Highlights
- •Responses of hens′ cecal bacteria to dietary n-3 polyunsaturated fatty acids assessed.
- •Flaxseed oil or marine algae as sources of n-3 polyunsaturated fatty acids were used.
- •Compared doses supplying 0.20% or 0.60% of diet′s n-3 polyunsaturated fatty acids.
- •Cecal microbes showed distinct clustering patterns with type and dosage of the supplements.
- •Supplements enriched specific microbes that have potential physiological and health benefits to laying hens.
Abstract
Supplementation of n-3 fatty acids to poultry diets is widely acknowledged for its
role in enhancing poultry products, however, little is known about the compositional
responses of gut microbial communities to type and dosage of these supplements. Here,
we compared the effects of n-3 polyunsaturated fatty acids (PUFA), supplied as alpha-linolenic
acid (ALA) or docosahexaenoic acid (DHA), on the composition of bacterial communities
in ceca of laying hens. Corn-soybean basal diets were supplemented with either flaxseed
oil (FO, ALA-rich) or marine algal biomass (MA, DHA-rich), and each supplied 0.20
and 0.60% of total n-3 PUFA in the diet. Lohmann LSL-Classic laying hens (n = 10/treatment) were randomly allocated to one of the 4 diets. After 8 weeks of
feeding, blood, liver and cecal digesta samples were obtained for plasma glucose,
fatty acids, and short chain fatty acids analyses, respectively. The gut bacterial
communities were characterized using genomic DNA extracted from cecal contents, whereby
the V3-V4 hypervariable region of the 16S rRNA gene was sequenced using the Illumina
Miseq® platform. Firmicutes and Bacteroidetes were the predominant phyla in both the FO- and MA-fed groups. The relative abundance
of Tenericutes, often associated with immunomodulation, was relatively higher (P<0.0001) in the FO than MA group. Although the relative abundance of Bacteroides was greater for the FO- than the MA-fed group, this genus was negatively correlated
(P<0.05) with total n-3 PUFA in the liver at higher dosages of both FO- and MA-fed hens.
Higher dose of FO (0.60%) and both dosages of MA (0.20 and 0.60%) substantially enriched
several members of Firmicutes (e.g., Faecalibacterium, Clostridium and Ruminococcus) which are known to produce butyrate. Moreover, co-occurrence network analysis revealed
that, in the FO 0.60- and MA 0.20-fed hens, Ruminococcaceae was the most influential taxon accounting for about 31% of the network complexity.
These findings demonstrate that supplementation of different type and level of n-3
PUFA in hens′ diets could enrich microbial communities with potential role in lipid
metabolism and health.
Keywords
Abbreviations:
FO (flaxseed oil), MA (marine algal biomass), ALA (alpha-linolenic), EPA (eicosapentaenoic), DHA (docosahexaenoic acids)To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Prostaglandins, Leukotrienes and Essential Fatty AcidsAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Microbiota, gut health and chicken productivity: what Is the connection?.Microorganisms (Basel). 2019; 7: 374
- Impact of environmental microbes on the composition of the gut microbiota of adult BALB/c mice.PLoS ONE. 2016; 11e0160568
- Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling.Cell Metab. 2015; 22: 658-668
- The role of the commensal gut microbial community in broiler chickens.Worlds Poult. Sci. J. 2005; 61: 95-104
- Relationship between the microbiota in different sections of the gastrointestinal tract, and the body weight of broiler chickens.Springerplus. 2016; 5: 1-9
- Bacterial succession in the broiler gastrointestinal tract.Appl. Environ. Microbiol. 2016; 82: 2399-2410
- An update on alternatives to antimicrobial growth promoters for broilers.Vet. J. 2011; 187: 182-188
- Effects of different feed additives alone or in combination on broiler performance, gut microflora and ileal histology.Br. Poult. Sci. 2008; 49: 202-212
- Intestinal microbiome of poultry and its interaction with host and diet.Gut Microbes. 2014; 5: 108-119
