Ecological Importance of Cross-Feeding of the Intermediate Metabolite 1,2-Propanediol between Bacterial Gut Symbionts
- 1 June 2020
- journal article
- research article
- Published by American Society for Microbiology in Applied and Environmental Microbiology
- Vol. 86 (11)
- https://doi.org/10.1128/AEM.00190-20
Abstract
Cross-feeding based on the metabolite 1,2-propanediol has been proposed to have an important role in the establishment of trophic interactions among gut symbionts, but its ecological importance has not been empirically established. Here, we show that in vitro growth of Lactobacillus reuteri (syn. Limosilactobacillus reuteri) ATCC PTA 6475 is enhanced through 1,2-propanediol produced by Bifidobacterium breve UCC2003 and Escherichia coli MG1655 from the metabolization of fucose and rhamnose, respectively. Work with isogenic mutants showed that the trophic interaction is dependent on the pduCDE operon in L. reuteri, which encodes the ability to use 1,2-propanediol, and the L-fucose permease (fucP) gene in B. breve, which is required for 1,2-propanediol formation from fucose. Experiments in gnotobiotic mice revealed that, although the pduCDE operon bestows a fitness burden on L. reuteri ATCC PTA 6475 in the mouse digestive tract, the ecological performance of the strain was enhanced in the presence of B. breve UCC2003 and the mucus-degrading species Bifidobacterium bifidum. The use of the respective pduCDE and fucP mutants of L. reuteri and B. breve in the mouse experiments indicated that the trophic interaction was specifically based on 1,2-propanediol. Overall, our work established the ecological importance of cross-feeding relationships based on 1,2-propanediol for the fitness of a bacterial symbiont in the vertebrate gut. IMPORTANCE Through experiments in gnotobiotic mice that employed isogenic mutants of bacterial strains that produce (Bifidobacterium breve) and utilize (Lactobacillus reuteri) 1,2-propanediol, this study provides mechanistic insight into the ecological ramifications of a trophic interaction between gut symbionts. The findings improve our understanding on how cross-feeding influences the competitive fitness of L. reuteri in the vertebrate gut and revealed a putative selective force that shaped the evolution of the species. The findings are relevant since they provide a basis to design rational microbial-based strategies to modulate gut ecosystems, which could employ mixtures of bacterial strains that establish trophic interactions or a personalized approach based on the ability of a resident microbiota to provide resources for the incoming microbe.Funding Information
- Campus Alberta Innovation Program
- Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada (Discovery Grant)
This publication has 57 references indexed in Scilit:
- Microbial degradation of complex carbohydrates in the gutGut Microbes, 2012
- Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomachThe ISME Journal, 2011
- The Evolution of Host Specialization in the Vertebrate Gut Symbiont Lactobacillus reuteriPLoS Genetics, 2011
- Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foragingProceedings of the National Academy of Sciences of the United States of America, 2010
- Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigmProceedings of the National Academy of Sciences of the United States of America, 2010
- Mucosal Glycan Foraging Enhances Fitness and Transmission of a Saccharolytic Human Gut Bacterial SymbiontCell Host & Microbe, 2008
- Removal of Antibiotic Resistance Gene-Carrying Plasmids from Lactobacillus reuteri ATCC 55730 and Characterization of the Resulting Daughter Strain, L . reuteri DSM 17938Applied and Environmental Microbiology, 2008
- Lactobacillus reuteri DSM 20016 Produces Cobalamin-Dependent Diol Dehydratase in Metabolosomes and Metabolizes 1,2-Propanediol by DisproportionationJournal of Bacteriology, 2008
- Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteriaBMC Microbiology, 2007
- Identification and Characterization of a Fructose Phosphotransferase System in Bifidobacterium breve UCC2003Applied and Environmental Microbiology, 2007