Dynamics of gut colonization by commensal and pathogenic bacteria that adhere to the intestinal epithelium

Abstract

Maintaining a healthy gut microbiome plays a critical role in avoiding gut-related pathologies. Bacterial adherence to the intestinal epithelium plays a vital role in niche establishment in the gut, as in vitro experiments and mathematical modeling suggest that adherence provides a strong competitive advantage over free-floating planktonic microbes. Currently, we lack the ability to study gut microbiome adherence in an in vivo model system. Through sampling natural populations of Caenorhabditis, we discovered three bacterial species that adhere to the intestinal epithelium of several wild Caenorhabditis isolates. When transferred to C. elegans, all three bacterial species colonized the entire anterior to posterior length of the intestine lumen. We isolated these bacterial species via in vitro growth or selective enrichment in the nematode gut and identified them as Lelliottia jeotgali, Candidatus Lumenectis limosiae, and Candidatus Enterosymbion pterelaium, the latter two representing new species. Adherent Ca. L. limosiae negatively affects host fitness, while Lelliottia jeotgali and Ca. E. pterelaium exhibited a neutral effect in our assays. We demonstrated that two of these species can actively proliferate in the intestine throughout the host lifespan, with Lelliottia jeotgali colonizing throughout the lumen simultaneously and Candidatus Lumenectis limosiae showing anterior-to-posterior directionality. In competition assays, animals pre-colonized with L. jeotgali significantly reduced colonization by pathogenic Ca. L. limosiae, but this effect was not seen when animals were colonized by both bacteria simultaneously. Strikingly, regardless of the colonization paradigm, populations exposed to both bacteria showed a near-identical mitigation of the pathogenic effects of Ca. L. limosiae. Altogether, these strains illustrate the capacity of microbiome bacteria to adhere, replicate, and establish a niche across the entire intestinal lumen in C. elegans and they present an opportunity to study bacterial adherence in the context of a whole, intact and transparent animal.