Literature DB >> 30171006

Cross-Feeding among Probiotic Bacterial Strains on Prebiotic Inulin Involves the Extracellular exo-Inulinase of Lactobacillus paracasei Strain W20.

Markus C L Boger1, Alicia Lammerts van Bueren1, Lubbert Dijkhuizen2.   

Abstract

Probiotic gut bacteria employ specific metabolic pathways to degrade dietary carbohydrates beyond the capabilities of their human host. Here, we report how individual commercial probiotic strains degrade prebiotic (inulin type) fructans. First, a structural analysis of commercial fructose oligosaccharide-inulin samples was performed. These β-(2-1)-fructans differ in termination by either glucose (GF) or fructose (FF) residues, with a broad variation in the degrees of polymerization (DPs). The growth of individual probiotic bacteria on short-chain inulin (sc-inulin) (Frutafit CLR), a β-(2-1)-fructan (DP 2 to DP 40), was studied. Lactobacillus salivarius W57 and other bacteria grew relatively poorly on sc-inulin, with only fractions of DP 3 and DP 5 utilized, reflecting uptake via specific transport systems followed by intracellular metabolism. Lactobacillus paracasei subsp. paracasei W20 completely used all sc-inulin components, employing an extracellular exo-inulinase enzyme (glycoside hydrolase family GH32 [LpGH32], also found in other strains of this species); the purified enzyme converted high-DP compounds into fructose, sucrose, 1-kestose, and F2 (inulobiose). The cocultivation of L. salivarius W57 and L. paracasei W20 on sc-inulin resulted in cross-feeding of the former by the latter, supported by this extracellular exo-inulinase. The extent of cross-feeding depended on the type of fructan, i.e., the GF type (clearly stimulating) versus the FF type (relatively low stimulus), and on fructan chain length, since relatively low-DP β-(2-1)-fructans contain a relatively high content of GF-type molecules, thus resulting in higher concentrations of GF-type DP 2 to DP 3 degradation products. The results provide an example of how in vivo cross-feeding on prebiotic β-(2-1)-fructans may occur among probiotic lactobacilli.IMPORTANCE The human gut microbial community is associated strongly with host physiology and human diseases. This observation has prompted research on pre- and probiotics, two concepts enabling specific changes in the composition of the human gut microbiome that result in beneficial effects for the host. Here, we show how fructooligosaccharide-inulin prebiotics are fermented by commercial probiotic bacterial strains involving specific sets of enzymes and transporters. Cross-feeding strains such as Lactobacillus paracasei W20 may thus act as keystone strains in the degradation of prebiotic inulin in the human gut, and this strain-exo-inulinase combination may be used in commercial Lactobacillus-inulin synbiotics.
Copyright © 2018 American Society for Microbiology.

Entities:  

Keywords:  Lactobacillus paracasei; cross-feeding; exo-inulinase; inulin; probiotics

Mesh:

Substances:

Year:  2018        PMID: 30171006      PMCID: PMC6193377          DOI: 10.1128/AEM.01539-18

Source DB:  PubMed          Journal:  Appl Environ Microbiol        ISSN: 0099-2240            Impact factor:   4.792


  36 in total

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Journal:  Biochim Biophys Acta       Date:  1999-07-06

2.  Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic.

Authors:  Colin Hill; Francisco Guarner; Gregor Reid; Glenn R Gibson; Daniel J Merenstein; Bruno Pot; Lorenzo Morelli; Roberto Berni Canani; Harry J Flint; Seppo Salminen; Philip C Calder; Mary Ellen Sanders
Journal:  Nat Rev Gastroenterol Hepatol       Date:  2014-06-10       Impact factor: 46.802

3.  Screening for and identification of starch-, amylopectin-, and pullulan-degrading activities in bifidobacterial strains.

Authors:  Sinéad M Ryan; Gerald F Fitzgerald; Douwe van Sinderen
Journal:  Appl Environ Microbiol       Date:  2006-08       Impact factor: 4.792

4.  Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose.

Authors:  Gwen Falony; Angeliki Vlachou; Kristof Verbrugghe; Luc De Vuyst
Journal:  Appl Environ Microbiol       Date:  2006-10-20       Impact factor: 4.792

5.  Sugar transport systems of Bifidobacterium longum NCC2705.

Authors:  Stephan Parche; Johannes Amon; Ivana Jankovic; Enea Rezzonico; Manfred Beleut; Hande Barutçu; Inke Schendel; Mike P Eddy; Andreas Burkovski; Fabrizio Arigoni; Fritz Titgemeyer
Journal:  J Mol Microbiol Biotechnol       Date:  2007

6.  Lactobacillus paracasei subsp. paracasei 8700:2 degrades inulin-type fructans exhibiting different degrees of polymerization.

