Regulation of amino acid metabolism as a defensive strategy in the brain of three freshwater teleosts in response to high environmental ammonia exposure

• Published in: Aquatic toxicology Vol. 130-131; pp. 86 - 96
• Main Authors: Sinha, Amit Kumar, Giblen, Terri, AbdElgawad, Hamada, De Rop, Michelle, Asard, Han, Blust, Ronny, De Boeck, Gudrun
• Format: Journal Article
• Language: English
• Published: Amsterdam Elsevier B.V 15.04.2013; Elsevier
• Subjects: alanine; alanine transaminase; amino acid metabolism; Amino Acids - metabolism; ammonia; Ammonia - metabolism; Ammonia - toxicity; Animal and plant ecology; Animal, plant and microbial ecology; Animals; Applied ecology; aspartate transaminase; Biological and medical sciences; brain; Brain - drug effects; Brain - enzymology; Brain - metabolism; Carassius auratus; Carps - metabolism; Common carp; Cyprinus carpio; Ecotoxicology, biological effects of pollution; Environmental Exposure; Fish Proteins - metabolism; Free amino acids; Fresh water ecosystems; freshwater; Fundamental and applied biological sciences. Psychology; General aspects; glutamate dehydrogenase; Glutamate dehydrogenase (GDH); glutamate-ammonia ligase; Glutamine; Glutamine - metabolism; Glutamine synthetase (GSase); Goldfish; Goldfish - metabolism; High environmental ammonia (HEA); Inactivation, Metabolic; Mass Spectrometry; Oncorhynchus mykiss; Oncorhynchus mykiss - metabolism; Rainbow trout; Species Specificity; Synecology; Teleostei; Time Factors; toxicity; trout; urea; Urea - metabolism; Water Pollutants, Chemical - metabolism; Water Pollutants, Chemical - toxicity; Common carp; AST; HEA; GSase; ALT; GDH; FAAs; Glutamine synthetase (GSase); Free amino acids; α-KG; High environmental ammonia (HEA); Rainbow trout; Glutamate dehydrogenase (GDH); Goldfish; Glutamine; Brain; Toxicity; Dehydrogenase; Freshwater environment; Aquatic environment; Pisces; Cyprinus carpio; Osteichthyes; Ecotoxicology; Enzyme; Glutamate; Metabolism; Oncorhynchus mykiss; Ammonia; Vertebrata; Carassius auratus; Aminoacid; Strategy; Oxidoreductases; Teleostei
• ISSN: 0166-445X; 1879-1514
• DOI: 10.1016/j.aquatox.2013.01.003

► Role of amino acid metabolism in ammonia detoxification process was tested in trout, carp and goldfish brain. ► At 1mM NH3 exposure, goldfish and carp could reduce accumulated ammonia in brain to control level. ► Glutamine level increased significantly in goldfish and carp at 24–48h but delayed in trout. ► During exposure periods, glutamate pool was maintained in cyprinids but depleted in trout. ► Protective strategies to combat ammonia toxicity in brain are more pronounced in carp and goldfish than in trout. Many teleosts have evolved mechanisms to cope with ammonia toxicity in the brain when confronted with high environmental ammonia (HEA). In the present study, the possible role of conversion of accumulated ammonia to glutamine and other free amino acids in the brain of three freshwater teleosts differing in their sensitivities to ammonia was investigated. The detoxification mode of ammonia in brain is suggested to be through amination of glutamate to glutamine by the coupled activities of glutamate dehydrogenase (GDH), transaminase (aspartate aminotransaminase ‘AST’ and alanine aminotransaminase ‘ALT’) and glutamine synthetase (GSase). We investigated the metabolic response of amino acids in the brain of highly sensitive salmonid Oncorhynchus mykiss (rainbow trout), the less sensitive cyprinid Cyprinus carpio (common carp) and the highly resistant cyprinid Carassius auratus (goldfish) when exposed to 1mM ammonia (as NH4HCO3; pH 7.9) for 0h (control), 3h, 12h, 24h, 48h, 84h and 180h. Results show that HEA exposure increased ammonia accumulation significantly in the brain of all the three species from 12h onwards. Unlike in trout, ammonia accumulation in carp and goldfish was restored to control levels (48–84h); which was accompanied with a significant increase in glutamine content as well as GSase activity. In trout, glutamine levels also increased (84–180h) but GSase was not activated. The elevated glutamine level in trout was accompanied by a significant depletion of the glutamate pool in contrast to the stable glutamate levels seen in carp and goldfish. This suggests a simultaneous increase in the rate of glutamate formation to match with the demand of glutamine formation in cyprinids. The activity of GDH was elevated significantly in carp and goldfish but remained unaltered in trout. Also, the transaminase enzymes (AST and ALT) were elevated significantly in exposed carp and goldfish while only ALT was up-regulated in trout. Consequently, in carp and goldfish both aspartate and alanine were utilized under HEA, whereas only alanine was consumed in trout. With ammonia treatment, significant changes in concentrations of other amino acids also occurred. None of the species could detoxify brain ammonia into urea. This study suggests that protective strategies to combat ammonia toxicity in brain are more pronounced in carp and goldfish than in trout.