Investigating the Impact of Disrupting the Glutamine Metabolism Pathway on Ammonia Excretion in Crucian Carp (Carassius auratus) under Carbonate Alkaline Stress Using Metabolomics Techniques

Yanchun Sun; Chuanye Geng; Wenzhi Liu; Ying Liu; Lu Ding; Peng Wang

doi:10.3390/antiox13020170

journal article Open Access Jan 29, 2024

Investigating the Impact of Disrupting the Glutamine Metabolism Pathway on Ammonia Excretion in Crucian Carp (Carassius auratus) under Carbonate Alkaline Stress Using Metabolomics Techniques

Yanchun Sun

Chuanye Geng Wenzhi Liu

Ying Liu

Lu Ding

Peng Wang

Antioxidants Vol. 13 No. 2 pp. 170 · MDPI AG

View at Publisher Save 10.3390/antiox13020170

Abstract

With the gradual decline in freshwater resources, the space available for freshwater aquaculture is diminishing and the need to maximize saline water for aquaculture is increasing. This study aimed to elucidate the impact mechanisms of the disruption of the glutamate pathway on serum metabolism and ammonia excretion in crucian carp (Carassius auratus) under carbonate alkaline stress. A freshwater control group (C group), a 20 mmol/L NaHCO3 stress group (L group), and a 40 mmol/L NaHCO3 stress group (H group) were established. After 30 days of exposure, methionine sulfoximine (MSO) was injected to block the glutamate pathway metabolism, and the groups post-blocking were labeled as MC, ML, and MH. Ultra-high-performance liquid chromatography coupled with the quadrupole time-of-flight mass spectrometry (UPLC-Q-TOF/MS) metabolomics technique was employed to detect changes in the composition and content of crucian carp serum metabolites. Significant differential metabolites were identified, and related metabolic pathways were analyzed. The results revealed that, following the glutamate pathway blockade, a total of 228 differential metabolites (DMs) were identified in the three treatment groups. An enrichment analysis indicated significant involvement in glycerophospholipid metabolism, arachidonic acid metabolism, sphingolipid metabolism, purine metabolism, arginine and proline biosynthesis, pantothenate and CoA biosynthesis, glutathione metabolism, and fatty acid degradation, among other metabolic pathways. The results showed that ROS imbalances and L-arginine accumulation in crucian carp after the glutamate pathway blockade led to an increase in oxidative stress and inflammatory responses in vivo, which may cause damage to the structure and function of cell membranes. Crucian carp improves the body’s antioxidant capacity and regulates cellular homeostasis by activating glutathione metabolism and increasing the concentration of phosphatidylcholine (PC) analogs. Additionally, challenges such as aggravated ammonia excretion obstruction and disrupted energy metabolism were observed in crucian carp, with the upregulation of purine metabolism alleviating ammonia toxicity and maintaining energy homeostasis through pantothenate and CoA biosynthesis as well as fatty acid degradation. This study elucidated the metabolic changes in crucian carp under carbonate alkaline stress after a glutamate pathway blockade at the cellular metabolism level and screened out the key metabolic pathways, which provide a scientific basis for further in-depth studies on the ammonia excretion of freshwater scleractinian fishes under saline and alkaline habitats at a later stage.

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Details

Published: Jan 29, 2024
Vol/Issue: 13(2)
Pages: 170
License: View

Authors

Y

Yanchun Sun

Department of Food Science and Engineering, College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China; Laboratory of Quality & Safety Risk Assessment for Aquatic Products, Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China

C

Chuanye Geng

Department of Food Science and Engineering, College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China; Laboratory of Quality & Safety Risk Assessment for Aquatic Products, Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China

W

Wenzhi Liu

Department of Food Science and Engineering, College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China; Laboratory of Quality & Safety Risk Assessment for Aquatic Products, Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China

Y

Ying Liu

Department of Food Science and Engineering, College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China; Laboratory of Quality & Safety Risk Assessment for Aquatic Products, Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China

L

Lu Ding

Department of Food Science and Engineering, College of Food Science and Technology, Shanghai Ocean University, Shanghai 201306, China; Laboratory of Quality & Safety Risk Assessment for Aquatic Products, Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China

P

Peng Wang

Laboratory of Quality & Safety Risk Assessment for Aquatic Products, Heilongjiang River Fisheries Research Institute of Chinese Academy of Fishery Sciences, Ministry of Agriculture and Rural Areas, Harbin 150070, China

Funding

China Postdoctoral Science Foundation Award: JQ2023C007

Natural Science Foundation of Heilongjiang Province for Distinguished Young Scholars Award: JQ2023C007

Central Public Interest Scientific Institution Basal Research Fund, HRFRI Award: JQ2023C007

National Agricultural Biological Breeding Major Project Award: JQ2023C007

Postdoctoral Science Foundation of Heilongjiang Province of China Award: JQ2023C007

Cite This Article

Yanchun Sun, Chuanye Geng, Wenzhi Liu, et al. (2024). Investigating the Impact of Disrupting the Glutamine Metabolism Pathway on Ammonia Excretion in Crucian Carp (Carassius auratus) under Carbonate Alkaline Stress Using Metabolomics Techniques. Antioxidants, 13(2), 170. https://doi.org/10.3390/antiox13020170

Investigating the Impact of Disrupting the Glutamine Metabolism Pathway on Ammonia Excretion in Crucian Carp (Carassius auratus) under Carbonate Alkaline Stress Using Metabolomics Techniques

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