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Alpha-ketoglutaric acid mitigates the detrimental effects of soy antigenic protein on the intestinal health and growth performance of Mirror carp Cyprinus carpio

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Abstract

The study investigated the alleviated effects of Alpha-ketoglutaric acid (AKG) on the intestinal health of mirror carp (Cyprinus carpio Songpu) caused by soy antigenic protein. The diets were formulated from fishmeal (CON), 50% soybean meal (SBM), the mixture of glycinin and β-conglycinin (11 + 7S) and adding 1% AKG in the 11 + 7S (AKG). Carp (~ 4 g) in triplicate (30 fish per tank) was fed to apparent satiation thrice a day for six weeks. Compared with CON, SBM treatment resulted in significantly poor growth performance (P < 0.05), whereas 11 + 7S and AKG treatments were not significantly different from CON (P > 0.05). Gene expression of tumor necrosis factor (TNF-α) and interleukin-1 β (IL-1β) in proximal intestines (PI) and distal intestines (DI) were increased (P < 0.05), and transforming growth factor (TGF-β) in PI and middle intestines (MI) was decreased (P < 0.05) in both SBM and 11 + 7S. The caspase-3 in DI increased in SBM (P < 0.05) and the caspase-3 and caspase-9 in DI increased in 11 + 7S (P < 0.05); conversely, TGF-β in PI and MI was increased, TNF-α and IL-1β in the MI, caspase-3, and caspase-9 in DI was decreased in AKG (P < 0.05). The TOR (target of rapamycin) in PI and MI, ACC in PI, MI and DI was decreased in SBM (P < 0.05), the AMPK in the PI and DI, TOR in PI, MI and DI, ACC in PI and DI, 4E-BP in DI was reduced in 11 + 7S (P < 0.05). AMPK in the PI and DI, ACC in the PI and MI, TOR in PI, MI, and DI, 4E-BP in PI and DI was recovered by AKG supplementation (P < 0.05). Lipids and lipid-like metabolism, organic acids and derivatives metabolism increased in AKG dietary treatment. In conclusion, AKG reduces the expression of intestinal inflammation and apoptosis pathway and changes glycerophospholipid metabolism and sphingolipid metabolism in the intestine of fish.

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Data availability

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

Code availability

Not applicable.

Abbreviations

AKG:

Alpha-ketoglutaric acid

TNF-α,:

Tumor necrosis factor

IL-1β:

Interleukin-1 β

TGF-β:

Transforming growth factor

WG:

Weight gain

FCR:

Feed conversion ratio

CF:

Condition factor

SR:

Survival rate

PER:

Protein efficiency ratio

SGR:

Specific growth rate

PI:

Proximal intestines

MI:

Middle intestines

DI:

Distal intestines

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Acknowledgements

The funding support provided by the Natural Science Foundation of China, NSFC (31972800) and Key Laboratory of Freshwater Aquatic Biotechnology and Genetic Breeding of Ministry of Agriculture Key Laboratory (HSY202209K1) is gratefully acknowledged. The authors are grateful to the Dr. Zhili Ding for providing necessary facilities and support to successfully carry out this study.

Funding

Funded by the Natural Science Foundation of China, NSFC (31972800), Key Laboratory of Freshwater Aquatic Biotechnology and Genetic Breeding of Ministry of Agriculture Key Laboratory (HSY202209K1).

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Authors

Contributions

Zuliang Zhou have participated in conceptualization, methodology, data statistics and writing—Original Draft conception; Jianhua Zhao participated in conceptualization, methodology; Clement R. de Cruz completed writing—review & editing; Hong Xu and Liansheng Wang analyzed; Qiyou Xu participated in conceptualization, writing—review & editing and supervision.

Corresponding author

Correspondence to Qiyou Xu.

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Ethical Approval

The study was conducted strictly following the Guidance of the Care and Use of Laboratory Animals in China. The experimental protocol was approved by the Committee on the Ethics of Animal Experiments of Huzhou University (20180306).

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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Zhou, Z., Zhao, J., de Cruz, C.R. et al. Alpha-ketoglutaric acid mitigates the detrimental effects of soy antigenic protein on the intestinal health and growth performance of Mirror carp Cyprinus carpio. Fish Physiol Biochem 49, 951–965 (2023). https://doi.org/10.1007/s10695-023-01234-0

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