Abstract

We compared the gut microbial populations in 100 women, from rural Ghana and urban US [50% lean (BMI < 25 kg/m2) and 50% obese (BMI ≥ 30 kg/m2)] to examine the ecological co-occurrence network topology of the gut microbiota as well as the relationship of short chain fatty acids (SCFAs) with obesity. Ghanaians consumed significantly more dietary fiber, had greater microbial alpha-diversity, different beta-diversity, and had a greater concentration of total fecal SCFAs (p-value < 0.002). Lean Ghanaians had significantly greater network density, connectivity and stability than either obese Ghanaians, or lean and obese US participants (false discovery rate (FDR) corrected p-value ≤ 0.01). Bacteroides uniformis was significantly more abundant in lean women, irrespective of country (FDR corrected p < 0.001), while lean Ghanaians had a significantly greater proportion of Ruminococcus callidus, Prevotella copri, and Escherichia coli, and smaller proportions of Lachnospiraceae, Bacteroides and Parabacteroides. Lean Ghanaians had a significantly greater abundance of predicted microbial genes that catalyzed the production of butyric acid via the fermentation of pyruvate or branched amino-acids, while obese Ghanaians and US women (irrespective of BMI) had a significantly greater abundance of predicted microbial genes that encoded for enzymes associated with the fermentation of amino-acids such as alanine, aspartate, lysine and glutamate. Similar to lean Ghanaian women, mice humanized with stool from the lean Ghanaian participant had a significantly lower abundance of family Lachnospiraceae and genus Bacteroides and Parabacteroides, and were resistant to obesity following 6-weeks of high fat feeding (p-value < 0.01). Obesity-resistant mice also showed increased intestinal transcriptional expression of the free fatty acid (Ffa) receptor Ffa2, in spite of similar fecal SCFAs concentrations. We demonstrate that the association between obesity resistance and increased predicted ecological connectivity and stability of the lean Ghanaian microbiota, as well as increased local SCFA receptor level, provides evidence of the importance of robust gut ecologic network in obesity.

Highlights

  • Obesity is a complex medical condition with a multi-faceted etiology

  • While short chain fatty acids (SCFAs) have been implicated in obesity[31], we explored how fecal SCFA concentrations may be associated with obesity

  • In part 1; we describe the differences in the microbial co-occurrence network topology and fecal SCFA concentrations in lean and obese women from two distinct geographic sites, rural Ghana and urban US, with significant differences in their intake of dietary fiber, and obesity prevalence[39]

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Summary

Introduction

Obesity is a complex medical condition with a multi-faceted etiology. Though diet, lifestyle and genetic factors are thought to play a role in the onset of such disorders, increasing evidence points to a pivotal role for the gut microbiota[1,2]. Differences in geographic location, and possibly differences in diet and lifestyle, may be useful for describing the majority of the variance in microbial community composition and structure[13,18,19,20] This is of particular importance, given that the obesity epidemic is emerging globally at different rates[21,22], it is essential that we disentangle the geographic differences in microbiota to determine the elements most influential for obesity. The gut microbiota can influence the host by changing the energy harvest potential of food, in part through the fermentation of non-digestible fibers, such as pectin, cellulose, and resistant starches[30] Microbial fermentation of these fibers leads to the production of short chain fatty acids (SCFAs), mainly butyric, propionic and acetic acid[31]. In part 2, we tested our hypothesis that the ecological co-occurrence network topology of the fecal microbiota associates with obesity in mice in a prospective fecal microbiome transplant (FMT) study, and challenged with a high fat diet for 6 weeks

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