- Quantitative analysis of the intestinal bacterial community in one-to three-week-old commercially reared broiler chickens fed conventional or antibiotic‐free vegetable-based diets.J. Appl. Microbiol. 2007; 102: 1138-1149
- Diet-induced dysbiosis of the intestinal microbiota and the effects on immunity and disease.Nutrients. 2012; 4: 1095-1119
- Editorial: gut health: the new paradigm in food animal production.Front. Vet. Sci. 2016; 3: 71
- Linking long-term dietary patterns with gut microbial enterotypes.Science. 2011; 334: 105-108
- The role of added feed enzymes in promoting gut health in swine and poultry.Nutr. Res. Rev. 2013; 26: 71-88
- Effects of direct-fed microbials on growth performance, gut morphometry, and immune characteristics in broiler chickens.Poult. Sci. 2010; 89: 203-216
- Effects of direct-fed microbial supplementation on broiler performance, intestinal nutrient transport and integrity under experimental conditions with increased microbial challenge.Br. Poult. Sci. 2014; 55: 89-97
- The effect of dietary oils on cecal microflora in experimental colitis in mice.Indian J. Gastroenterol. 2008; 27: 186
- Omega-3 fatty acids correlate with gut microbiome diversity and production of N-carbamylglutamate in middle aged and elderly women.Sci. Rep. 2017; 7 (11079-11011)
- Long-chain polyunsaturated fatty acids and inflammation.Scand. J. Food Nutr. 2006; 50: 54-61
- Effects of fish oil with a high content of n-3 polyunsaturated fatty acids on mouse gut microbiota.Arch. Med. Res. 2014; 45: 195-202
- Dietary fish oil alters specific and inflammatory immune responses in chicks.J. Nutr. 1997; 127: 2039-2046
- Dietary polyunsaturated fatty acids alter lymphocyte subset proportion and proliferation, serum immunoglobulin G concentration, and immune tissue development in chicks.Poult. Sci. 2000; 79: 1741-1748
- Omega-3 and omega-6 fatty acids in poultry nutrition: effect on production performance and health.Animals. 2019; 9: 573
- Omega-3 polyunsaturated fatty acids enrichment alters performance and immune response in infectious bursal disease challenged broilers.Lipids Health Dis. 2012; 11 (15-15)
- Impact of omega-3 fatty acids on the gut microbiota.Int. J. Mol. Sci. 2017; 18: 2645
- Fish oil, lard and soybean oil differentially shape gut microbiota of middle-aged rats.Sci. Rep. 2017; 7 (826-812)
- Dietary omega-3 polyunsaturated fatty acid does not influence the intestinal microbial communities of broiler chickens.Poult. Sci. 2009; 88: 2399-2405
- A comparison of the effects of antibiotics, probiotics, synbiotics and prebiotics on the performance and carcass characteristics of broilers.Vet. Res. Commun. 2018; 42: 195-207
- Dietary modulation of gut microflora in broiler chickens: a review of the role of six kinds of alternatives to in-feed antibiotics.Worlds Poult. Sci. J. 2009; 65: 97-114
- Poultry coccidiosis: recent advancements in control measures and vaccine development.Expert Rev. Vaccines. 2006; 5: 143-163
- Necrotic enteritis; a continuing challenge for the poultry industry.Worlds Poult. Sci. J. 2006; 62: 221-247
- Potential of fructooligosaccharide prebiotics in alternative and nonconventional poultry production systems.Poult. Sci. 2015; 94: 1411-1418
- Laying hen welfare I. Social environment and space.Worlds Poult. Sci. J. 2016; 72: 333-342
- Lipoprotein metabolism and fattening in poultry.J. Nutr. 1997; 127: 805S-808S
- The form of absorption of lipids in the chicken, Gallus domesticus.Proc. Soc. Exp. Biol. Med. 1972; 141: 814-817
- Contribution of gut bacteria to liver pathobiology.Gastroenterol. Res. Pract. 2010; 2010: 1-13
- Fatty acid profile and sensory characteristics of table eggs from laying hens fed diets containing microencapsulated fish oil.Anim. Feed Sci. Technol. 2010; 156: 97-103
- Growth performance, breast yield, gastrointestinal ecology and plasma biochemical profile in broiler chickens fed multiple doses of a blend of red, brown and green seaweeds.Br. Poult. Sci. 2020;
- Increasing levels of dietary hempseed products leads to differential responses in the fatty acid profiles of egg yolk, liver and plasma of laying hens.J. Lipids. 2016; 51: 615-633
