An in vitro study of urea and ammonia production and transport by the intestinal tract of fed and fasted rainbow trout: responses to luminal glutamine and ammonia loading

Abstract

Digestion of dietary protein in teleosts results in high ammonia levels within the intestinal chyme that may reach concentrations that are many-fold greater than blood plasma levels. We used in vitro gut sac preparations of the ammoniotelic rainbow trout (Oncorhynchus mykiss) to investigate the role of the intestine in producing and transporting ammonia and urea, with specific focus on feeding versus fasting, and on responses to loading of the lumen with 2 mmol L−1 glutamine or 2 mmol L−1 ammonia. Feeding increased not only ammonia production and both mucosal and serosal fluxes, but also increased urea production and serosal fluxes. Elevated urea production was accompanied by an increase in arginase activity but minimal CPS III activity, suggesting that urea may be produced by direct arginolysis. The ammonia production and serosal fluxes increased in fasted preparations with glutamine loading, indicating an ability of the intestinal tissue to deaminate glutamine and perhaps use it as an energy source. However, there was little evidence of urea production or transport resulting from the presence of glutamine. Furthermore, the intestinal tissues did not appear to convert surplus ammonia to urea as a detoxification mechanism, as urea production and serosal flux rates decreased in fed preparations, with minimal changes in fasted preparations. Nevertheless, there was indirect evidence of detoxification by another pathway, as ammonia production rate decreased with ammonia loading in fed preparations. Overall, our study suggests that intestinal tissues of rainbow trout have the ability to produce urea and detoxify ammonia, likely via arginolysis.

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Funding

This work was supported by NSERC Discovery grants (NSERC RGPIN 473-2012 and RGPIN 03843-2017) to CMW, who was also supported by the Canada Research Chair Program (Award 203776).

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JS, JGR, and CMW: conceptualization, methodology, investigation. EHJ: formal analysis, writing—original draft preparation. EHJ, JS, JGR, and CMW: writing. All authors—review and editing.

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Correspondence to Ellen H. Jung.

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Jung, E.H., Smich, J., Rubino, J.G. et al. An in vitro study of urea and ammonia production and transport by the intestinal tract of fed and fasted rainbow trout: responses to luminal glutamine and ammonia loading. J Comp Physiol B 191, 273–287 (2021). https://doi.org/10.1007/s00360-020-01335-9

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Keywords

  • Oncorhynchus mykiss
  • Arginase
  • CPS III
  • Ornithine urea cycle
  • Prandial
  • Gastrointestinal tract