Abstract
Roseburia hominis is a flagellated gut anaerobic bacterium belonging to the Lachnospiraceae family within the Firmicutes phylum. A significant decrease of R. hominis colonization in the gut of ulcerative colitis patients has recently been demonstrated. In this work, we have investigated the mechanisms of R. hominis-host cross talk using both murine and in vitro models. The complete genome sequence of R. hominis A2-183 was determined. C3H/HeN germ-free mice were mono-colonized with R. hominis, and the host-microbe interaction was studied using histology, transcriptome analyses and FACS. Further investigations were performed in vitro and using the TLR5KO and DSS-colitis murine models. In the bacterium, R. hominis, host gut colonization upregulated genes involved in conjugation/mobilization, metabolism, motility, and chemotaxis. In the host cells, bacterial colonization upregulated genes related to antimicrobial peptides, gut barrier function, toll-like receptors (TLR) signaling, and T cell biology. CD4+CD25+FoxP3+ T cell numbers increased in the lamina propria of both mono-associated and conventional mice treated with R. hominis. Treatment with the R. hominis bacterium provided protection against DSS-induced colitis. The role of flagellin in host-bacterium interaction was also investigated. Mono-association of mice with R. hominis bacteria results in specific bidirectional gene expression patterns. A set of genes thought to be important for host colonization are induced in R. hominis, while the host cells respond by strengthening gut barrier function and enhancing Treg population expansion, possibly via TLR5-flagellin signaling. Our data reveal the immunomodulatory properties of R. hominis that could be useful for the control and treatment of gut inflammation.
Highlights
The human gut microbiota consists of more than 500–1,000 different phylotypes the majority of which belong to the Bacteroidetes and Firmicutes bacterial phyla [1]
Bacterial RNA was isolated from three different experimental conditions to distinguish between the effects of the gut environment and animal dietary components, (i) in vivo, from the cecum of mono-associated mice; (ii) in vitro, from bacteria grown in the presence of dietary components; and (iii) in vitro, from bacteria grown in culture
Bar graphs represent the number of genes up- or downregulated in mice after 14 and 28 days of colonization. (C) Heatmap generated from differentially expressed genes with functional significance between GF and R. hominis-colonized mice at 14 and 28 days
Summary
The human gut microbiota consists of more than 500–1,000 different phylotypes the majority of which belong to the Bacteroidetes and Firmicutes bacterial phyla [1]. The immunological importance of the gut Roseburia hominis Promotes Innate Immunity microbiota is well recognized; it is apparent in germ-free (GF) animals that have an impaired immune system, which, can be functionally reconstituted by the introduction of gut commensal bacteria [2,3,4]. Some species of clostridia, such as segmented filamentous bacteria (SFB), appear to be potent inducers of differentiation and maturation of intestinal Th1, Th17, and Treg cell lineages [7, 8]. Recent studies have demonstrated that the clostridia clusters IV and XIVa and the Altered Schaedler Flora can induce de novo generation of Treg cells, while mono-colonization with Bacteroides fragilis can correct the Th1/Th2 imbalance in germ-free mice by promoting the expansion of Treg cells [4, 9, 10]. The Treg-enhancing effects of B. fragilis are implemented via TLR2 signaling by polysaccharide A [12]
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