Article pubs.acs.org/JAFC
Cite This: J. Agric. Food Chem. 2019, 67, 6497−6507
Supplemental Docosahexaenoic-Acid-Enriched Microalgae Affected Fatty Acid and Metabolic Profiles and Related Gene Expression in Several Tissues of Broiler Chicks Samar A. Tolba,†,‡ Tao Sun,† Andrew D. Magnuson,† Guanchen C. Liu,† Walaa M. Abdel-Razik,‡ Mahmoud F. El-Gamal,‡ and Xin Gen Lei*,† †
Department of Animal Science, Cornell University, Ithaca, New York 14853, United States Department of Nutrition and Clinical Nutrition, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44511, Egypt
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S Supporting Information *
ABSTRACT: This experiment was to enrich docosahexaenoic acid (DHA) in broiler tissues through feeding a DHA-rich microalgal biomass and to explore the underlying metabolic and molecular mechanisms. Hatchling Cornish male broilers (total = 192) were fed a corn−soybean meal basal diet containing a full-fatted microalgae (Aurantiochytrium) at 0%, 1%, 2%, and 4% for 6 weeks (n = 6 cages/treatment, 8 birds/cage). The inclusion of microalgae led to dose-dependent (P < 0.01) enrichments of DHA and decreases (P < 0.01) of n-6/n-3 fatty acids (FAs) in plasma, liver, muscle, and adipose tissue. The microalgae supplementation also lowered (P < 0.05−0.1) nonesterified FAs concentrations in the plasma, liver and adipose tissue. The mRNA abundances of most assayed genes involved in lipid metabolism were decreased (P < 0.05) in the liver but elevated (P < 0.05) in the adipose in response to the biomass supplementation. In conclusion, the biomass-resultant DHA enrichments in the broiler tissues were associated with a distinctive difference in the expression of lipid metabolism-controlling genes between the liver and adipose tissue. KEYWORDS: broiler, DHA, enrichment, gene, microalgae
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INTRODUCTION Dietary recommendations evolve over time, particularly due to the shift of n-6/n-3 fatty acids (FAs) in the food supply of Western societies. Moreover, a close relation between deficiency in n-3 polyunsaturated FAs (n-3 PUFAs), particularly docosahexaenoic acid (DHA; C22:6), in the Western diet and noncommunicable diseases such as cardiovascular diseases (CVDs) is well-established. Increased dietary intake of DHA blunts the incidence of these diseases with an improvement in physiological and metabolic function of the body.1−3 The total n-3 PUFA intake by adults in the United States is 1.6 g/day (0.7% of total energy intake), of which 0.1−0.2 g is eicosapentaenoic acid (EPA; 20:5) and DHA.4 The n-6/n-3 PUFA ratio in Western diets is around 10/1 to 20−25/1 compared with the recommended 1/1.1,5 This shortage of n-3 PUFA intake is not only restricted to the United States or Western societies, as globally less than 20% of the world population consumes ≥250 mg/day of seafood n-3 PUFAs.6 Consequently, this phenomenon has led to recommendations of increasing consumption of EPA and DHA from 0.1−0.2 to 0.65 g/day so that the n-6/n-3 PUFA ratios could be improved for better health. Thus, food enrichment is considered as a strategy to manipulate n-3 PUFAs intake from the diet. Our laboratory previously enriched broilers (BR) meat with n-3 PUFAs (0.54− 0.79 mg EPA and DHA/100 g breast muscle)7 through feeding BR a defatted microalgal biomass. It has been well-established that BR meat can be enriched with α-linolenic acid (ALA; 18:3), EPA, and DHA through feeding them diets high in n-3 PUFA (rapeseed oil, fish oil, flaxseed oil, microalgae biomass, or microalgae products),8−12 while, to our best knowledge, few © 2019 American Chemical Society
studies have fully characterized the role of dietary n-3 PUFAs in regulating key genes related to lipid metabolism in the body.13,14 Generally, the health benefits of n-3 PUFAs are related to their potential to be incorporated into or used instantly as substrates for cellular constituent synthesis,15 redirection to other body compartments for being used in different physiological processes,16 and performing their role as a precursor for different metabolites or their action in controlling ß-oxidation.15 Moreover, lipid-derived eicosanoids production may have either a proinflammatory or anti-inflammatory function depending on if they are made from n-6 or n-3 FAs.17 Thus, understanding the mechanism behind the DHA influence on lipid metabolism needs further investigation. Therefore, the primary objectives of our study were (1) to produce DHA-rich BR meat with improved n-6/n-3 PUFAs ratios; (2) to explore the metabolic impact of dietary DHA on the distribution and profile of lipid and FAs in tissues; and (3) to compare the systematic changes of genes controlling lipid biosynthesis and degradation between the two major lipid metabolism-regulatory tissues: liver and adipose tissue.
