Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice and chickens

Yin, Yeshi; Wang, Yu; Zhu, Liying; Liu, Wei; Liao, Ningbo; Jiang, Mizu; Zhu, Baoli; Yu, Hongwei D.; Xiang, Charlie; Wang, Xin

doi:10.1038/ismej.2012.128

Cited by 128 publications

(139 citation statements)

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“…A complex microbial community was insufficient for generating a robust population of Th17 cells in the gut of SPF mice lacking SFB (9, 10) and gnotobiotic mice colonized long term with human fecal contents (42). Although SFB has been detected in multiple vertebrate species (43), there exists only sparse evidence of a related microbe colonizing humans (43)(44)(45)(46). A recent study showed that a consortium of 20 symbionts from the feces of an IBD patient could induce Th17 cells in mice but failed to identify the active microbes in healthy people (11).…”

Section: Discussionmentioning

confidence: 99%

Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice

Tan

Sefik

Geva‐Zatorsky

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

361

287

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Th17 cells accrue in the intestine in response to particular microbes. In rodents, segmented filamentous bacteria (SFB) induce intestinal Th17 cells, but analogously functioning microbes in humans remain undefined. Here, we identified human symbiont bacterial species, in particular Bifidobacterium adolescentis, that could, alone, induce Th17 cells in the murine intestine. Similar to SFB, B. adolescentis was closely associated with the gut epithelium and engendered cognate Th17 cells without attendant inflammation. However, B. adolescentis elicited a transcriptional program clearly distinct from that of SFB, suggesting an alternative mechanism of promoting Th17 cell accumulation. Inoculation of mice with B. adolescentis exacerbated autoimmune arthritis in the K/BxN mouse model. Several off-the-shelf probiotic preparations that include Bifidobacterium strains also drove intestinal Th17 cell accumulation.

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Section: Discussionmentioning

confidence: 99%

Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice

Tan

Sefik

Geva‐Zatorsky

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

361

287

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“…SFB is highly sensitive to diet composition and, because of a large number of auxotrophies (75), SFB survives by establishing close proximity to the epithelial surface, and possibly symbiotic interactions with certain commensal bacteria (76). The few studies analyzing the potential symbiotic relationship between specific commensal bacteria and SFB indicate that members of the Bacteroides/Prevotella or Lactobacillus genus may be key to explain its maintenance and abundance in infants and mice, respectively (77,78). Moreover, a recent paper shows that decrease of SFB in the ileum corresponds to an increase of the Erysipelotrichi class (79).…”

Section: Discussionmentioning

confidence: 99%

High-fat diet modifies the PPAR-γ pathway leading to disruption of microbial and physiological ecosystem in murine small intestine

Tomas

Mulet

Saffarian

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

203

146

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Diet is among the most important factors contributing to intestinal homeostasis, and basic functions performed by the small intestine need to be tightly preserved to maintain health. Little is known about the direct impact of high-fat (HF) diet on small-intestinal mucosal defenses and spatial distribution of the microbiota during the early phase of its administration. We observed that only 30 d after HF diet initiation, the intervillous zone of the ileum—which is usually described as free of bacteria—became occupied by a dense microbiota. In addition to affecting its spatial distribution, HF diet also drastically affected microbiota composition with a profile characterized by the expansion of Firmicutes (appearance of Erysipelotrichi), Proteobacteria (Desulfovibrionales) and Verrucomicrobia, and decrease of Bacteroidetes (family S24-7) and Candidatus arthromitus. A decrease in antimicrobial peptide expression was predominantly observed in the ileum where bacterial density appeared highest. In addition, HF diet increased intestinal permeability and decreased cystic fibrosis transmembrane conductance regulator (Cftr) and the Na-K-2Cl cotransporter 1 (Nkcc1) gene and protein expressions, leading to a decrease in ileal secretion of chloride, likely responsible for massive alteration in mucus phenotype. This complex phenotype triggered by HF diet at the interface between the microbiota and the mucosal surface was reversed when the diet was switched back to standard composition or when mice were treated for 1 wk with rosiglitazone, a specific agonist of peroxisome proliferator-activated receptor-γ (PPAR-γ). Moreover, weaker expression of antimicrobial peptide-encoding genes and intervillous bacterial colonization were observed in Ppar-γ–deficient mice, highlighting the major role of lipids in modulation of mucosal immune defenses.

