Genotypic adaptations associated with prolonged persistence of Lactobacillus plantarum in the murine digestive tract

Hermien van Bokhorst-van de Veen, Maaike J. Smelt, Michiel Wels, Sacha A.F.T. van Hijum, Paul de Vos, Michiel Kleerebezem, Peter A. Bron

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Probiotic bacteria harbor effector molecules that confer health benefits, but also adaptation factors that enable them to persist in the gastrointestinal tract of the consumer. To study these adaptation factors, an antibiotic-resistant derivative of the probiotic model organism Lactobacillus plantarum WCFS1 was repeatedly exposed to the mouse digestive tract by three consecutive rounds of (re)feeding of the longest persisting colonies. This exposure to the murine intestine allowed the isolation of intestine-adapted derivatives of the original strain that displayed prolonged digestive tract residence time. Re-sequencing of the genomes of these adapted derivatives revealed single nucleotide polymorphisms as well as a single nucleotide insertion in comparison with the genome of the original WCFS1 strain. Detailed in silico analysis of the identified genomic modifications pinpointed that alterations in the coding regions of genes encoding cell envelope associated functions and energy metabolism appeared to be beneficial for the gastrointestinal tract survival of L. plantarum WCFS1. This work demonstrates the feasibility of experimental evolution for the enhancement of the gastrointestinal residence time of probiotic strains, while full-genome resequencing of the adapted isolates provided clues towards the bacterial functions involved. Enhanced gastrointestinal residence is industrially relevant because it enhances the efficacy of the delivery of viable probiotics in situ.

Original languageEnglish
Pages (from-to)895-904
JournalPlant biotechnology journal
Volume8
Issue number8
DOIs
Publication statusPublished - Aug 2013

Fingerprint

Lactobacillus plantarum
Probiotics
digestive tract
probiotics
Gastrointestinal Tract
mice
Genome
gastrointestinal system
Intestines
genome
intestines
refeeding
Insurance Benefits
Computer Simulation
energy metabolism
Energy Metabolism
single nucleotide polymorphism
Single Nucleotide Polymorphism
Nucleotides
nucleotides

Keywords

  • adaptation, biological/genetics
  • animals
  • bacterial proteins/genetics
  • evolution, molecular
  • gastrointestinal tract/microbiology
  • genome, bacterial
  • genotype
  • lactobacillus plantarum/genetics
  • male
  • mice
  • microbiotics
  • polymorphism, single nucleotide
  • probiotics

Cite this

van Bokhorst-van de Veen, H., Smelt, M. J., Wels, M., van Hijum, S. A. F. T., de Vos, P., Kleerebezem, M., & Bron, P. A. (2013). Genotypic adaptations associated with prolonged persistence of Lactobacillus plantarum in the murine digestive tract. Plant biotechnology journal, 8(8), 895-904. https://doi.org/10.1002/biot.201200259
van Bokhorst-van de Veen, Hermien ; Smelt, Maaike J. ; Wels, Michiel ; van Hijum, Sacha A.F.T. ; de Vos, Paul ; Kleerebezem, Michiel ; Bron, Peter A. / Genotypic adaptations associated with prolonged persistence of Lactobacillus plantarum in the murine digestive tract. In: Plant biotechnology journal. 2013 ; Vol. 8, No. 8. pp. 895-904.
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abstract = "Probiotic bacteria harbor effector molecules that confer health benefits, but also adaptation factors that enable them to persist in the gastrointestinal tract of the consumer. To study these adaptation factors, an antibiotic-resistant derivative of the probiotic model organism Lactobacillus plantarum WCFS1 was repeatedly exposed to the mouse digestive tract by three consecutive rounds of (re)feeding of the longest persisting colonies. This exposure to the murine intestine allowed the isolation of intestine-adapted derivatives of the original strain that displayed prolonged digestive tract residence time. Re-sequencing of the genomes of these adapted derivatives revealed single nucleotide polymorphisms as well as a single nucleotide insertion in comparison with the genome of the original WCFS1 strain. Detailed in silico analysis of the identified genomic modifications pinpointed that alterations in the coding regions of genes encoding cell envelope associated functions and energy metabolism appeared to be beneficial for the gastrointestinal tract survival of L. plantarum WCFS1. This work demonstrates the feasibility of experimental evolution for the enhancement of the gastrointestinal residence time of probiotic strains, while full-genome resequencing of the adapted isolates provided clues towards the bacterial functions involved. Enhanced gastrointestinal residence is industrially relevant because it enhances the efficacy of the delivery of viable probiotics in situ.",
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van Bokhorst-van de Veen, H, Smelt, MJ, Wels, M, van Hijum, SAFT, de Vos, P, Kleerebezem, M & Bron, PA 2013, 'Genotypic adaptations associated with prolonged persistence of Lactobacillus plantarum in the murine digestive tract', Plant biotechnology journal, vol. 8, no. 8, pp. 895-904. https://doi.org/10.1002/biot.201200259

Genotypic adaptations associated with prolonged persistence of Lactobacillus plantarum in the murine digestive tract. / van Bokhorst-van de Veen, Hermien; Smelt, Maaike J.; Wels, Michiel; van Hijum, Sacha A.F.T.; de Vos, Paul; Kleerebezem, Michiel; Bron, Peter A.

In: Plant biotechnology journal, Vol. 8, No. 8, 08.2013, p. 895-904.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Genotypic adaptations associated with prolonged persistence of Lactobacillus plantarum in the murine digestive tract

AU - van Bokhorst-van de Veen, Hermien

AU - Smelt, Maaike J.

AU - Wels, Michiel

AU - van Hijum, Sacha A.F.T.

AU - de Vos, Paul

AU - Kleerebezem, Michiel

AU - Bron, Peter A.

PY - 2013/8

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AB - Probiotic bacteria harbor effector molecules that confer health benefits, but also adaptation factors that enable them to persist in the gastrointestinal tract of the consumer. To study these adaptation factors, an antibiotic-resistant derivative of the probiotic model organism Lactobacillus plantarum WCFS1 was repeatedly exposed to the mouse digestive tract by three consecutive rounds of (re)feeding of the longest persisting colonies. This exposure to the murine intestine allowed the isolation of intestine-adapted derivatives of the original strain that displayed prolonged digestive tract residence time. Re-sequencing of the genomes of these adapted derivatives revealed single nucleotide polymorphisms as well as a single nucleotide insertion in comparison with the genome of the original WCFS1 strain. Detailed in silico analysis of the identified genomic modifications pinpointed that alterations in the coding regions of genes encoding cell envelope associated functions and energy metabolism appeared to be beneficial for the gastrointestinal tract survival of L. plantarum WCFS1. This work demonstrates the feasibility of experimental evolution for the enhancement of the gastrointestinal residence time of probiotic strains, while full-genome resequencing of the adapted isolates provided clues towards the bacterial functions involved. Enhanced gastrointestinal residence is industrially relevant because it enhances the efficacy of the delivery of viable probiotics in situ.

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KW - animals

KW - bacterial proteins/genetics

KW - evolution, molecular

KW - gastrointestinal tract/microbiology

KW - genome, bacterial

KW - genotype

KW - lactobacillus plantarum/genetics

KW - male

KW - mice

KW - microbiotics

KW - polymorphism, single nucleotide

KW - probiotics

KW - biotechnologie

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DO - 10.1002/biot.201200259

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JO - Plant biotechnology journal

JF - Plant biotechnology journal

SN - 1467-7644

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ER -