The lifestyle of the segmented filamentous bacterium: A non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing

Tomomi Kuwahara, Yositoshi Ogura, Kenshiro Oshima, Ken Kurokawa, Tadasuke Ooka, Hideki Hirakawa, Takehiko Itoh, Haruyuki Nakayama-Imaohji, Minoru Ichimura, Kikuji Itoh, Chieko Ishifune, Yoichi Maekawa, Koji Yasutomo, Masahira Hattori, Tetsuya Hayashi

Research output: Contribution to journalArticle

60 Citations (Scopus)

Abstract

Numerous microbes inhabit the mammalian intestinal track and strongly impact host physiology; however, our understanding of this ecosystem remains limited owing to the high complexity of the microbial community and the presence of numerous non-culturable microbes. Segmented filamentous bacteria (SFBs), which are clostridia-related Gram-positive bacteria, are among such non-culturable populations and are well known for their unique morphology and tight attachment to intestinal epithelial cells. Recent studies have revealed that SFBs play crucial roles in the post-natal maturation of gut immune function, especially the induction of Th17 lymphocytes. Here, we report the complete genome sequence of mouse SFBs. The genome, which comprises a single circular chromosome of 1 620 005 bp, lacks genes for the biosynthesis of almost all amino acids, vitamins/cofactors and nucleotides, but contains a full set of genes for sporulation/germination and, unexpectedly, for chemotaxis/flagella- based motility. These findings suggest a triphasic lifestyle of the SFB, which comprises two types of vegetative (swimming and epicellular parasitic) phases and a dormant (spore) phase. Furthermore, SFBs encode four types of flagellin, three of which are recognized by Toll-like receptor 5 and could elicit the innate immune response. Our results reveal the non-culturability, lifestyle and immunostimulation mechanisms of SFBs and provide a genetic basis for the future development of the SFB cultivation and gene-manipulation techniques.

Original languageEnglish
Pages (from-to)291-303
Number of pages13
JournalDNA Research
Volume18
Issue number4
DOIs
Publication statusPublished - 2011 Aug
Externally publishedYes

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Keywords

  • flagella
  • genome
  • non-culturable bacteria
  • segmented filamentous bacterium

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology

Cite this

Kuwahara, T., Ogura, Y., Oshima, K., Kurokawa, K., Ooka, T., Hirakawa, H., Itoh, T., Nakayama-Imaohji, H., Ichimura, M., Itoh, K., Ishifune, C., Maekawa, Y., Yasutomo, K., Hattori, M., & Hayashi, T. (2011). The lifestyle of the segmented filamentous bacterium: A non-culturable gut-associated immunostimulating microbe inferred by whole-genome sequencing. DNA Research, 18(4), 291-303. https://doi.org/10.1093/dnares/dsr022