Resource partitioning in relation to cohabitation of Lactobacillus species in the mouse forestomach

Abstract

Phylogenetic analysis of gut communities of vertebrates is advanced, but the relationships, especially at the trophic level, between commensals that share gut habitats of monogastric animals have not been investigated to any extent. Lactobacillus reuteri strain 100-23 and Lactobacillus johnsonii strain 100-33 cohabit in the forestomach of mice. According to the niche exclusion principle, this should not be possible because both strains can utilise the two main fermentable carbohydrates present in the stomach digesta: glucose and maltose. We show, based on gene transcription analysis, in vitro physiological assays, and in vivo experiments that the two strains can co-exist in the forestomach habitat because 100-23 grows more rapidly using maltose, whereas 100-33 preferentially utilises glucose. Mutation of the maltose phosphorylase gene (malA) of strain 100-23 prevented its growth on maltose-containing culture medium, and resulted in the numerical dominance of 100-33 in the forestomach. The fundamental niche of L. reuteri 100-23 in the mouse forestomach can be defined in terms of 'glucose and maltose trophism'. However, its realised niche when L. johnsonii 100-33 is present is 'maltose trophism'. Hence, nutritional adaptations provide niche differentiation that assists cohabitation by the two strains through resource partitioning in the mouse forestomach. This real life, trophic phenomenon conforms to a mathematical model based on in vitro bacterial doubling times, in vitro transport rates, and concentrations of maltose and glucose in mouse stomach digesta.

Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing

“…In contrast to 13 C, almost all cells analyzed were enriched in 15 N, which is likely due to an enrichment of 15 N in the luminalfree ammonium pool and subsequent incorporation of the labeled ammonium via amino acid synthesis into biomass of all growing cells. 15 N-ammonium can originate from microbial disproportionation during fermentation of labeled proteins, but may also result from secretion of labeled urea into the lumen and subsequent hydrolysis if threonine in the host was deaminated (14).…”

“…These probes were specific for Akkermansia spp., Bacteroides acidifaciens, Mucispirillum spp., Lactobacillaceae/Enterococcaceae spp., and a Ruminococcaceae OTU_5807 species-level phylotype. All targeted microbial groups were enriched in 13 C compared with unlabeled controls (Fig. 3), indicating phylogenetically widespread incorporation of 13 Clabeled substrates either via direct utilization of host-derived compounds or cross-feeding.…”

“…Given the abundance of B. acidifaciens and Akkermansia spp. in these communities (relative abundance of 1.0 and 2.1%, respectively; Table S3) and the high proportions of 13 C-enriched cells in these populations (42 and 29%, respectively), these two groups are the numerically dominant foragers of host-derived proteins in this mouse cecum community.…”

“…To establish the tracer approach and to define the optimal sampling time for the NanoSIMS measurements, a physiologically relevant concentration of stable isotope labeled threonine (both 13 C and 15 N labeled) was given i.v. to mice and the transport of the stable isotopes was tracked in the blood serum, cecum tissue, and gut lumen using elemental analysis isotope ratio mass spectrometry (EA-IRMS).…”

“…This variation may either be due to the targeting of different genotypes or ecotypes with the same probe-stained population, or to heterogeneity in the location or activity of genetically similar or identical populations. It is, for example, possible that resource partitioning of mucosal products between related organisms leads to divergent or complementary ecological niches, a phenomenon that has been observed for Lactobacillus species in the forestomach of mice (13).…”