Authors:  Lefteris Makras; Gerald Van Acker; Luc De Vuyst
Journal:  Appl Environ Microbiol       Date:  2005-11       Impact factor: 4.792

7.  Selective carbohydrate utilization by lactobacilli and bifidobacteria.

Authors:  D Watson; M O'Connell Motherway; M H C Schoterman; R J Joost van Neerven; A Nauta; D van Sinderen
Journal:  J Appl Microbiol       Date:  2013-01-11       Impact factor: 3.772

8.  Functional analysis of the fructooligosaccharide utilization operon in Lactobacillus paracasei 1195.

Authors:  Yong Jun Goh; Jong-Hwa Lee; Robert W Hutkins
Journal:  Appl Environ Microbiol       Date:  2007-07-20       Impact factor: 4.792

Review 9.  Some are more equal than others: the role of "keystone" species in the degradation of recalcitrant substrates.

Authors:  Xiaolei Ze; Fanny Le Mougen; Sylvia H Duncan; Petra Louis; Harry J Flint
Journal:  Gut Microbes       Date:  2013-04-02

10.  dbCAN: a web resource for automated carbohydrate-active enzyme annotation.

Authors:  Yanbin Yin; Xizeng Mao; Jincai Yang; Xin Chen; Fenglou Mao; Ying Xu
Journal:  Nucleic Acids Res       Date:  2012-05-29       Impact factor: 16.971

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  15 in total

1.  Enzymatic and structural characterization of β-fructofuranosidase from the honeybee gut bacterium Frischella perrara.

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Journal:  Appl Microbiol Biotechnol       Date:  2022-03-10       Impact factor: 4.813

2.  Inulin Fermentation by Lactobacilli and Bifidobacteria from Dairy Calves.

Authors:  Yuanting Zhu; Jinxin Liu; Julian M Lopez; David A Mills
Journal:  Appl Environ Microbiol       Date:  2020-12-17       Impact factor: 4.792

3.  Gene-Phenotype Associations Involving Human-Residential Bifidobacteria (HRB) Reveal Significant Species- and Strain-Specificity in Carbohydrate Catabolism.

Authors:  Shijie Liu; Zhifeng Fang; Hongchao Wang; Qixiao Zhai; Feng Hang; Jianxin Zhao; Hao Zhang; Wenwei Lu; Wei Chen
Journal:  Microorganisms       Date:  2021-04-21

4.  Fermentation of Chicory Fructo-Oligosaccharides and Native Inulin by Infant Fecal Microbiota Attenuates Pro-Inflammatory Responses in Immature Dendritic Cells in an Infant-Age-Dependent and Fructan-Specific Way.

Authors:  Madelon J Logtenberg; Renate Akkerman; Ran An; Gerben D A Hermes; Bart J de Haan; Marijke M Faas; Erwin G Zoetendal; Henk A Schols; Paul de Vos
Journal:  Mol Nutr Food Res       Date:  2020-06-02       Impact factor: 5.914

5.  Harvesting of Prebiotic Fructooligosaccharides by Nonbeneficial Human Gut Bacteria.

Authors:  Zhi Wang; Alexandra S Tauzin; Elisabeth Laville; Pietro Tedesco; Fabien Létisse; Nicolas Terrapon; Pascale Lepercq; Myriam Mercade; Gabrielle Potocki-Veronese
Journal:  mSphere       Date:  2020-01-08       Impact factor: 4.389

6.  Structural Identity of Galactooligosaccharide Molecules Selectively Utilized by Single Cultures of Probiotic Bacterial Strains.

Authors:  Markus Böger; Sander S van Leeuwen; Alicia Lammerts van Bueren; Lubbert Dijkhuizen
Journal:  J Agric Food Chem       Date:  2019-12-05       Impact factor: 5.279

Review 7.  Diet-microbiome-disease: Investigating diet's influence on infectious disease resistance through alteration of the gut microbiome.

Authors:  Erica V Harris; Jacobus C de Roode; Nicole M Gerardo
Journal:  PLoS Pathog       Date:  2019-10-31       Impact factor: 6.823

8.  Fitness and Productivity Increase with Ecotypic Diversity among Escherichia coli Strains That Coevolved in a Simple, Constant Environment.

Authors:  Dong-Dong Yang; Ashley Alexander; Margie Kinnersley; Emily Cook; Amy Caudy; Adam Rosebrock; Frank Rosenzweig
Journal:  Appl Environ Microbiol       Date:  2020-04-01       Impact factor: 4.792

9.  Genotyping and plant-derived glycan utilization analysis of Bifidobacterium strains from mother-infant pairs.

Authors:  Zeyu Kan; Baolong Luo; Jingjing Cai; Yan Zhang; Fengwei Tian; Yongqing Ni
Journal:  BMC Microbiol       Date:  2020-09-10       Impact factor: 3.605

10.  Extraction and characterisation of arabinoxylan from brewers spent grain and investigation of microbiome modulation potential.

Authors:  Kieran M Lynch; Conall R Strain; Crystal Johnson; Dhrati Patangia; Catherine Stanton; Fatma Koc; Jorge Gil-Martinez; Patrick O'Riordan; Aylin W Sahin; R Paul Ross; Elke K Arendt
Journal:  Eur J Nutr       Date:  2021-05-31       Impact factor: 5.614

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