Abstract

Bacteroides thetaiotaomicron is commonly found in the human colon and stabilizes its ecosystem by catabolism of various polysaccharides. A model of cross-talk between the metabolism of amino acids and fructans in B. thetaiotaomicron was proposed. The growth of B. thetaiotaomicron DSM 2079 in two defined media containing mineral salts and vitamins, and supplemented with either 20 or 2 amino acids, was studied in an isothermal microcalorimeter. The polyfructans inulin (from chicory) and levan (synthesized using levansucrase from Pseudomonas syringae), two fructooligosaccharide preparations with different composition, sucrose and fructose were tested as substrates. The calorimetric power-time curves were substrate specific and typically multiauxic. A surplus of amino acids reduced the consumption of longer oligosaccharides (degree of polymerization > 3). Bacterial growth was not detected either in the carbohydrate free medium containing amino acids or in the medium with inulin as a sole carbohydrate. In amino acid-restricted medium, fermentation leading to acetic acid formation was dominant at the beginning of growth (up to 24 h), followed by increased lactic acid production, and mainly propionic and succinic acids were produced at the end of fermentation. In the medium supplemented with 20 amino acids, the highest production of d-lactate (82 ± 33 mmol/gDW) occurred in parallel with extensive consumption (up to 17 mmol/gDW) of amino acids, especially Ser, Thr, and Asp. The production of Ala and Glu was observed at growth on all substrates, and the production was enhanced under amino acid deficiency. The study revealed the influence of amino acids on fructan metabolism in B. thetaiotaomicron and showed that defined growth media are invaluable in elucidating quantitative metabolic profiles of the bacteria. Levan was shown to act as an easily degradable substrate for B. thetaiotaomicron. The effect of levan on balancing or modifying colon microbiota will be studied in further experiments.

Highlights

  • In last decades, the genetic composition and species diversity of the gastrointestinal tract ecosystem have been studied intensively, but the dynamics of the microbiota at the metabolic level are still insufficiently understood

  • The growth of the common gut bacterium B. thetaiotaomicron on these substrates was addressed with a focus on the effect of an amino acid supply (20 vs. 2 amino acids) on fructan metabolism

  • The most important growth differences described here are apparently related to the different amino acid composition of the two media, variations in vitamin and mineral contents may influence the growth and metabolism of B. thetaiotaomicron to some extent [19]

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Summary

Introduction

The genetic composition and species diversity of the gastrointestinal tract ecosystem have been studied intensively, but the dynamics of the microbiota at the metabolic level are still insufficiently understood. The colon microbiota members, Bacteroides bacteria, are highly efficient degraders of complex polysaccharides, including mucins and dietary fibers [3]. Dietary fiber compounds are resistant to human digestive enzymes and reach the colon virtually unmodified [4]. The content and composition of polysaccharides in the diet shape the colon microbiota and certain types of food fibers can be used as prebiotics to support the host’s health [5, 6]. A β 2,1 linked fructan [degree of polymerization (DP) 2– 60], and inulin-derived fructooligosaccharides (FOSinu, DP < 10) are abundant and the best studied dietary fibers (prebiotic compounds). The prebiotic effects of levan (a β 2,6 linked fructan) and levan-type oligosaccharides (FOSlev) have been much less studied. Levan and respective FOS are produced by extracellular enzymes of several bacteria, e.g., bacilli, www.frontiersin.org

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