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Transcriptional shifts account for divergent resource allocation in feed efficient broiler chickens.

ABSTRACT: Considerable variation in feed efficiency (FE) has been observed in indigenous and selected meat-type chicken populations. Although this variation could be partially linked to extrinsic factors like diet, housing environment and microbiota, it further illustrates the existence of strong molecular mechanisms enabling the differential allocation of resources for various physiological processes. To further deepen the molecular basis of individual allocation capacity in male and female broilers, an RNA-seq experiment was conducted which based on a phenotyped chicken population divergent in FE. Transcriptional differences linked to FE were pronounced in intestinal and muscular tissue sites of male animals. Specifically, signalling pathways of farnesoid X receptor (FXR) and retinoid X receptor (RXR) might contribute to mediate individual FE. The transcriptional profiles suggested ACSBG2 (muscular lipid utilisation), ASBT (intestinal bile salt transport), CLEC2B (natural killer cell activation), HMGCS2 (jejunal, duodenal and muscular ketogenesis), and SCARB1 (jejunal lipid uptake) as potential mediators driving FE. Results indicate that improvements in FE exploit shifts in resource allocation which might occur at the expense of general immune responsiveness in high efficient male chickens. Consequently, to further improve FE traits and to explore causative molecular patterns, effects originating from sex-dimorphism in chickens need to be taken into consideration.

SUBMITTER: Reyer H

PROVIDER: S-EPMC6110741 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Transcriptional shifts account for divergent resource allocation in feed efficient broiler chickens.

Reyer Henry H Metzler-Zebeli Barbara U BU Trakooljul Nares N Oster Michael M Muráni Eduard E Ponsuksili Siriluck S Hadlich Frieder F Wimmers Klaus K

Scientific reports 20180827 1

Considerable variation in feed efficiency (FE) has been observed in indigenous and selected meat-type chicken populations. Although this variation could be partially linked to extrinsic factors like diet, housing environment and microbiota, it further illustrates the existence of strong molecular mechanisms enabling the differential allocation of resources for various physiological processes. To further deepen the molecular basis of individual allocation capacity in male and female broilers, an ...[more]

PMID: 30150666

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Project description:Differences in chickens' feed intake may be the underlying factor influencing feed-efficiency (FE)-associated variation in intestinal microbiota and physiology. In chickens eating the same amount of feed, quantitative feed restriction may create similar intestinal conditions and help clarify this cause-and-effect relationship. This study investigated the effect of ad libitum versus restrictive feeding (85% of ad libitum) on ileal and cecal microbiota, concentrations of short-chain fatty acids, visceral organ size, intestinal morphology, permeability, and expression of genes related to nutrient uptake, barrier function, and innate immune response in broiler chickens with divergent residual feed intake (RFI; metric for FE). On day 30 posthatch, 28 low-RFI (good FE) and 29 high-RFI (poor FE) chickens across both feeding-level groups (n?=?112) were selected. Supervised multigroup data integration and relevance network analyses showed that especially Lactobacillus (negative) in ileal digesta, Turicibacter (positive) in cecal digesta, and Enterobacteriaceae (positive) in both intestinal segments depended on chicken's feed intake, whereas the level of Anaerotruncus in cecal digesta was most discriminative for high RFI. Moreover, shallower crypts and fewer goblet cells in ceca indicated host-related energy-saving mechanisms with low RFI, whereas greater tissue resistance suggested a stronger jejunal barrier function in low-RFI chickens. Values corresponding to feed intake level × RFI interactions indicated larger pancreas and lower levels of ileal and cecal short-chain fatty acids in restrictively fed high-RFI chickens than in the other 3 groups, suggesting host physiological adaptations to support greater energy and nutrient needs of high-RFI chickens compensating for the restricted feeding. IMPORTANCE The impact of the FE-associated differences in feed intake on intestinal bacterial and host physiological parameters has so far not been clarified. Understanding the underlying principles is essential for the development of cost-effective strategies to improve FE in chicken production. Under conditions of quantitative feed restriction, low- and high-RFI chickens ate the same amount of feed. Therefore, this research helps in distinguishing intestinal bacterial taxa and functions that were highly reliant on feed intake from those that were associated with physiological adaptations to RFI-associated differences in host nutritional needs and intestinal nutrient availability. This work provides a background for further research to assess manipulation of the intestinal microbiota, host physiology, and FE in chickens by dietary intervention.