- Hempseed products fed to hens effectively increased n‐3 polyunsaturated fatty acids in total lipids, triacylglycerol and phospholipid of egg yolk.J. Lipids. 2016; 51: 601-614
- Effects of feeding broiler breeder hens a coextruded full-fat flaxseed and pulses mixture without or with multienzyme supplement.Poult. Sci. 2020; 99: 2616-2623
- Effect of n-3 fatty acids on immune function in broiler chickens.Poult. Sci. 2012; 91: 74-88
- Cecal environment and TBARS level in mice fed corn oil, beef tallow and menhaden fish oil.J. Nutr. Sci. Vitaminol. 2000; 46: 65-70
- The care and use of farm animals in research, teaching, and testing.Ottawa, Ontario, Canada. 2009
- Impact of dietary precursor ALA versus preformed DHA on fatty acid profiles of eggs, liver and adipose tissue and expression of genes associated with hepatic lipid metabolism in laying hens.Prostaglandins Leukot. Essent. Fatty Acids. 2017; 119: 1-17
- Effect of flaxseed oil and microalgae DHA on the production performance, fatty acids and total lipids of egg yolk and plasma in laying hens.Prostaglandins Leukot. Essent. Fatty Acids. 2016; 115: 77-88
- Effect of antioxidants and unsaturated fatty acids on reproduction in the hen.J. Nutr. 1962; 76: 284-290
- A simple method for the isolation and purification of total lipides from animal tissues.J. Biol. Chem. 1957; 226: 497-509
- Characterization of microbial populations and volatile fatty acid concentrations in the jejunum, ileum, and cecum of pigs weaned at 17vs 24 days of age.J. Anim. Sci. 2002; 80: 2904-2910
- Effects of yeast culture supplementation on growth performance, intestinal health, and immune response of nursery pigs.J. Anim. Sci. 2009; 87: 2614-2624
- An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform.Microbiome. 2014; 2: 6
- Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2.Nat. Biotechnol. 2019; 37: 852-857
- DADA2: high-resolution sample inference from Illumina amplicon data.Nat. Methods. 2016; 13: 581-583
- Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities.Appl. Environ. Microbiol. 2009; 75: 7537
- STAMP: statistical analysis of taxonomic and functional profiles.Bioinformatics. 2014; 30: 3123-3124
- Metagenomic biomarker discovery and explanation.Genome Biol. 2011; 12: R60
- Inferring correlation networks from genomic survey data.PLoS Comput. Biol. 2012; 8e1002687
- Gephi: an open source software for exploring and manipulating networks.in: International AAAI Conference on Weblogs and Social Media. 2009
- A method of linking multivariate community structure to environmental variables.Mar. Ecol. Prog. Ser. (Halstenbek). 1993; 92: 205-219
- Modularity and community structure in networks.Proc. Natl. Acad. Sci. 2006; 103: 8577-8582
- The influence of diet on the gut microbiota.Pharmacol. Res. 2013; 69: 52-60
- Influence of flaxseed oil on fecal microbiota, egg quality and fatty acid composition of egg yolks in laying hens.Curr. Microbiol. 2016; 72: 259-266
- Proteome and microbiota analysis reveals alterations of liver-gut axis under different stocking density of Peking ducks.PLoS ONE. 2018; 13e0198985
- Spatial and temporal changes in the broiler chicken cecal and fecal microbiomes and correlations of bacterial taxa with cytokine gene expression.Front. Vet. Sci. 2016; 3: 11
- Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative for fish oil.Food Chem. 2014; 160: 393-400
- Alteration of the antioxidant capacity and gut microbiota under high levels of molybdenum and green tea polyphenols in laying hens.Antioxidants. 2019; 8: 503
- High-throughput sequencing reveals the effect of Bacillus subtilis CGMCC 1.921 on the cecal microbiota and gene expression in ileum mucosa of laying hens.Poult. Sci. 2018; 97: 2543-2556
- Effects of wild blueberry (Vaccinium angustifolium) pomace feeding on gut microbiota and blood metabolites in free-range pastured broiler chickens.Poult. Sci. 2019; 98: 3739-3755
- Bacillus subtilis Strain DSM 29784 modulates the cecal Microbiome, concentration of short-chain fatty acids, and apparent retention of dietary components in Shaver White chickens during grower, developer, and laying phases.Appl. Environ. Microbiol. 2019; 85: e00402-e00419
