Research Article: Optimizing long chain-polyunsaturated fatty acid synthesis in salmonids by balancing dietary inputs

Date Published: October 10, 2018

Publisher: Public Library of Science

Author(s): Stefanie M. Colombo, Christopher C. Parrish, Manju P. A. Wijekoon, Juan J Loor.

http://doi.org/10.1371/journal.pone.0205347

Abstract

The increasing use of terrestrial plant lipids to replace of fish oil in commercial aquafeeds requires understanding synthesis and storage of long chain-polyunsaturated fatty acids (LC-PUFA) in farmed fish. Manipulation of dietary fatty acids may maximize tissue storage of LC-PUFA, through increased production and selective utilization. A data synthesis study was conducted to estimate optimal levels of fatty acids that may maximize the production and storage of LC-PUFA in the edible portion of salmonids. Data were compiled from four studies with Atlantic salmon, rainbow trout, and steelhead trout (total n = 180) which were fed diets containing different terrestrial-based oils to replace fish oil. LC-PUFA (%) were linearly correlated between diet and muscle tissue (p < 0.001; r2 > 44%), indicating proportional storage after consumption. The slope, or retention rate, was highest for docosahexaenoic acid (DHA) at 1.23, indicating that an additional 23% of DHA was stored in the muscle. Dietary saturated fatty acids were positively related to DHA stored in the muscle (p < 0.001; r2 = 22%), which may involve membrane structural requirements, as well as selective catabolism. DHA was found to be optimally stored with a dietary n-3: n-6 ratio of 1.03: 1. These new results provide a baseline of optimal dietary ratios that can be tested experimentally to determine the efficacy of balancing dietary fatty acids for maximum LC-PUFA storage.

Partial Text

The need to reduce fish meal (FM) and fish oil (FO) levels in aquafeeds has become critical with the growth of the aquaculture industry. This has been, and continues to be, a challenge because FM and FO provide unique nutrients that are required by finfish species, at varying levels depending on species and life stage. In particular, marine resources (i.e., FM and FO) contain significant levels of long-chain polyunsaturated fatty acids (LC-PUFA; ≥ 20 carbons in length), namely the n-3 and n-6 LC-PUFA: eicosapentaenoic acid (EPA; 20:5n-3), docosahexaenoic acid (DHA; 22:6n-3), and arachidonic acid (20:4n-6). These LC-PUFA play numerous physiologically important roles essential to health of all vertebrates [1] and are primarily produced and abundant in marine ecosystems [2]. Although vertebrates have some ability to synthesise LC-PUFA from the C18 precursors linoleic acid (LNA, 18:2n-6) and α-linolenic acid (ALA, 18:3n-3), dietary supply of these LC-PUFA is still required to meet physiological demands. Fish are the primary source of n-3 LC-PUFA for humans [3], and this has prompted interest in LC-PUFA metabolism in fish, with biosynthesis being one of the most targeted pathways under investigation.

Retention of LC-PUFA in fillets has been a research concern since it has become necessary to reduce the level of FO and FM in aquafeeds. Providing a minimum level of LC-PUFA may be adequate to meet basic requirements for fish; however, levels stored in fillet tissue have decreased over time. It has been documented that EPA and DHA have lowered in commercial farmed-raised Atlantic salmon fillets [8]. In order to summarize our previous studies to identify a starting place for subsequent research, we compiled data from four previous experiments to pinpoint optimal levels and ratios of dietary FA that encourage maximum production and yield the highest levels of LC-PUFA in fillets, when feeding diets that are low or devoid in FO. While our study is limited to those compiled from these experiments, these single studies may be representative of other similar experiments that have replaced fish oil in diets for salmonids, so our conclusions could be broadly applicable. However, pooling our data from different species did introduce some variation, and was a significant factor in our regression and multivariate models. Clearly species is a defining factor in the muscle LC-PUFA content between salmon and trout. This could be attributed to lipid and fatty acid metabolism and total dietary lipid levels formulated on a per species basis. Some of the variation is also caused by differences in experimental methods among trials: differences in total lipid in the diet, different diet compositions, different feeding durations, and different rearing temperatures. However, we found patterns in the data despite species differences, which helps make broad inferences on the relationship between diet and tissue composition in a large family of teleosts. While not all relationships that we report in this study are strong explanatory models, this was part of the exploratory process, to determine which relationships could be the strongest predictors of LC-PUFA muscle tissue storage. This can then be used as a starting place for experimental studies in vivo. Using muscle tissue response data from limited dietary lipid sources to investigate dietary FA and LC-PUFA storage we are able to investigate optimal dietary FA levels and ratios. Our study utilized a novel method which draws new, broad conclusions on optimal levels of dietary FA to promote synthesis and storage of LC-PUFA.

Strategies to improve utilization and storage of LC-PUFA in fish may include a balance of dietary n-3 to n-6 ratios, from sustainable sources. We specifically focused on the dietary ALA: LNA ratio and its effect on LC-PUFA accumulation in the muscle tissue, as looking at the total dietary n-3: n-6 is more constrained, as it does not distinguish among members of the same omega family. Abundance of ALA supply does not necessarily improve production of DHA, and while this has been generally observed in single experiments, we found that a one to one ratio of ALA to LNA optimizes DHA storage based on four experiments. Higher ALA to LNA ratios in the diet resulted in greater storage of ALA in the muscle. However, it is worth mentioning that a high n-3 to n-6 ratio (therefore a low n-6 to n-3 ratio) stored in the flesh is still beneficial for human consumption, even if a generous proportion of n-3 is supplied from ALA. A high n-6 to n-3 ratio for human consumers promotes the pathogenesis of many diseases, particularly because an inflammatory state may be activated or exacerbated by a high dietary ratio [40]. The n-6 to n-3 ratio was estimated to be 15 to 20:1 for consumers in Western societies [3], which has been linked with cardiovascular diseases [40] and cognitive decline [41]. This is further concerning if farmed seafood may not be supplying an adequate ratio of n-3 to n-6 [42]. Because consumers depend on seafood as a source of n-3 to balance high dietary n-6, balancing dietary FA inputs for farmed fish could be a beneficial strategy to optimize final muscle tissue levels of the n-3 LC-PUFA.

 

Source:

http://doi.org/10.1371/journal.pone.0205347

 

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