Isolation of Segmented Filamentous Bacteria from Complex Gut Microbiota

Ericsson, Aaron C.; Turner, Giedre; Montoya, Lisa; Wolfe, Annie E.; Meeker, Stacey; Hsu, Charlie C.; Maggio‐Price, Lillian; Franklin, Craig L.

doi:10.2144/000114319

Cited by 14 publications

(23 citation statements)

References 11 publications

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“…Single-cell sequencing demonstrated that single nucleotide polymorphism (SNP) mutations exist within disparate SFB genomes isolated from the same host (23). Current technology for SFB culture and passage in vitro is relatively unrefined (13,14). There are no simple single-cell sequencing methods available for detecting various SFB strains.…”

Section: Discussionmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

“…Ericsson et al and Schnupf et al established culturing methods for mouse SFB in vitro (13,14), although passaging of SFB in vitro is still problematic (13). Cultureindependent bioinformatic analysis could be used as a tool in finding candidate SFB functional genes.…”

mentioning

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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“…Experimental infection of susceptible Rainbow trout stock with feces from RTGE animals induced colonization and characteristic histopathological lesions containing SFB and an unidentified Gram-negative coccus, suggesting that SFB, in part, may be the etiological cause of RTGE ( McCarthy et al, 2016 ). Recent advances have identified different methods to culture SFB in vitro , accelerating research to study the interaction of SFB with different members of the intestinal microbiota ( Ericsson et al, 2015 ; Schupf et al, 2015 ).…”

Section: Effect On Host Microbiomementioning

confidence: 99%

Segmented Filamentous Bacteria – Metabolism Meets Immunity

et al. 2018

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Segmented filamentous bacteria (SFB) are a group of host-adapted, commensal organisms that attach to the ileal epithelium of vertebrate and invertebrate hosts. A genetic relative of the genus Clostridium, these morphologically unique bacteria display a replication and differentiation lifecycle initiated by epithelial tissue binding and filamentation. SFB intimately bind to the surface of absorptive intestinal epithelium without inducing an inflammatory response. Rather, their presence impacts the generation of innate and differentiation of acquired immunity, which impact the clearance of extracellular bacterial or fungal pathogens in the gastrointestinal and respiratory tracts. SFB have recently garnered attention due to their role in promoting adaptive and innate immunity in mice and rats through the differentiation and maturation of Th17 cells in the intestinal tract and production of immunoglobulin A (IgA). SFB are the first commensal bacteria identified that impact the maturation and development of Th17 cells in mice. Recently, microbiome studies have revealed the presence of Candidatus Arthromitus (occasionally designated as Candidatus Savagella), a proposed candidate species of SFB, in higher proportions in higher-performing flocks as compared to matched lower-performing flocks, suggesting that SFB may serve to establish a healthy gut and protect commercial turkeys from pathogens resulting in morbidity and decreased performance. In this review we seek to describe the life cycle, host specificity, and genetic capabilities of SFB, such as bacterial metabolism, and how these factors influence the host immunity and microbiome. Although the role of SFB to induce antigen-specific Th17 cells in poultry is unknown, they may play an important role in modulating the immune response in the intestinal tract to promote resistance against some infectious diseases and promote food-safety. This review demonstrates the importance of studying and further characterizing commensal, host-specific bacteria in food-producing animals and their importance to animal health.

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“…Later on, SFB load decreases becoming stable in adult animals probably in relation to age-dependent maturation and activity of the immune system. 17 It is difficult to validate similar data in humans, with follow-up studies of children from weaning to adult age. However, Yin et al analysed fresh faecal samples 18 and showed that SFB colonisation is age dependent in humans with the majority of individuals colonised within the first 2 years of life, and also that this colonisation disappeared by the age of 3 years.…”

Section: Introductionmentioning

confidence: 99%

PCR detection of segmented filamentous bacteria in the terminal ileum of patients with ulcerative colitis

Finotti

Gasparello

Cosenza

et al. 2017

BMJ Open Gastroenterol

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ObjectivesSegmented filamentous bacteria (SFB) have been detected in a wide range of different animal. Recently, the presence of SFB-like bacteria was shown in biopsies of the terminal ileum and ileocecal valve of both patients with ulcerative colitis and control subjects. The aim of this study was to verify whether PCR methods could be used for the detection of SFB in biopsy of patients with ulcerative colitis and its relationships with the disease stage.MethodsPCR methods were used to identify SFB in biopsies from the terminal ileum of patients with ulcerative colitis, showing that this approach represents a useful tool for the detection of SFB presence and analysis of the bacterial load.ResultsOur analysis detected SFB in all faecal samples of children at the time of weaning, and also show that putative SFB sequences are present in both patients with ulcerative colitis and control subjects. Results obtained using real-time quantitative PCR analysis confirm the presence of putative SFB sequences in samples from the terminal ileum of patients with ulcerative colitis and in control subjects.ConclusionsThe presence of putative SFB sequence in both patients with ulcerative colitis and control subject suggests that SFB cannot be considered as being uniquely associated with the disease. The second conclusion is that among the patients with ulcerative colitis, a tendency does exist for active disease samples to show higher SFB load, opening new perspectives about possible identification and pharmacological manipulation of SFB-mediated processes for new therapeutic strategy.

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Isolation of Segmented Filamentous Bacteria from Complex Gut Microbiota

Cited by 14 publications

References 11 publications

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

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

Segmented Filamentous Bacteria – Metabolism Meets Immunity

PCR detection of segmented filamentous bacteria in the terminal ileum of patients with ulcerative colitis

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