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Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations.

ABSTRACT: BACKGROUND: Dietary fibers contribute to health and physiology primarily via the fermentative actions of the host's gut microbiome. Physicochemical properties such as solubility, fermentability, viscosity, and gel-forming ability differ among fiber types and are known to affect metabolism. However, few studies have focused on how they influence the gut microbiome and how these interactions influence host health. The aim of this study is to investigate how the gut microbiome of growing pigs responds to diets containing gel-forming alginate and fermentable resistant starch and to predict important interactions and functional changes within the microbiota. RESULTS: Nine growing pigs (3-month-old), divided into three groups, were fed with either a control, alginate-, or resistant starch-containing diet (CON, ALG, or RS), and fecal samples were collected over a 12-week period. SSU (small subunit) rDNA amplicon sequencing data was annotated to assess the gut microbiome, whereas comprehensive microarray polymer profiling (CoMPP) of digested material was employed to evaluate feed degradation. Gut microbiome structure variation was greatest in pigs fed with resistant starch, where notable changes included the decrease in alpha diversity and increase in relative abundance of Lachnospiraceae- and Ruminococcus-affiliated phylotypes. Imputed function was predicted to vary significantly in pigs fed with resistant starch and to a much lesser extent with alginate; however, the key pathways involving degradation of starch and other plant polysaccharides were predicted to be unaffected. The change in relative abundance levels of basal dietary components (plant cell wall polysaccharides and proteins) over time was also consistent irrespective of diet; however, correlations between the dietary components and phylotypes varied considerably in the different diets. CONCLUSIONS: Resistant starch-containing diet exhibited the strongest structural variation compared to the alginate-containing diet. This variation gave rise to a microbiome that contains phylotypes affiliated with metabolically reputable taxonomic lineages. Despite the significant microbiome structural shifts that occurred from resistant starch-containing diet, functional redundancy is seemingly apparent with respect to the microbiome's capacity to degrade starch and other dietary polysaccharides, one of the key stages in digestion.

SUBMITTER: Umu OC

PROVIDER: S-EPMC4405844 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations.

Umu Özgün C O ÖC Frank Jeremy A JA Fangel Jonatan U JU Oostindjer Marije M da Silva Carol Souza CS Bolhuis Elizabeth J EJ Bosch Guido G Willats William G T WG Pope Phillip B PB Diep Dzung B DB

Microbiome 20150416

<h4>Background</h4>Dietary fibers contribute to health and physiology primarily via the fermentative actions of the host's gut microbiome. Physicochemical properties such as solubility, fermentability, viscosity, and gel-forming ability differ among fiber types and are known to affect metabolism. However, few studies have focused on how they influence the gut microbiome and how these interactions influence host health. The aim of this study is to investigate how the gut microbiome of growing pig ...[more]

PMID: 25905018

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Project description:Diet can influence the composition of the human microbiome, and yet relatively few dietary ingredients have been systematically investigated with respect to their impact on the functional potential of the microbiome. Dietary resistant starch (RS) has been shown to have health benefits, but we lack a mechanistic understanding of the metabolic processes that occur in the gut during digestion of RS. Here, we collected samples during a dietary crossover study with diets containing large or small amounts of RS. We determined the impact of RS on the gut microbiome and metabolic pathways in the gut, using a combination of "omics" approaches, including 16S rRNA gene sequencing, metaproteomics, and metabolomics. This multiomics approach captured changes in the abundance of specific bacterial species, proteins, and metabolites after a diet high in resistant starch (HRS), providing key insights into the influence of dietary interventions on the gut microbiome. The combined data showed that a high-RS diet caused an increase in the ratio of Firmicutes to Bacteroidetes, including increases in relative abundances of some specific members of the Firmicutes and concurrent increases in enzymatic pathways and metabolites involved in lipid metabolism in the gut.IMPORTANCE This work was undertaken to obtain a mechanistic understanding of the complex interplay between diet and the microorganisms residing in the intestine. Although it is known that gut microbes play a key role in digestion of the food that we consume, the specific contributions of different microorganisms are not well understood. In addition, the metabolic pathways and resultant products of metabolism during digestion are highly complex. To address these knowledge gaps, we used a combination of molecular approaches to determine the identities of the microorganisms in the gut during digestion of dietary starch as well as the metabolic pathways that they carry out. Together, these data provide a more complete picture of the function of the gut microbiome in digestion, including links between an RS diet and lipid metabolism and novel linkages between specific gut microbes and their metabolites and proteins produced in the gut.

Project description:Carbadox is a quinoxaline-di-N-oxide antibiotic fed to over 40% of young pigs in the United States that has been shown to induce phage DNA transduction in vitro; however, the effects of carbadox on swine microbiome functions are poorly understood. We investigated the in vivo longitudinal effects of carbadox on swine gut microbial gene expression (fecal metatranscriptome) and phage population dynamics (fecal dsDNA viromes). Microbial metagenome, transcriptome, and virome sequences were annotated for taxonomic inference and gene function by using FIGfam (isofunctional homolog sequences) and SEED subsystems databases. When the beta diversities of microbial FIGfam annotations were compared, the control and carbadox communities were distinct 2 days after carbadox introduction. This effect was driven by carbadox-associated lower expression of FIGfams (n = 66) related to microbial respiration, carbohydrate utilization, and RNA metabolism (q < 0.1), suggesting bacteriostatic or bactericidal effects within certain populations. Interestingly, carbadox treatment caused greater expression of FIGfams related to all stages of the phage lytic cycle 2 days following the introduction of carbadox (q ?0.07), suggesting the carbadox-mediated induction of prophages and phage DNA recombination. These effects were diminished by 7 days of continuous carbadox in the feed, suggesting an acute impact. Additionally, the viromes included a few genes that encoded resistance to tetracycline, aminoglycoside, and beta-lactam antibiotics but these did not change in frequency over time or with treatment. The results show decreased bacterial growth and metabolism, prophage induction, and potential transduction of bacterial fitness genes in swine gut bacterial communities as a result of carbadox administration.IMPORTANCE FDA regulations on agricultural antibiotic use have focused on antibiotics that are important for human medicine. Carbadox is an antibiotic not used in humans but frequently used on U.S. pig farms. It is important to study possible side effects of carbadox use because it has been shown to promote bacterial evolution, which could indirectly impact antibiotic resistance in bacteria of clinical importance. Interestingly, the present study shows greater prophage gene expression in feces from carbadox-fed animals than in feces from nonmedicated animals 2 days after the initiation of in-feed carbadox treatment. Importantly, the phage genetic material isolated in this study contained genes that could provide resistance to antibiotics that are important in human medicine, indicating that human-relevant antibiotic resistance genes are mobile between bacteria via phages. This study highlights the collateral effects of antibiotics and demonstrates the need to consider diverse antibiotic effects whenever antibiotics are being used or new regulations are considered.

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Dataset Information

Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations.

Publications

Resistant starch diet induces change in the swine microbiome and a predominance of beneficial bacterial populations.

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