BackgroundThe newborn mammal is rapidly colonized by a complex microbial community, whose importance for host health is becoming increasingly clear. Understanding the forces that shape the early community, especially during the nursing period, is critical to gain insight into how this consortium of microbes is assembled. Pigs present an attractive model for nursing humans, given physiological and compositional similarity of pig and human milk and the utility of pigs in experimental studies. However, there is a paucity of data examining the gut microbiome in nursing pigs from birth through weaning using modern molecular methods and fewer experimental studies that examine the impact of diet on these microbial communities.ResultsWe characterized the fecal microbiome of pigs from birth through 7 weeks of age, during which the animals were transitioned from an exclusive diet of sow milk to a starter diet composed of plant and animal-based components. Microbial communities were clearly distinguishable based on diet, being relatively stable absent dietary changes. Metagenomic sequencing was used to characterize a subset of animals before and after weaning, which identified glycan degradation pathways differing significantly between diets. Predicted enzymes active on milk-derived glycans that are otherwise indigestible to the host animal were enriched in the microbial metagenome of milk-fed animals. In contrast, the bacterial metagenome of weaned animals was enriched in functional pathways involved in plant glycan deconstruction and consumption.ConclusionsThe gut microbiome in young pigs is dramatically shaped by the composition of dietary glycans, reflected by the different functional capacities of the microbiome before and after weaning.Electronic supplementary materialThe online version of this article (doi:10.1186/s40168-015-0091-8) contains supplementary material, which is available to authorized users.

Recent research has provided mechanistic insight into the important contributions of the gut microbiota to vertebrate biology, but questions remain about the evolutionary processes that have shaped this symbiosis. In the present study, we showed in experiments with gnotobiotic mice that the evolution of Lactobacillus reuteri with rodents resulted in the emergence of host specialization. To identify genomic events marking adaptations to the murine host, we compared the genome of the rodent isolate L. reuteri 100-23 with that of the human isolate L. reuteri F275, and we identified hundreds of genes that were specific to each strain. In order to differentiate true host-specific genome content from strain-level differences, comparative genome hybridizations were performed to query 57 L. reuteri strains originating from six different vertebrate hosts in combination with genome sequence comparisons of nine strains encompassing five phylogenetic lineages of the species. This approach revealed that rodent strains, although showing a high degree of genomic plasticity, possessed a specific genome inventory that was rare or absent in strains from other vertebrate hosts. The distinct genome content of L. reuteri lineages reflected the niche characteristics in the gastrointestinal tracts of their respective hosts, and inactivation of seven out of eight representative rodent-specific genes in L. reuteri 100-23 resulted in impaired ecological performance in the gut of mice. The comparative genomic analyses suggested fundamentally different trends of genome evolution in rodent and human L. reuteri populations, with the former possessing a large and adaptable pan-genome while the latter being subjected to a process of reductive evolution. In conclusion, this study provided experimental evidence and a molecular basis for the evolution of host specificity in a vertebrate gut symbiont, and it identified genomic events that have shaped this process.

Highlights d An ordered sequence of immune changes after birth driven by microbial interactions d Lack of gut bifidobacteria and HMO-utilization genes correlates with systemic inflammation d Feeding B. infantis EVC001 upregulates IFNb and silences intestinal Th2 and Th17 d EVC001-associated indole-3-lactic acid upregulates inhibitory galectin-1 in T cells

The gut microbiome in early life plays an important role for long-term health and is shaped in large part by diet. Probiotics may contribute to improvements in health, but they have not been shown to alter the community composition of the gut microbiome. Here, we found that breastfed infants could be stably colonized at high levels by provision of B. infantis EVC001, with significant changes to the overall microbiome composition persisting more than a month later, whether the infants were born vaginally or by caesarean section. This observation is consistent with previous studies demonstrating the capacity of this subspecies to utilize human milk glycans as a nutrient and underscores the importance of pairing a probiotic organism with a specific substrate. Colonization by B. infantis EVC001 resulted in significant changes to fecal microbiome composition and was associated with improvements in fecal biochemistry. The combination of human milk and an infant-associated Bifidobacterium sp. shows, for the first time, that durable changes to the human gut microbiome are possible and are associated with improved gut function.