Project description:BackgroundIntestinal microbiota plays a key role in nutrient digestion and utilization with a profound impact on feed efficiency of livestock animals. However, the intestinal microbes that are critically involved in feed efficiency remain elusive.MethodsTo identify intestinal bacteria associated with residual feed intake (RFI) in chickens, male Cobb broiler chicks were individually housed from day 14 to day 35. Individual RFI values were calculated for 56 chickens. Luminal contents were collected from the ileum, cecum, and cloaca of each animal on day 35. Bacterial DNA was isolated and subjected to 16S rRNA gene sequencing. Intestinal microbiota was classified to the feature level using Deblur and QIIME 2. High and low RFI groups were formed by selecting 15 and 17 chickens with the most extreme RFI values for subsequent LEfSe comparison of the difference in the microbiota. Spearman correlation analysis was further performed to identify correlations between the intestinal microbiota composition and RFI.ResultsNo significant difference in evenness, richness, and overall diversity of the microbiota in the ileum, cecum, or cloaca was observed between high and low RFI chickens. However, LEfSe analysis revealed a number of bacterial features being differentially enriched in either high or low RFI chickens. Spearman correlation analysis further identified many differentially enriched bacterial features to be significantly correlated with RFI (P < 0.05). Importantly, not all short-chain fatty acid (SCFA) producers showed a positive association with RFI. While two novel members of Oscillibacter and Butyricicoccus were more abundant in low-RFI, high-efficiency chickens, several other SCFA producers such as Subdoligranulum variabile and two related Peptostreptococcaceae members were negatively associated with feed efficiency. Moreover, a few closely-related Lachnospiraceae family members showed a positive correlation with feed efficiency, while others of the same family displayed an opposite relationship.ConclusionsOur results highlight the complexity of the intestinal microbiota and a need to differentiate the bacteria to the species, subspecies, and even strain levels in order to reveal their true association with feed efficiency. Identification of RFI-associated bacteria provides important leads to manipulate the intestinal microbiota for improving production efficiency, profitability, and sustainability of poultry production.

Project description:We contrast the pectoralis muscle transcriptomes of broilers selected from within a single genetic line expressing divergent feed efficiency (FE) in an effort to improve our understanding of the mechanistic basis of FE.Application of a virtual muscle model to gene expression data pointed to a coordinated reduction in slow twitch muscle isoforms of the contractile apparatus (MYH15, TPM3, MYOZ2, TNNI1, MYL2, MYOM3, CSRP3, TNNT2), consistent with diminishment in associated slow machinery (myoglobin and phospholamban) in the high FE animals. These data are in line with the repeated transition from red slow to white fast muscle fibres observed in agricultural species selected on mass and FE. Surprisingly, we found that the expression of 699 genes encoding the broiler mitoproteome is modestly-but significantly-biased towards the high FE group, suggesting a slightly elevated mitochondrial content. This is contrary to expectation based on the slow muscle isoform data and theoretical physiological capacity arguments. Reassuringly, the extreme 40 most DE genes can successfully cluster the 12 individuals into the appropriate FE treatment group. Functional groups contained in this DE gene list include metabolic proteins (including opposing patterns of CA3 and CA4), mitochondrial proteins (CKMT1A), oxidative status (SEPP1, HIG2A) and cholesterol homeostasis (APOA1, INSIG1). We applied a differential network method (Regulatory Impact Factors) whose aim is to use patterns of differential co-expression to detect regulatory molecules transcriptionally rewired between the groups. This analysis clearly points to alterations in progesterone signalling (via the receptor PGR) as the major driver. We show the progesterone receptor localises to the mitochondria in a quail muscle cell line.Progesterone is sometimes used in the cattle industry in exogenous hormone mixes that lead to a ~20% increase in FE. Because the progesterone receptor can localise to avian mitochondria, our data continue to point to muscle mitochondrial metabolism as an important component of the phenotypic expression of variation in broiler FE.

Project description:There is a great interest to understand the impact of the gut microbiota on host's nutrient use and FE in chicken production. Both chicken's feed intake and gut bacterial microbiota differ between high and low-feed efficient chickens. To evaluate the impact of the feed intake level on the feed efficiency (FE)-associated variation in the chicken intestinal microbiota, differently feed efficient chickens need to eat the same amount of feed, which can be achieved by feeding chickens restrictively. Therefore, we investigated the effect of restrictive vs. ad libitum feeding on the fecal microbiome at 16 and 29 days posthatch (dph), FE and nutrient retention in chickens of low and high residual feed intake (RFI; metric for FE). Restrictively fed chickens were provided the same amount of feed which corresponded to 85% of the ad libitum fed group from 9 dph. FE was determined for the period between 9 and 30 dph and feces for nutrient retention were collected on 31 to 32 dph. From the 112 chickens (n = 56 fed ad libitum, and n = 56 fed restrictively), 14 low RFI and 15 high RFI ad libitum fed chickens, and 14 low RFI (n = 7 per sex) and 14 high RFI restrictively fed chickens were selected as the extremes in RFI and were retrospectively chosen for data analysis. Bray-Curtis dissimilarity matrices showed significant separation between time points, and feeding level groups at 29 dph for the fecal bacterial communities. Relevance networking indicated positive associations between Acinetobacter and feed intake at 16 dph, whereas at 29 dph Escherichia/Shigella and Turicibacter positively and Lactobacillus negatively correlated to chicken's feed intake. Enterobacteriaceae was indicative for low RFI at 16 dph, whereas Acinetobacter was linked to high RFI across time points. However, restrictive feeding-associated changes in the fecal microbiota were not similar in low and high RFI chickens, which may have been related to the higher nutrient retention and thus lower fecal nutrient availability in restrictively fed high RFI chickens. This may also explain the decreased RFI value in restrictively fed high RFI chickens indicating improved FE, with a stronger effect in females.

Dataset Information

Transcriptional shifts account for divergent resource allocation in feed efficient broiler chickens.

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Transcriptional shifts account for divergent resource allocation in feed efficient broiler chickens.

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