- Effect of dietary porphyran from the red alga, Porphyra yezoensis, on glucose metabolism in diabetic KK-Ay mice.J. Nutr. Sci. Vitaminol. 2012; 58: 14-19
- Faecal bacterial and short-chain fatty acids signature in hypercholesterolemia.Sci. Rep. 2019; 9: 1772
- Beef, casein, and soy proteins differentially affect lipid metabolism, triglycerides accumulation and gut microbiota of high-fat diet-fed C57BL/6J mice.Front. Microbiol. 2018; 9: 2200
- Effects of fish n-3 PUFAs on intestinal microbiota and immune system.Mar. Drugs. 2019; 17: 374
- Position of the academy of nutrition and dietetics: dietary fatty acids for healthy adults.J. Acad. Nutr. Diet. 2014; 114: 136-153
- Conversion of alpha-linolenic acid in humans is influenced by the absolute amounts of alpha-linolenic acid and linoleic acid in the diet and not by their ratio.Am. J. Clin. Nutr. 2006; 84: 44-53
- Metabolism of highly unsaturated n-3 and n-6 fatty acids.Biochim. Biophys. Acta, Mol. Cell. Biol. Lipids. 2000; 1486: 219-231
- Cocoa diet and antibody immune response in preclinical studies.Front. Nutr. (Lausanne). 2017; 4: 28
- Microbial ecology of the murine gut associated with the development of dextran sodium sulfate‐induced colitis.Inflamm. Bowel Dis. 2011; 17: 917-926
- Gut microbial metabolites fuel host antibody responses.Cell Host Microbe. 2016; 20: 202-214
- Pistachio consumption alleviates inflammation and improves gut microbiota composition in mice fed a high-fat diet.Int. J. Mol. Sci. 2020; 21: 365
- Dietary flaxseed oil rich in omega-3 suppresses severity of type 2 diabetes mellitus via anti-inflammation and modulating gut microbiota in rats.Lipids Health Dis. 2020; 19 (20-16)
- Session: short-chain fatty acids. Regulation of short-chain fatty acid production.Proc. Nutr. Soc. 2003; 62: 67-72
- Ruminococcus gnavus, a member of the human gut microbiome associated with Crohn's disease, produces an inflammatory polysaccharide.Proc. Natl. Acad. Sci. 2019; 116: 12672-12677
- Interaction between chicken intestinal microbiota and protein digestion.Anim. Feed Sci. Technol. 2016; 221: 323-330
- Identification and characterization of potential performance-related gut microbiotas in broiler chickens across various feeding trials.Appl. Environ. Microbiol. 2011; 77: 5868-5878
- The butyrate story: old wine in new bottles?.Curr. Opin. Clin. Nutr. Metab. Care. 2004; 7: 563-567
- Is bile acid a determinant of the gut microbiota on a high-fat diet?.Gut Microbes. 2014; 3: 455-459
- The influence of polyunsaturated fatty acids on probiotic growth and adhesion.FEMS Microbiol. Lett. 2001; 194: 149-153
- The fatty acid composition of excreta of broiler chickens fed different dietary fatty acids.Int. J. Poult. Sci. 2017; 16: 424-443
- Omega-3 fatty acids and inflammatory processes.Nutrients. 2010; 2: 355-374
- The nutritional significance of lipid rafts.Annu. Rev. Nutr. 2009; 29: 257-282
- n-3 polyunsaturated fatty acids prevent disruption of epithelial barrier function induced by proinflammatory cytokines.Mol. Immunol. 2008; 45: 1356-1365
- Role of FADS1 and FADS2 polymorphisms in polyunsaturated fatty acid metabolism.Metab. 2010; 59: 993-999
- Diet-gene interactions and PUFA metabolism: a potential contributor to health disparities and human diseases.Nutrients. 2014; 6: 1993-2022
- Mechanisms of action of (n-3) fatty acids.J. Nutr. 2012; 142: 592S-599S
- Updates to the n-3 polyunsaturated fatty acid biosynthesis pathway: DHA synthesis rates, tetracosahexaenoic acid and (minimal) retroconversion.Prog. Lipid Res. 2019; 76
- Alpha-linolenic acid and its conversion to longer chain n−3 fatty acids: benefits for human health and a role in maintaining tissue n−3 fatty acid levels.Prog. Lipid Res. 2009; 48: 355-374
- α-Linolenic acid metabolism in men and women: nutritional and biological implications.Curr. Opin. Clin. Nutr. Metab. Care. 2004; 7: 137-144
- The effect of microbiome modulation on the intestinal health of poultry.Anim. Feed Sci. Technol. 2019; 250: 32-40
