Mechanisms of ammonotelism, epithelium damage, cellular apoptosis, and proliferation in gill of Litopenaeus vannamei under NH4Cl exposure

• Published in: Environmental science and pollution research international 2024-02, Vol.31 (10), p.15153-15171
• Main Authors: Li, Yaobing, Zhang, Xin, Tong, Ruixue, Xu, Qiuhong, Zhang, Ning, Liao, Qilong, Pan, Luqing
• Format: Article
• Language: English
• Subjects: amino acid metabolism; Amino acids; Ammonia; Ammonium chloride; ammonium nitrogen; Apoptosis; Aquaculture; Aquatic Pollution; Atmospheric Protection/Air Quality Control/Air Pollution; Biosynthesis; Chondroitin sulfate; Cluster analysis; Clustering; Coastal environments; Connective tissues; Damage; Earth and Environmental Science; Ecotoxicology; Environment; Environmental Chemistry; Environmental Health; Environmental stress; Epithelium; Excretion; Exocytosis; Exposure; Extracellular matrix; Glycosaminoglycans; Glycosyltransferase; Hemocytes; Hemolymph; histology; inflammation; Ion channels; Litopenaeus vannamei; Marine organisms; Metabolism; Molecular modelling; mucus; Research Article; transcriptome; Transcriptomes; Transcriptomics; Vector quantization; Waste Water Technology; Water Management; Water Pollution Control
• ISSN: 1614-7499; 0944-1344; 1614-7499
• DOI: 10.1007/s11356-024-32111-9

Excessive ammonia-N in coastal environment and aquaculture threatens the health of marine organisms. To explore the mechanism of gill damage induced by ammonia-N, transcriptome of Litopenaeus vannamei ’s gill was carried out under 20 mg/L NH 4 Cl for 0, 6, and 48 h. K -means clustering analysis suggested that ammonia excretion and metabolism-related genes were elevated. GO and KEGG enrichment analysis suggested that glycosyltransferase activity and amino acid metabolism were affected by ammonia. Moreover, histological observation via three staining methods gave clues on the changes of gill after ammonia-N exposure. Increased mucus, hemocyte infiltration, and lifting of the lamellar epithelium suggested that gill epithelium was suffering damage under ammonia-N stress. Meanwhile, the composition of extracellular matrix (ECM) in connective tissue changed. Based on the findings of transcriptomic and histological analysis, we further investigated the molecular mechanism of gill damage under multiple concentrations of NH 4 Cl (0, 2, 10, 20 mg/L) for multiple timepoints (0, 3, 6, 12, 24, 48, 72 h). First, ammonia excretion was elevated via ion channel, transporter, and exocytosis pathways, but hemolymph ammonia still kept at a high level under 20 mg/L NH 4 Cl exposure. Second, we focused on glycosaminoglycan metabolism which was related to the dynamics of ECM. It turned out that the degradation and biosynthesis of chondroitin sulfate (CS) were elevated, suggesting that the structure of CS might be destructed under ammonia-N stress and CS played an important role in maintaining gill structure. It was enlightening that the destructions occurred in extracellular regions were vital to gill damage. Third, ammonia-N stress induced a series of cellular responses including enhanced apoptosis, active inflammation, and inhibited proliferation which were closely linked and jointly led to the impairment of gill. Our results provided some insights into the physiological changes induced by ammonia-N and enriched the understandings of gill damage under environmental stress. Graphical Abstract