13C values of glycolytic amino acids as indicators of carbohydrate utilization in carnivorous fish

Yiming V Wang; Alex H L Wan; Åshild Krogdahl; Mark Johnson; Thomas Larsen

doi:10.7717/peerj.7701

¹³C values of glycolytic amino acids as indicators of carbohydrate utilization in carnivorous fish

PeerJ. 2019 Sep 18:7:e7701. doi: 10.7717/peerj.7701. eCollection 2019.

Authors

Yiming V Wang¹, Alex H L Wan², Åshild Krogdahl³, Mark Johnson², Thomas Larsen¹

Affiliations

¹ Department of Archaeology, Max Planck Institute for the Science of Human History, Jena, Germany.
² Aquaculture Nutrition and Aquafeed Research Unit and Irish Seaweed Research Group, Ryan Institute, National University of Ireland, Galway, Ireland.
³ Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Oslo, Norway.

Abstract

Background: Stable isotope analysis of single amino acids (AA) is usually applied in food web studies for tracing biosynthetic origins of AA carbon backbones and establishing trophic positions of consumers, but the method is also showing promise for characterizing quantity and quality of dietary lipids and carbohydrates.

Methods: To investigate whether changes in high- and low-digestible carbohydrates affect δ ¹³C values of glycolytic AA, i.e., AA carbon backbones sourced from the glycolytic pathway, we compared Atlantic salmon (Salmo salar) from a feeding experiment with and without dietary inclusion of the red macroalga Palmaria palmata. The Control and experimental diets had similar relative proportions of macronutrients, but their ingredients differed; in the experimental treatment, 15% Palmaria inclusion substituted proteins from fishmeal and carbohydrates from corn starch.

Results: We found that ¹³C values of the glycolytic AA were highly sensitive to substitution of corn starch with Palmaria. The δ ¹³C offsets of glycolytic AA between salmon and their diets were significantly greater in the Palmaria inclusion than Control treatment. This greater offset can be attributed to the different utilization of high- vs. low-digestible carbohydrate sources, i.e., corn starch vs. Palmaria, in the two treatments, and metabolic routing of dietary lipids. In addition, similar δ ¹³C values of essential AA between treatments indicate similar nutrient assimilation efficiency for all terrestrial (pea protein concentrate and wheat gluten meal) and marine (fishmeal and red alga) derived protein sources. These results show that δ ¹³C_AA analysis is a promising tool for improving our understanding of how carnivorous fish utilize macronutrient and route metabolic intermediates to tissue.

Keywords: Assimilation; Compound specific isotopes; High- and low-digestible carbohydrates; Naturally occurring 13C isotope variability; Non-essential amino acids; Palmaria palmata; Protein metabolism; Salmo salar; Stable isotope fingerprinting of amino acids; Starch.

Grants and funding

This work was supported by the Cluster of Excellence 80 “The Future Ocean”. The “Future Ocean” is funded within the framework of the Excellence Initiative by the Deutsche Forschungsgemeinschaft (DFG) on behalf of the German federal and state governments. Yiming V. Wang was supported by the German Federal Ministry of Education and Research (BMBF) [grant No. 03F0722A] during 2017–2018. Thomas Larsen is supported by BMBF [grant No. 07F00805A]. Alex H.L. Wan was supported by Grant-Aid [Agreement No. MFFRI/07/01] under the Sea Change Strategy with the support of the Marine Institute and also National Development Plan 2007–2013 grant to the Department of Agriculture, Food and the Marine, Ireland. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.