Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids

Bacteroides thetaiotaomicron is commonly found in the human colon and stabilizes its ecosystem by the 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...

Full description

Bibliographic Details
Main Authors: Signe eAdamberg, Katrin eTomson, Heiki eVija, Marju ePuurand, Natalja eKabanova, Triinu eVisnapuu, Eerik eJõgi, Tiina eAlamäe, Kaarel eAdamberg
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-12-01
Series:Frontiers in Nutrition
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnut.2014.00021/full
_version_ 1818110751381913600
author Signe eAdamberg
Katrin eTomson
Heiki eVija
Marju ePuurand
Natalja eKabanova
Triinu eVisnapuu
Eerik eJõgi
Tiina eAlamäe
Kaarel eAdamberg
Kaarel eAdamberg
Kaarel eAdamberg
author_facet Signe eAdamberg
Katrin eTomson
Heiki eVija
Marju ePuurand
Natalja eKabanova
Triinu eVisnapuu
Eerik eJõgi
Tiina eAlamäe
Kaarel eAdamberg
Kaarel eAdamberg
Kaarel eAdamberg
author_sort Signe eAdamberg
collection DOAJ
description Bacteroides thetaiotaomicron is commonly found in the human colon and stabilizes its ecosystem by the 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 (DP > 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.
first_indexed 2024-12-11T02:52:07Z
format Article
id doaj.art-0ba12baa1a094c0ea85f1189db91302e
institution Directory Open Access Journal
issn 2296-861X
language English
last_indexed 2024-12-11T02:52:07Z
publishDate 2014-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Nutrition
spelling doaj.art-0ba12baa1a094c0ea85f1189db91302e2022-12-22T01:23:16ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2014-12-01110.3389/fnut.2014.00021119326Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acidsSigne eAdamberg0Katrin eTomson1Heiki eVija2Marju ePuurand3Natalja eKabanova4Triinu eVisnapuu5Eerik eJõgi6Tiina eAlamäe7Kaarel eAdamberg8Kaarel eAdamberg9Kaarel eAdamberg10Tallinn University of TechnologyCompetence Center of Food and Fermentation TechnologiesNational Institute of Chemical Physics and BiophysicsTallinn University of TechnologyCompetence Center of Food and Fermentation TechnologiesUniversity of TartuUniversity of TartuUniversity of TartuTallinn University of TechnologyCompetence Center of Food and Fermentation TechnologiesTallinn University of TechnologyBacteroides thetaiotaomicron is commonly found in the human colon and stabilizes its ecosystem by the 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 (DP > 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.http://journal.frontiersin.org/Journal/10.3389/fnut.2014.00021/fullamino acid metabolismMetabolic Flux AnalysisFosfructandefined mediumBacteroides thetaiotaomicron
spellingShingle Signe eAdamberg
Katrin eTomson
Heiki eVija
Marju ePuurand
Natalja eKabanova
Triinu eVisnapuu
Eerik eJõgi
Tiina eAlamäe
Kaarel eAdamberg
Kaarel eAdamberg
Kaarel eAdamberg
Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids
Frontiers in Nutrition
amino acid metabolism
Metabolic Flux Analysis
Fos
fructan
defined medium
Bacteroides thetaiotaomicron
title Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids
title_full Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids
title_fullStr Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids
title_full_unstemmed Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids
title_short Degradation of fructans and production of propionic acid by Bacteroides thetaiotaomicron are enhanced by shortage of amino acids
title_sort degradation of fructans and production of propionic acid by bacteroides thetaiotaomicron are enhanced by shortage of amino acids
topic amino acid metabolism
Metabolic Flux Analysis
Fos
fructan
defined medium
Bacteroides thetaiotaomicron
url http://journal.frontiersin.org/Journal/10.3389/fnut.2014.00021/full
work_keys_str_mv AT signeeadamberg degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT katrinetomson degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT heikievija degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT marjuepuurand degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT nataljaekabanova degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT triinuevisnapuu degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT eerikejogi degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT tiinaealamae degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT kaareleadamberg degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT kaareleadamberg degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids
AT kaareleadamberg degradationoffructansandproductionofpropionicacidbybacteroidesthetaiotaomicronareenhancedbyshortageofaminoacids