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Whole-body protein turnover reveals the cost of detoxification of secondary metabolites in a vertebrate browser

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Abstract

The detoxification limitation hypothesis predicts that the metabolism and biotransformation of plant secondary metabolites (PSMs) elicit a cost to herbivores. There have been many attempts to estimate these costs to mammalian herbivores in terms of energy, but this ignores what may be a more important cost—increases in protein turnover and concomitant losses of amino acids. We measured the effect of varying dietary protein concentrations on the ingestion of two PSMs (1,8 cineole—a monoterpene, and benzoic acid—an aromatic carboxylic acid) by common brushtail possums (Trichosurus vulpecula). The dietary protein concentration had a small effect on how much cineole possums ingested. In contrast, protein had a large effect on how much benzoate they ingested, especially at high dietary concentrations of benzoate. This prompted us to measure the effects of dietary protein and benzoate on whole-body protein turnover using the end-product method following an oral dose of [15N] glycine. Increasing the concentration of dietary protein in diets without PSMs improved N balance but did not influence whole-body protein turnover. In contrast, feeding benzoate in a low-protein diet pushed animals into negative N balance. The concomitant increases in the rates of whole-body protein turnover in possums eating diets with more benzoate were indicative of a protein cost of detoxification. This was about 30 % of the dietary N intake and highlights the significant effects that PSMs can have on nutrient metabolism and retention.

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Acknowledgments

The Animal Experimentation Ethics Committee of the Australian National University approved the work described in this paper, which conforms to the Australian Code of Practice for the Care and Use of Animals for Scientific Purposes. We thank Ms Bori Cser for helping with the maintenance of the possums. We are grateful to Dr. Hilary Stuart-Williams (Research School of Biology, ANU) for help with mass spectrometry and to Dr. Terry Neeman of the Statistical Consulting Unit, ANU for advice on experimental design and analysis. The comments of Amanda Padovan and an anonymous reviewer greatly improved the manuscript. A DECRA Fellowship (DE120101263) to KJM from the Australian Research Council funded this work.

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Correspondence to Ian R. Wallis.

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Communicated by I.D. Hume.

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Au, J., Marsh, K.J., Wallis, I.R. et al. Whole-body protein turnover reveals the cost of detoxification of secondary metabolites in a vertebrate browser. J Comp Physiol B 183, 993–1003 (2013). https://doi.org/10.1007/s00360-013-0754-3

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  • DOI: https://doi.org/10.1007/s00360-013-0754-3

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