Investigation of biomarkers of early taurine deficiency in Florida pompano Trachinotus carolinus

Abstract

Despite garnering high interest in fish nutrition as an essential amino acid in a number of teleosts, the metabolic and physiological functions of taurine remain poorly described in fish. This study describes the postprandial changes of taurine in Florida pompano juveniles fed a taurine-replete diet, followed by a wide screening of metabolic and physiological markers when fed a taurine-deficient diet over 16days. The goal was to screen for markers of early taurine deficiency and identify its initial components. Postprandial taurine levels varied between 106.75 and 170.37μg/ml with a mild peak at 2–4h after feeding, and decreased to 72.1% of the baseline value at 6h. Fish fed the taurine-deficient diet did not have reduced hematocrit or increased bilirubin, suggesting an absence of hemolysis. However, linear decreases in alkaline phosphatase activity and in bile acid content were observed (R2=0.5968 and 0.5613, respectively, P<0.005). Filet composition showed an overall linear increase in moisture (R2=0.2666, P=0.0338) and a marked, linear loss in lipid over time (R2=0.4059, P=0.0059). There was also a drastic, quadratic decrease in all amino acid content of the liver (R2>0.75, P<0.0001), which had decreased by 40% by day 16. Notably, levels of taurine, hydroxylysine and hydroxyproline sharply decreased and remained low. In the filet however, levels of most amino acids were not affected, except for hydroxyproline, hydroxylysine, proline, and glycine, whose levels increased significantly by day 16 while taurine levels had decreased. Serum levels were variable, and no pattern of change could be identified. Liver histology revealed marked vacuolation of hepatocytes and significant glycogen accumulation. Finally, hepatic mitochondrial proteins quadratically decreased with time (R2=0.6218, P=0.0007), paralleled with a severe linear decrease in cytochrome c oxidase (COX) specific activity (R2=0.5940, P=0.0002). This indicates that the mitochondrial electron transport chain was greatly disrupted, and which resulted in poor hepatic metabolism and production of oxidative radicals. In summary, the present study describes the first screening for metabolic and physiological biomarkers of early taurine deficiency. Although we found no evidence of overt hepatocellular damage during the course of the experiment, we observed significant alterations of cellular metabolism, especially in hepatocytes (i.e., histology, amino acid content, COX activity). Changes in serum parameters were detected, although their suitability as biomarkers will require additional research. The absence of hematocrit decrease is noteworthy in light of published literature; longer term investigations are necessary to further our understanding of taurine functions in teleosts. Statement of relevanceThis manuscript presents results of scientific research relevant to the field of aquaculture. Taurine is a nutrient of great importance for many teleost species and for the sustainability of fish feeds; yet its metabolic functions remain unclear. This study constitutes, to the authors' knowledge, the first attempt at characterizing these functions. These results shed light on the complexities of taurine metabolism and emphasize possible hypotheses for future research. Therefore this study presents novel research results of high interest to the aquaculture and fish biology communities.