Co A reductase (p < 0.05), which acts as a rate-limiting enzyme in the mevalonate pathway for cholesterol production. HMG-CoA reductase inhibition was obvious in the gonads and liver of both sexes during 18.00 h and 21.00 h resulting in hypocholesterolemia (p < 0.05). The levels of sex steroids, such as estradiol, testosterone, and 11-keto-testosterone in gonads were depleted below the optimum levels owing to disruption of de novo cholesterol synthesis along with attenuation of HDL-cholesterol level in serum. Inhibition of melatonin under hypoxic conditions indicates disruption of melatonin effects on the hypothalamus-pituitary-gonadal (HPG) axis of koi carp. Under severe hypoxic stress, koi carp promoted energy conservation by switching over to the triglyceride (TGA) pathway instead of the mevalonate pathway to suppress cholesterol production. Chronic hypoxia inhibited cholesterol synthesis, a prerequisite for gonadal maturation. It promoted TGA production, as an alternative energy source, suggesting a probable mitigation strategy adopted by hypoxia-tolerant fish to deal with low dissolved oxygen frequently occurring in aquatic bodies.

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Acknowledgments

The authors are grateful to Director, Central Institute of Fisheries Education, Mumbai and Indian Council of Agricultural Research for providing support and necessary facilities for carrying out this experiment as part of doctoral thesis.

Funding

The Director, Central Institute of Fisheries Education, Mumbai and Indian Council of Agricultural Research provided funds for carrying out this experiment as part of doctoral thesis.

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Authors and Affiliations

  1. ICAR- Central Institute of Brackishwater Aquaculture , Chennai, Tamil Nadu, 600028, India

    Aritra Bera

  2. ICAR-Central Institute of Fisheries Education , Versova, Mumbai, Maharashtra, 400061, India

    Narinder Kumar Chadha, Srijit Chakravarty & Paramita Banerjee Sawant

  3. ICAR-Central Institute of Fisheries Education, Kolkata Centre, Sector V, Salt Lake City, Kolkata, West Bengal, 700091, India

    Subrata Dasgupta

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  1. Aritra Bera
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  2. Narinder Kumar Chadha
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  4. Srijit Chakravarty
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  5. Paramita Banerjee Sawant
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Contributions

This study forms part of the doctoral research of the first author. Conceived and designed the experiments: AB SD NKC PBS. Performed the experiments: AB SD PBS SC. Analyzed the data: AB PBS SD. Contributed reagents/materials/analysis tools: NKC SD PBS. Wrote the paper: AB PBS. Edited the manuscript: SD.

Corresponding author

Correspondence to Paramita Banerjee Sawant.

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The authors declare that they have no conflict of interest.

Ethics statement

The research undertaken complies with the current animal welfare laws in India. Care and treatment of fishes used in this study were in accordance with the guidelines of the CPCSEA [(Committee for the Purpose of Control and Supervision of Experiments on Animals), Ministry of Environment & Forests (Animal Welfare Division), Govt. of India] on care and use of animals in scientific research. The study was undertaken with approval of statutory authorities of the ICAR-Central Institute of Fisheries Education, Mumbai, India (Deemed to be University under Sec. 3 of University Grants Commission Act, 1956 and ISO 9001:2015 certified). As the experimental fish, Cyprinus carpio is not an endangered fish; the provisions of the Govt. of India’s Wildlife Protection Act of 1972 are not applicable for experiments on this fish.

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Bera, A., Chadha, N.K., Dasgupta, S. et al. Hypoxia-mediated inhibition of cholesterol synthesis leads to disruption of nocturnal sex steroidogenesis in the gonad of koi carp, Cyprinus carpio. Fish Physiol Biochem 46, 2421–2435 (2020). https://doi.org/10.1007/s10695-020-00887-5

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