- Lipid biosynthesis in the chick. A consideration of site of synthesis, influence of diet and possible regulatory mechanisms.Poult. Sci. 1975; 54: 1075-1093
- Gastrointestinal tract microbiota and probiotics in production animals.Annu. Rev. Anim. Biosci. 2014; 2: 469-486
- Lipid metabolism.in: Bell D.J. Freeman B.M. Physiology and Biochemistry of the Domestic Fowl. Academic Press, London1983: 165-174
- Chia seed (Salvia hispanica L.) as an ω-3 fatty acid source for broilers: influence on fatty acid composition, cholesterol and fat content of white and dark meats, growth performance, and sensory characteristics.Poult. Sci. 2002; 81: 826-837
- Vitamin profiles of eggs as indicators of nutritional-status in the laying hen - Diet to egg transfer and commercial flock survey.Poult. Sci. 1993; 72: 1046-1053
- Polyunsaturated fatty acid regulation of genes of lipid metabolism.Annu. Rev. Nutr. 2005; 25: 317-340
- Role of coccidia in the occurrence of necrotic enteritis of chickens.Avian Dis. 1980; 24: 324-333
- The interplay between Campylobacter and Helicobacter species and other gastrointestinal microbiota of commercial broiler chickens.Gut Pathog. 2014; 6: 18
- Understanding the impact of omega-3 rich diet on the gut microbiota.Case Rep. Med. 2016; 2016: 1-6
- Digestion, absorption and effects on cholesterol absorption of menhaden oil, fish oil concentrate and corn oil by rats.J. Nutr. 1987; 117: 1676-1680
- Insights into the role of Erysipelotrichaceae in the human host.Front. Cell. Infect. Microbiol. 2015; 5: 84
- Changes in gut microbiota in rats fed a high fat diet correlate with obesity-associated metabolic parameters.PLoS ONE. 2015; 10e0126931
- Feeding a DHA-enriched diet increases skeletal muscle protein synthesis in growing pigs: association with increased skeletal muscle insulin action and local mRNA expression of insulin-like growth factor 1.Br. J. Nutr. 2013; 110: 671-680
- Intestinal structure and function of broiler chickens on diets supplemented with a synbiotic containing Enterococcus faecium and oligosaccharides.Int. J. Mol. Sci. 2008; 9: 2205-2216
- The gut microbiota as an environmental factor that regulates fat storage.Proc. Natl. Acad. Sci. 2004; 101: 15718-15723
- Microbial populations in naked neck chicken ceca raised on pasture flock fed with commercial yeast cell wall prebiotics via an Illumina MiSeq platform.PLoS ONE. 2016; 11e0151944
- Evaluation of the performance and intestinal gut microflora of broilers fed on corn-soy diets supplemented with Bacillus subtilis PB6 (CloSTAT).J. Appl. Poult. Res. 2007; 16: 296-303
- Molecular fingerprints of the human fecal microbiota from 9 to 18 months old and the effect of fish oil supplementation.J. Pediatr. Gastr. Nutr. 2011; 53: 303-309
- Enhancement of nutraceutical value of table eggs through poultry feeding strategies.Int. J. Pharmacol. 2015; 11: 201-212
- Lipidomic characterization of omega-3 polyunsaturated fatty acids in phosphatidylcholine and phosphatidylethanolamine species ofegg yolk lipid derived from hens fed flaxseed oil and marine algal biomass.in: Prostaglandins Leukot. Essent. Fatty Acids, 161. 2020
- Effect of dietary fat sources and antioxidant types on growth performance and carcass quality of Japanese quails.Int. J. Poult. Sci. 2017; 16: 443-450
- The interactive effect of dietary n-6:n-3 fatty acid ratio and vitamin E level on tissue lipid peroxidation, DNA damage in intestinal epithelial cells, and gut morphology in chickens of different ages.Poult. Sci. 2018; 97: 149-158
- Microflora of the digestive tract critical factors and consequences for poultry.Worlds Poult. Sci. J. 2006; 62: 499-511
- Impact of polyunsaturated fatty acids on human colonic bacterial metabolism: an in vitro and in vivo study.Br. J. Nutr. 1995; 74: 733-741
Article info
Publication history
Published online: September 28, 2020
Accepted:
September 24,
2020
Received in revised form:
September 24,
2020
Received:
July 31,
2020
Identification
Copyright
Crown Copyright © 2020 Published by Elsevier Ltd. All rights reserved.