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MATERIALS AND METHODS
Animals, Diets, and Management. The animal protocol was approved by the Institutional Animal Care and Use Committee of Cornell University. Cornish male BR (day old, total = 192) were Received: Revised: Accepted: Published: 6497
January 26, 2019 May 9, 2019 May 14, 2019 May 14, 2019 DOI: 10.1021/acs.jafc.9b00629 J. Agric. Food Chem. 2019, 67, 6497−6507
Article
Journal of Agricultural and Food Chemistry
Table 1. Effect of Different Concentrations of Microalgal DHA on Plasma and Tissue Fatty Acid Profiles of Broiler Chicks at Week 3a DHAb g/kg diet
P-value
0
1.2
2.4
16:00 16:01 18:00 18:1n-9c 18:2n-6c 18:3n-3 20:4n-6 22:6n-3
0.69 N.D.c 0.64 N.D. 0.85a N.D. N.D. 0c
0.68 N.D. 0.54 N.D. 0.67ab N.D. N.D. 0.29b
0.64 N.D. 0.44 N.D. 0.57b N.D. N.D. 0.38ab
16:00 16:01 18:00 18:1n-9c 18:2n-6c 18:3n-3 20:4n-6 22:6n-3
1.9 0.41 0.58a 2.6a 2.2a N.D. 0.29a 0.00c
1.7 0.35 0.54ab 2.0ab 1.2b N.D. 0.18b 0.38b
1.8 0.39 0.49b 2.0ab 1.3b N.D. 0.13c 0.45b
16:00 16:01 18:00 18:1n-9c 18:2n-6c 18:3n-3 20:4n-6 22:6n-3
2.06 0.43 0.78 2.7a 2.5a 0.05 0.38a 0.00c
2.3 0.58 0.84 2.8a 1.9b 0.07 0.29b 0.41b
2.4 0.52 0.89 2.7a 1.8bc 0.06 0.26b 0.67b
16:00 16:01 18:00 18:1n-9c 18:2n-6c 18:3n-3 20:4n-6 22:6n-3
5.7 0.76 5.1ab N.D. 4.5a N.D. N.D. 0.22c
7.9 1.3 5.3ab N.D. 3.4ab N.D. N.D. 2.4b
6.2 0.71 4.7b N.D. 2.7b N.D. N.D. 3.5ab
4.9 Plasma, mg/mL 0.64 N.D. 0.40 N.D. 0.48b N.D. N.D. 0.48a Breast, mg/g Tissue 1.7 0.37 0.47b 1.6b 1.2b N.D. 0.09c 0.82a Thigh, mg/g Tissue 2.1 0.38 0.78 1.7b 1.4c 0.06 0.20c 1.1a Liver, mg/g Tissue 7.6 0.45 6.0a N.D. 2.7b N.D. N.D. 4.4a
SEM
ANOVA
linear
R2
0.069
0.95
0.61
0.015
0.057
0.062
0.011
0.33
0.061
0.008