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“…SFB are gut commensal bacteria that colonize the ileum mucosa of various vertebrates, including humans, mice, rats, chickens, and pigs (5)(6)(7)(8). However, SFB colonization is host specific (9,10), and a direct interaction with the ileum mucosa may be required for regulating the differentiation of Th17 cells (2,4,10).…”

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confidence: 99%

Host Specificity of Flagellins from Segmented Filamentous Bacteria Affects Their Patterns of Interaction with Mouse Ileal Mucosal Proteins

Chen

Yin

Wang

et al. 2017

Appl Environ Microbiol

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Segmented filamentous bacteria (SFB) are known modulators of the mammalian immune system. Currently, the technology for investigating SFB culture in vitro is immature, and as a result, the mechanisms of SFB colonization and immune regulation are not yet fully elucidated. In this study, we investigated the gene diversity and host specificity of SFB flagellin genes. The fliC1 and fliC2 genes are relatively conserved, while the fliC3 and fliC4 genes are more variable, especially at the central and C-terminal regions. Host specificity analysis demonstrated that the fliC1 genes do not cluster together based on the host organism, whereas the fliC3 and fliC4 genes were host specific at the nucleotide and deduced amino acid levels. SFB flagellin protein expression in the ileum mucosa and cecal contents was detected by using fluorescence in situ hybridization (FISH) combined with immunohistochemical (IHC) analysis, immunoblotting, and liquid chromatography-tandem mass spectrometry (LC-MS/MS). Although the purified SFB FliC3 protein originating from both mouse and rat was able to activate Toll-like receptor 5 (TLR5)-linked NF-B signaling, no host specificity was observed. Interestingly, the patterns of interaction with mouse ileum mucosal proteins were different for mouse FliC3 (mFliC3) and rat FliC3 (rFliC3). Gene Ontology (GO) and KEGG analyses indicated that more adherence-related proteins interacted with mFliC3, while more lysosome-and proteolysis-related proteins interacted with rFliC3. In vitro degradation experiments indicated that the stability of rFliC3 was lower than that of mFliC3 when they were incubated with mouse ileum mucosal proteins. In summary, the gene diversity and host specificity of SFB flagellin genes were investigated, and SFB flagellin expression was detected in gut samples.IMPORTANCE Since SFB genomes contain only one copy of each FliC gene, the diversity of FliC is representative of SFB strain diversity. Currently, little is known regarding the diversity and specificity of members of the group of SFB. The work presented herein demonstrates that select SFB strains, exhibiting unique FliC patterns, are present in a variety of mammalian hosts. SFB fliC genes were found to interact with a number of unique targets, providing further evidence for SFB host selection. Together, this work represents a major advancement in identifying SFB and delineating how members of the group of SFB interact with the host. Future examination of FliC genes will likely enhance our knowledge of intestinal colonization by the gut microbiota.KEYWORDS segmented filamentous bacteria, flagellin, host specificity, gene diversity, ileum mucosal proteins

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Comparative analysis of the distribution of segmented filamentous bacteria in humans, mice and chickens

Cited by 128 publications

References 31 publications

Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice

Identifying species of symbiont bacteria from the human gut that, alone, can induce intestinal Th17 cells in mice

High-fat diet modifies the PPAR-γ pathway leading to disruption of microbial and physiological ecosystem in murine small intestine

Host Specificity of Flagellins from Segmented Filamentous Bacteria Affects Their Patterns of Interaction with Mouse Ileal Mucosal Proteins

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