Host-microbial symbiosis in the vertebrate gastrointestinal tract and the Lactobacillus reuteri paradigm

Abstract

Vertebrates engage in symbiotic associations with vast and complex microbial communities that colonize their gastrointestinal tracts. Recent advances have provided mechanistic insight into the important contributions of the gut microbiome to vertebrate biology, but questions remain about the evolutionary processes that have shaped symbiotic interactions in the gut and the consequences that arise for both the microbes and the host. Here we discuss the biological principles that underlie microbial symbiosis in the vertebrate gut and the potential of the development of mutualism. We then review phylogenetic and experimental studies on the vertebrate symbiont Lactobacillus reuteri that have provided novel insight into the ecological and evolutionary strategy of a gut microbe and its relationship with the host. We argue that a mechanistic understanding of the microbial symbiosis in the vertebrate gut and its evolution will be important to determine how this relationship can go awry, and it may reveal possibilities by which the gut microbiome can be manipulated to support health.vertebrate symbiont | microbiota | mutualism

The inconstant gut microbiota of Drosophila species revealed by 16S rRNA gene analysis

“…The distinctiveness of the gut microbiota can be attributed to the ecological conditions in the gut, including regions with extreme pH or redox potential, biologically active compounds (for example, digestive enzymes, immune effectors) and disturbance (for example, bulk flow of food, production of mucus or other extracellular secretions, epithelial cell turnover) (Karasov and Douglas, 2013). Furthermore, the gut is a living habitat, and coevolutionary interactions between the microbiota and the animal have been predicted, potentially resulting in the evolutionary divergence of gut-associated microorganisms from their free-living relatives, and codiversification of the microbiota and animal host (Dethlefsen et al, 2007;Walter et al, 2011). Sustained codiversification results incongruence between host phylogeny and composition of the gut microbiota.…”

Dangerous Disappearing Act: Commensal Gut Microbiota After Acute Severe Insults

“…SCFA also contribute to the host defense by decreasing intestinal pH, inhibiting pathogen expression of virulence factors, and interfering with the capacity of enteric pathogens to invade intestinal cells [16]. Loss of competitive inhibition by commensal bacteria creates a favorable environment for pathogen growth [10]. It is not surprising, then, that pathogens proliferated after the depletion of commensal bacteria in this study [5].…”

“…Many anaerobic Bifidobacterium and facultatively anaerobic Lactobacillus species produce bacteriocins that kill enteric pathogens [10,11]. Lactic acid-producing bacteria also acidify their surroundings, thus, inhibiting the growth of pathogens such as Escherichia coli 0157:H7 [12].…”

“…The presence of beneficial commensal bacteria strengthens intestinal barrier function, reduces the translocation of lipopolysaccharide and bacteria, and reverses inflammatory signaling [13]. The vertebrate immune system has evolved the capacity for immunomodulation by specialized commensals [10], resulting in tolerance that protects beneficial bacteria from immune killing and allows some to adhere to intestinal epithelial cells [14].…”

“…The bacteria that are destroyed during acute severe stress, obligate anaerobes and Lactobacillus, have been shown to protect the host from infection by competitive exclusion of pathogens, production of antimicrobial substances, and prevention of pathogen adhesion to epithelial cells [10].…”