Abstract

Bacteroides is among the most abundant microorganism inhabiting the human intestine. They are saccharolytic bacteria able to use dietary or host-derived glycans as energy sources. Some Bacteroides fragilis strains contribute to the maturation of the immune system but it is also an opportunistic pathogen. The intestine is the habitat of most Bifidobacterium species, some of whose strains are considered probiotics. Bifidobacteria can synthesize exopolysaccharides (EPSs), which are complex carbohydrates that may be available in the intestinal environment. We studied the metabolism of B. fragilis when an EPS preparation from bifidobacteria was added to the growth medium compared to its behavior with added glucose. 2D-DIGE coupled with the identification by MALDI-TOF/TOF evidenced proteins that were differentially produced when EPS was added. The results were supported by RT-qPCR gene expression analysis. The intracellular and extracellular pattern of certain amino acids, the redox balance and the α-glucosidase activity were differently affected in EPS with respect to glucose. These results allowed us to hypothesize that three general main events, namely the activation of amino acids catabolism, enhancement of the transketolase reaction from the pentose-phosphate cycle, and activation of the succinate-propionate pathway, promote a shift of bacterial metabolism rendering more reducing power and optimizing the energetic yield in the form of ATP when Bacteroides grow with added EPSs. Our results expand the knowledge about the capacity of B. fragilis for adapting to complex carbohydrates and amino acids present in the intestinal environment.

Highlights

  • The microbes in our body reach levels of up to 100 trillion (1012) cells, the majority of which reside in the colon and are anaerobes (Qin et al, 2010)

  • The pH-free liquid batch cultures of B. fragilis were performed in 50 mL of a non-defined peptone and yeast-extract containing basal medium (BM) previously used by us in human fecal cultures (Salazar et al, 2008) and which was subsequently adapted for Bacteroides co-cultivation with bifidobacteria (Rios-Covian et al, 2013)

  • Under the culture conditions used in the present study, B. fragilis was able to grow in the presence of glucose and bifidobacterial EPS, the pH decrease in the culture medium being more pronounced with glucose than with the bacterial polymers

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Summary

Introduction

The microbes in our body reach levels of up to 100 trillion (1012) cells, the majority of which reside in the colon and are anaerobes (Qin et al, 2010). The adult human distal gut microbiota is dominated by two phyla, the Firmicutes and the Bacteroidetes, the genus Bacteroides accounting for 20–50% in most individuals (Rigottier-Gois et al, 2003; Mahowald et al, 2009) This group of microorganisms appears during the first few days of life in the intestine of full-term neonates. Acetic, lactic, and propionic acids are produced by Bacteroides in variable proportions during fermentation (RiosCovian et al, 2013) These organic acids and short chain fatty acids (SCFAs) can be utilized by other intestinal microorganisms through cross-feeding mechanisms (Scott et al, 2008) or be partly reabsorbed through the large intestine, serving as an energy source for the host (Hooper et al, 2002)

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