Integrative functional analyses using rainbow trout selected for tolerance to plant diets reveal nutrigenomic signatures for soy utilization without the concurrence of enteritis

Authors: Abernathy, Jason; BREZAS, ANDREAS - University Of Idaho; SNEKVIK, KEVIN - Washington State University; HARDY, RONALD - University Of Idaho; Overturf, Kenneth - Ken

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/24/2017
Publication Date: 7/19/2017
Citation: Abernathy, J.W., Brezas, A., Snekvik, K., Hardy, R., Overturf, K.E. 2017. Integrative functional analyses using rainbow trout selected for tolerance to plant diets reveal nutrigenomic signatures for soy utilization without the concurrence of enteritis. PLoS One. 12(7). https://doi.org/10.1371/journal.pone.0180972.
DOI: https://doi.org/10.1371/journal.pone.0180972

Interpretive Summary: Currently fishmeal is the major protein component in feeds for carnivorous species, such as salmon and trout. The annual level of fishmeal available has been steadily decreasing while aquaculture growth has been continuing to increase at a rapid pace. This has led to reduced availability of fishmeal and a rapid rise in its cost, thus constraining aquaculture production for a number of commercially important species. Our research group, through genetic selection, has developed the only available carnivorous fish strain that grows rapidly and efficiently on an all plant-protein feed containing high levels of soy protein. In this study we evaluated the differences in metabolic gene regulation of dietary utilization in the liver and muscle between selected and non-selected fish. Our findings provide evidence of discrete gene expression changes between the two strains and identify a number of candidate genes that could be used for improving plant protein dietary utilization in other carnivorous species.

Technical Abstract: Finding suitable alternative protein sources for diets of carnivorous fish species remains a major concern for sustainable aquaculture. Through genetic selection, we created a strain of rainbow trout that outperforms parental lines in utilizing an all-plant protein diet and does not develop enteritis in the distal intestine, as is typical with salmonids on long-term plant protein-based feeds. By incorporating this strain into functional analyses, we set out to determine which genes are critical to plant protein utilization in the absence of gut inflammation. After a 12-week feeding trial with our selected strain and a control trout strain fed either a fishmeal-based diet or an all-plant protein diet, high-throughput RNA sequencing was completed on both liver and muscle tissues. Differential gene expression analyses, weighted correlation network analyses and further functional characterization were performed. A strain-by-diet design revealed differential expression ranging from a few dozen to over one thousand genes among the various comparisons and tissues. Major gene ontology groups identified between comparisons included those encompassing central, intermediary and foreign molecule metabolism, associated biosynthetic pathways as well as immunity. A systems approach indicated that genes involved in purine metabolism were highly perturbed. Systems analysis among the tissues tested further suggests the interplay between selection for growth, dietary utilization and protein tolerance may also have implications for nonspecific immunity. By combining data from differential gene expression and co-expression networks using selected trout, along with ontology and pathway analyses, a set of 63 candidate genes for plant diet tolerance was found. Risk loci in human inflammatory bowel diseases were also found in our datasets, indicating rainbow trout selected for plant-diet tolerance may have added utility as a potential biomedical model.