Bacteroides thetaiotaomicron Starch Utilization Promotes Quercetin Degradation and Butyrate Production by Eubacterium ramulus.

Gina Paola Rodriguez-Castaño,Federico E Rey,Xingbo Liu,Alejandro Acosta-Gonzalez,Matthew R Dorris,Bradley W Bolling

doi:10.3389/fmicb.2019.01145

Gina Paola Rodriguez-Castaño, Federico E Rey + Show 4 more

Open Access

https://doi.org/10.3389/fmicb.2019.01145

Copy DOI

Abstract

Consumption of flavonoids has been associated with protection against cardiovascular and neurodegenerative diseases. Most dietary flavonoids are subjected to bacterial transformations in the gut where they are converted into biologically active metabolites that are more bioavailable and have distinct effects relative to the parent compounds. While some of the pathways involved in the breakdown of flavonoids are emerging, little it is known about the impact of carbon source availability and community dynamics on flavonoid metabolism. This is relevant in the gut where there is a fierce competition for nutrients. In this study, we show that metabolism of one of the most commonly consumed flavonoids, quercetin, by the gut-associated bacterium Eubacterium ramulus is dependent on interspecies cross-feeding interactions when starch is the only energy source available. E. ramulus can degrade quercetin in the presence of glucose but is unable to use starch for growth or quercetin degradation. However, the starch-metabolizing bacterium Bacteroides thetaiotaomicron, which does not metabolize quercetin, stimulates degradation of quercetin and butyrate production by E. ramulus via cross-feeding of glucose and maltose molecules released from starch. These results suggest that dietary substrates and interactions between species modulate the degradation of flavonoids and production of butyrate, thus shaping their bioavailability and bioactivity, and likely impacting their health-promoting effects in humans.

Highlights

Flavonoids are phenolic compounds produced by the secondary metabolism of plants
We found that B. thetaiotaomicron liberates glucose and maltose from starch at levels that support the growth of E. ramulus and degradation of quercetin by this bacterium
Glucose and starch were evaluated for their capacity to promote quercetin degradation by E. ramulus

Summary

INTRODUCTION

Flavonoids are phenolic compounds produced by the secondary metabolism of plants. They are present in fruits, grains, and vegetables. Most polyphenols are poorly absorbed in the upper gastrointestinal tract (stomach, duodenum, jejunum, and ileum) and reach the colon where they are metabolized by the gut microbiota into more readily absorbable phenolic acids, increasing bioavailability of these biologically active compounds (Hollman et al, 1999; Manach et al, 2005). In vitro studies indicate that E. ramulus requires glucose for the co-metabolization of quercetin (Schneider and Blaut, 2000) Degradation of this flavonoid results in the production of 3,4-dihydroxyphenylacetic acid (DOPAC), which has antiproliferative activity in colon cancer cells (Schneider and Blaut, 2000; Schneider et al, 2000; Gao et al, 2006). Dietary compounds that can impact microbial flavonoid metabolism in the colon are those that resist digestion in the upper gastrointestinal tract. Our results illustrate how crossfeeding between bacterial taxa can impact the metabolic fate of flavonoids in the gut

MATERIALS AND METHODS

RESULTS

DISCUSSION