Impact of birth weight and postnatal diet on the gut microbiota of young adult guinea pigs.

Kait Al,Kristyn Dunlop,Jeremy Burton,Gregory B Gloor,Ousseynou Sarr,Gregor Reid,Timothy R.H Regnault

doi:10.7717/peerj.2840

Abstract

BackgroundThe gastrointestinal tract (GIT) microbiota is essential to metabolic health, and the prevalence of the Western diet (WD) high in fat and sugar is increasing, with evidence highlighting a negative interaction between the GIT and WD, resulting in liver dysfunction. Additionally, an adverse in utero environment such as placental insufficiency resulting in low birth weight (LBW) offspring, contributes to an increased risk of metabolic diseases such as fatty liver infiltration and liver dysfunction in later life. We sought to understand the potential interactive effects of exposure to a WD upon growing LBW offspring. We postulated that LBW offspring when challenged with a poor postnatal diet, would display an altered microbiota and more severe liver metabolic dysfunction.MethodsThe fecal microbiota of normal birth weight (NBW) and LBW young guinea pig offspring, weaned onto either a control diet (CD) or WD was determined with 16S rRNA gene next generation sequencing at young adulthood following the early rapid growth phase after weaning. A liver blood chemistry profile was also performed.ResultsThe life-long consumption of WD following weaning into young adulthood resulted in increased total cholesterol, triglycerides and alanine aminotransferase levels in association with an altered GIT microbiota when compared to offspring consuming CD. Neither birth weight nor sex were associated with any significant changes in microbiota alpha diversity, by measuring the Shannon’s diversity index. One hundred forty-eight operational taxonomic units were statistically distinct between the diet groups, independent of birth weight. In the WD group, significant decreases were detected in Barnesiella, Methanobrevibacter smithii and relatives of Oscillospira guillermondii, while Butyricimonas and Bacteroides spp. were increased.DiscussionThese results describe the GIT microbiota in a guinea pig model of LBW and WD associated metabolic syndrome and highlight several WD specific GIT alterations associated with human metabolic disease.

Highlights

Metabolic diseases such as obesity and the related metabolic syndrome are considered to be an epidemic and an increasing burden on health care systems (Mathers et al, 2001)
The gastrointestinal tract (GIT) microbiota utilizes indigestible components of our diets and some suggest it may influence calorie harvesting from food (Turnbaugh et al, 2006; Zeng et al, 2013). It has an important role in homeostasis and the maintenance of epithelial barriers, which when degraded may contribute to inflammation leading to chronic diseases characterized by metabolic dysfunction such as non-alcoholic fatty liver disease (NAFLD) and diabetes (Bäckhed et al, 2004; Dunne et al, 2014)
The model utilizes a combination of uterine artery ablation to induce low birth weight (LBW) offspring, with a postnatal diet high in total fat and sugar, and produces a non-overweight phenotype with impaired vascular function, increased visceral adiposity, and liver fibrosis with fatty infiltration of the liver, hallmarks of metabolic disease (Sarr et al, 2014; Sarr et al, 2015; Thompson et al, 2014)

Summary

Introduction

Metabolic diseases such as obesity and the related metabolic syndrome are considered to be an epidemic and an increasing burden on health care systems (Mathers et al, 2001). The consumption of a typical ‘‘Western’’ diet (WD) high in fat and sugar has been shown by some groups to alter the microbial diversity and relative abundance of two main phyla in humans and mice, Bacteroidetes and Firmicutes (Turnbaugh et al, 2009) For these reasons, the gastrointestinal microbiota is considered one of the potential environmental factors that advance the host to a metabolically diseased state (Hildebrandt et al, 2009). The gastrointestinal tract (GIT) microbiota is essential to metabolic health, and the prevalence of the Western diet (WD) high in fat and sugar is increasing, with evidence highlighting a negative interaction between the GIT and WD, resulting in liver dysfunction. These results describe the GIT microbiota in a guinea pig model of LBW and WD associated metabolic syndrome and highlight several WD specific GIT alterations associated with human metabolic disease

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