Characterization of the ecological role of genes mediating acid resistance in Lactobacillus reuteri during colonization of the gastrointestinal tract

Janina A. Krumbeck, Nathan L. Marsteller, Steven A. Frese, Daniel A. Peterson, Amanda E. Ramer-Tait, Robert W. Hutkins, Jens Walter

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Rodent-derived strains of Lactobacillus reuteri densely colonize the forestomach of mice and possess several genes whose predicted functions constitute adaptations towards an acidic environment. The objective of this study was to systematically determine which genes of L. reuteri 100-23 contribute to tolerance towards host gastric acid secretion. Genes predicted to be involved in acid resistance were inactivated, and their contribution to survival under acidic conditions was confirmed in model gastric juice. Fitness of five mutants that showed impaired in vitro acid resistance were then compared through competition experiments in ex-germ-free mice that were either treated with omeprazole, a proton-pump inhibitor that suppresses acid secretion in the stomach, or left untreated. This analysis revealed that the urease cluster was the predominant factor in mediating resistance to gastric acid production. Population levels of the mutant, which were substantially decreased in untreated mice, were almost completely restored through omeprazole, demonstrating that urease production in L. reuteri is mainly devoted to overcome gastric acid. The findings provide novel information on the mechanisms by which L. reuteri colonizes its gastric niche and demonstrate that in silico gene predictions and in vitro tests have limitations for predicting the ecological functions of colonization factors in bacterial symbionts.

Original languageEnglish (US)
Pages (from-to)2172-2184
Number of pages13
JournalEnvironmental microbiology
Volume18
Issue number7
DOIs
StatePublished - Jul 1 2016

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Lactobacillus reuteri
acid tolerance
gastric acid
gastrointestinal system
Gastrointestinal Tract
Gastric Acid
colonization
Acids
Omeprazole
Urease
gene
acid
urease
Genes
Stomach
mice
stomach
genes
secretion
gastric juice

ASJC Scopus subject areas

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Characterization of the ecological role of genes mediating acid resistance in Lactobacillus reuteri during colonization of the gastrointestinal tract. / Krumbeck, Janina A.; Marsteller, Nathan L.; Frese, Steven A.; Peterson, Daniel A.; Ramer-Tait, Amanda E.; Hutkins, Robert W.; Walter, Jens.

In: Environmental microbiology, Vol. 18, No. 7, 01.07.2016, p. 2172-2184.

Research output: Contribution to journalArticle

Krumbeck, Janina A. ; Marsteller, Nathan L. ; Frese, Steven A. ; Peterson, Daniel A. ; Ramer-Tait, Amanda E. ; Hutkins, Robert W. ; Walter, Jens. / Characterization of the ecological role of genes mediating acid resistance in Lactobacillus reuteri during colonization of the gastrointestinal tract. In: Environmental microbiology. 2016 ; Vol. 18, No. 7. pp. 2172-2184.
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