Letter to the Editor | Published:

Immune-modulating gut symbionts are not “Candidatus Arthromitus”

Mucosal Immunology volume 6, pages 200201 (2013) | Download Citation

To the Editor: It is becoming increasingly evident that the microbial community of the intestine is critical for refining the immune system of its host. Nothing illustrates this better than the segmented filamentous bacteria (SFB). These vertebrate gut symbionts are tightly anchored to epithelial cells of the ileal mucosa and possess the unique ability to specifically modulate the host immune response, which has consequences that extend beyond the gut wall. SFB trigger a diverse array of immune functions, inducing innate immune responses,1, 2, 3 increasing and activating cytotoxic intraepithelial lymphocyte populations,4 and coordinating T-cell responses, including the specific induction of CD4+ T-helper 17 cells.2, 3 They appear to act as a double-edged sword for the mammalian immune system—on one side mediating protective immunity by potently inducing IgA-secreting cells5 but on the other side promoting autoimmune disorders by triggering rheumatoid arthritis6 and multiple sclerosis7 in experimental mouse models. This makes SFB one of the very few examples of gut commensals that can stimulate the postnatal maturation of the immune system.

Although the study of gut bacteria has traditionally occurred within the realm of microbiology, immunological studies have formed the vanguard in the quest to understand the SFB. This is why we wish to draw attention to proposed changes to the classification of this immunologically significant group. When Snel et al.8 showed that SFB form a distinct lineage of uncultivated bacteria within the bacterial family Clostridiaceae, they assigned them to the genus Arthromitus—a group of equally conspicuous bacterial filaments from arthropod guts that had been described by the American scientist Joseph Leidy over 160 years ago.9 However, assuming relatedness based on morphology alone was a mistake. Using molecular phylogenetic analysis of 16S rRNA gene sequences, we have recently shown that Leidy's Arthromitus in fact belongs to a different bacterial family, the Lachnospiraceae10—despite their striking similarity to mammalian SFB (Figure 1).

Figure 1
Figure 1

Phase contrast micrographs of an Arthromitus filament from the termite gut (a) and a segmented filamentous bacterium (SFB) from the murine ileum (b). Phylogenetic tree showing the distinct positions of “Candidatus Arthromitus” from arthropods and the SFB (“Candidatus Savagella”) from mammals (c) (modified from ref. 10).

Given the immunological importance of mammalian SFB, it is imperative that these two bacterial groups be distinguished from each other. Biological functions attributed to Leidy's Arthromitus will not necessarily apply to mammalian SFB and vice versa. In view of their distinct phylogenetic positions, the same name can no longer be used for both groups. Given the historical priority of Leidy's Arthromitus, and the apparent absence of SFB-like 16S rRNA gene sequences from arthropod guts, we proposed to rename SFB to “Candidatus Savagella”10—in honor of the American gut microbiologist Dwayne C. Savage, who was the first to describe this bacterial group in the ileum of rodents.11

References

  1. 1.

    et al. Activation of RegIIIβ/γ and interferon γ expression in the intestinal tract of SCID mice: an innate response to bacterial colonisation of the gut. Gut 54, 623–629 (2005).

  2. 2.

    et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 31, 677–689 (2009).

  3. 3.

    et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485–498 (2009).

  4. 4.

    , , , & Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol. Immunol. 39, 555–562 (1995).

  5. 5.

    , , & Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect. Immun. 67, 1992–2000 (1999).

  6. 6.

    et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32, 815–827 (2010).

  7. 7.

    , , & Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl Acad. Sci. USA. 108, 4615–4622 (2011).

  8. 8.

    et al. Comparison of 16S rRNA sequences of segmented filamentous bacteria isolated from mice, rats, and chickens and proposal of “Candidatus Arthromitus”. Int. J. Syst. Bacteriol. 45, 780–782 (1995).

  9. 9.

    On the existence of entophyta in healthy animals, as a natural condition. Proc. Acad. Natl Sci. Phila. 4, 225–233 (1849).

  10. 10.

    , , , & ‘Candidatus Arthromitus’ revised: segmented filamentous bacteria in arthropod guts are members of Lachnospiraceae. Environ. Microbiol. 14, 1454–1465 (2012).

  11. 11.

    & Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect. Immun. 10, 948–956 (1974).

Download references

Author information

Affiliations

  1. Department of Biogeochemistry, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch-Strasse, Marburg, Germany

    • C L Thompson
    • , A Mikaelyan
    •  & A Brune

Authors

  1. Search for C L Thompson in:

  2. Search for A Mikaelyan in:

  3. Search for A Brune in:

Competing interests

The authors declared no conflict of interest.

Corresponding author

Correspondence to A Brune.

About this article

Publication history

Published

DOI

https://doi.org/10.1038/mi.2012.91

Further reading