Dataset Information

Microbiome-host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model.

ABSTRACT:

Background

Ruminant gastrointestinal tract homeostasis deploys interactive microbiome-host metabolic communication and signaling axes to underpin the fitness of the host. After this stable niche is destroyed by environmental triggers, remodeling of homeostasis can occur as a spontaneous physiological compensatory actor.

Results

In this study, 20 sheep were randomly divided into four groups: a hay-fed control (CON) group and a high-grain (HG) diet group for 7, 14, or 28?days. Then, we examined 16S rRNA gene sequences and transcriptome sequences to outline the microbiome-host co-oscillation patterns in remodeling of colonic homeostasis in a sheep model during adaptation to a HG diet. Our data revealed that with durations of an HG diet, the higher starch levels directly affected the colonic lumen environment (lower pH and higher fermentation parameters), which in turn filtered lumen-specific functional taxonomic groups (HG-sensitive and HG-tolerant taxa). The colonic epithelium then gave rise to a new niche that triggered endoplasmic reticulum stress to activate unfolded protein response, if the duration of endoplasmic reticulum stress was overlong, this process would regulate cell apoptosis (Caspase-3, Caspase-8, and TNFRSF21) to achieve a functional transformation.

Conclusions

Our results provide a holistic view of the colonic microbial assemblages and epithelium functional profile co-oscillation patterns in remodeling of colonic homeostasis during adaptation to an HG diet in a sheep model. These findings also provide a proof of concept that the microbe-host collaboration is vital for maintaining hindgut homeostasis to adapt to dietary dichotomies.

SUBMITTER: Lin L

PROVIDER: S-EPMC7807687 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Publications

Microbiome-host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model.

Lin Limei L Wang Yue Y Xu Lei L Liu Junhua J Zhu Weiyun W Mao Shengyong S

Animal microbiome 20200709 1

<h4>Background</h4>Ruminant gastrointestinal tract homeostasis deploys interactive microbiome-host metabolic communication and signaling axes to underpin the fitness of the host. After this stable niche is destroyed by environmental triggers, remodeling of homeostasis can occur as a spontaneous physiological compensatory actor.<h4>Results</h4>In this study, 20 sheep were randomly divided into four groups: a hay-fed control (CON) group and a high-grain (HG) diet group for 7, 14, or 28 days. Then, ...[more]

PMID: 33499965

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Project description:High-grain adaptation programs are widely used with feedlot cattle to balance enhanced growth performance against the risk of acidosis. This adaptation to a high-grain diet from a high-forage diet is known to change the rumen microbial population structure and help establish a stable microbial population within the rumen. Therefore, to evaluate bacterial population dynamics during adaptation to a high-grain diet, 4 ruminally cannulated beef steers were adapted to a high-grain diet using a step-up diet regimen containing grain and hay at ratios of 20:80, 40:60, 60:40, and 80:20. The rumen bacterial populations were evaluated at each stage of the step-up diet after 1 week of adaptation, before the steers were transitioned to the next stage of the diet, using terminal restriction fragment length polymorphism (T-RFLP) analysis, 16S rRNA gene libraries, and quantitative real-time PCR. The T-RFLP analysis displayed a shift in the rumen microbial population structure during the final two stages of the step-up diet. The 16S rRNA gene libraries demonstrated two distinct rumen microbial populations in hay-fed and high-grain-fed animals and detected only 24 common operational taxonomic units out of 398 and 315, respectively. The 16S rRNA gene libraries of hay-fed animals contained a significantly higher number of bacteria belonging to the phylum Fibrobacteres, whereas the 16S rRNA gene libraries of grain-fed animals contained a significantly higher number of bacteria belonging to the phylum Bacteroidetes. Real-time PCR analysis detected significant fold increases in the Megasphaera elsdenii, Streptococcus bovis, Selenomonas ruminantium, and Prevotella bryantii populations during adaptation to the high-concentrate (high-grain) diet, whereas the Butyrivibrio fibrisolvens and Fibrobacter succinogenes populations gradually decreased as the animals were adapted to the high-concentrate diet. This study evaluates the rumen microbial population using several molecular approaches and presents a broader picture of the rumen microbial population structure during adaptation to a high-grain diet from a forage diet.

Project description:Alterations in mucosal microbiota and metabolites are critical to intestinal homeostasis and host health. This study used a combination of 16S rRNA gene sequencing and liquid chromatography-mass spectrometry (LC/MS) to investigate mucosal microbiota and their metabolic profiles in the ileum of Hu sheep fed different diets. Here, we randomly allocated 15 Hu sheep to three diets, a non-pelleted low-grain diet (control diet; CON), a non-pelleted high-grain diet (HG), and a pelleted high-grain diet (HP). After 60 days of treatment, ileal mucosal samples were collected for microbiome and metabolome analysis. The results of principal coordinate analysis and permutation multivariate analysis showed that there was a tendency for microbial differentiation between the CON and HG groups (P < 0.1), although no significant difference between the HG and HP groups was observed (P > 0.05). Compared with the CON diet, the HG diet decreased (P < 0.05) the abundance of some probiotic species (e.g., Sphingomonas and Candidatus Arthromitus) and increased (P < 0.05) the abundance of acid-producing microbiota (e.g., Succiniclasticum, Nesterenkonia, and Alloprevotella) in the ileal mucosa. Compared with the HG diet, the HP diet decreased (P < 0.05) the abundance of Alloprevotella and increased (P < 0.05) the abundance of Mycoplasma in the ileal mucosa. Furthermore, partial least squares discriminant analysis and orthogonal partial least-squared discriminant analysis indicated that different dietary treatments resulted in different metabolic patterns in the ileal mucosa of the CON, HG, and HP groups. The HG diet altered (VIP > 1 and P < 0.05) the metabolic patterns of amino acids, fatty acids, and nucleotides/nucleosides (such as increased amounts of ornithine, tyrosine, cis-9-palmitoleic acid, and adenosine) compared with the CON diet. However, 10 differential metabolites (VIP > 1 and P < 0.05; including tyrosine, ornithine, and cis-9-palmitoleic acid) identified in the HG group exhibited a diametrically opposite trend in the HP group, suggesting that the HP diet could partially eliminate the changes brought upon by the HG diet. Collectively, our findings demonstrate that different diets altered the ileal mucosal microbiota and metabolites and provide new insight into the effects of high-grain diets on the intestinal health of ruminant animals.

Dataset Information

Microbiome-host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model.

Background

Results

Conclusions

Publications

Microbiome-host co-oscillation patterns in remodeling of colonic homeostasis during adaptation to a high-grain diet in a sheep model.

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