Transmission Electron Microscopic Demonstration of Phagocytosis and Intracellular Processing of Segmented Filamentous Bacteria by Intestinal Epithelial Cells of the Chick Ileum

Abstract

Segmented filamentous bacteria (SFB) are autochthonous bacteria colonizing the ileum of many young animals by attaching to intestinal epithelial cells. These nonpathogenic bacteria strongly stimulate the mucosal immune system and induce intestinal epithelial cells to express major histocompatibility complex class II molecules. We tried to discover whether SFB are phagocytized and intracellularly processed by the host cells, which is indicative of antigen processing. The middle part of the ileum was extracted from 10-and 20-day-old broiler chicks (Gallus gallus domesticus). Samples were processed and examined by scanning and transmission electron microscopy (SEM and TEM, respectively). In SEM, no, few, medium, and dense SFB colonization levels were classified. In TEM of cells from animals with medium or dense SFB colonization levels, we could observe extracellular particles ranging from those only indenting the cell membrane to particles found in the cytoplasmatic area beyond the terminal web. These particles had a structural similarity with SFB that were floating freely in the intestinal lumen. Furthermore, we observed unlacing of the membrane and septum surrounding the extracellular particles and their incorporation into host cytoplasmatic components, which strongly suggests that these particles are phagocytized and intracellularly processed SFB. This conclusion is supported by TEM analysis of samples with no or few SFB, in which we failed to find these characteristic morphologies. The phagocytosis process described here could be an important trigger for the stimulating effect of SFB on the mucosal immune system.Segmented filamentous bacteria (SFB) are known to be nonpathogenic, gram-positive, anaerobic, spore-forming bacteria that inhabit the intestinal tract. SFB are characterized by their long filamentous shape with defined septa between each segment and their attachment to epithelial cells. Although SFB have been reported in many animal species, an official taxonomic name has not been established as yet due to the lack of an in vitro culturing method. Using 16S ribosomal DNA analysis, the phylogenetic positions of SFB in mice, rats, and chickens have been reported as being closely related to each other and distantly related to members of the genus Clostridium (19). However, SFB of chickens are different from those of mice, because SFB of mice are longer, wider, and have slightly different morphological characteristics than those of chickens (1). Furthermore, SFB in chickens, rats, and mice are reported to be host specific (1,24). SFB adhere to intestinal epithelial cells with holdfasts, and filaments are usually found only at the ileal villus tip of young animals (4,6,10,12,16,17). Recently, SFB have been reported to have a potential antagonistic effect against gastrointestinal infections (8). Observations by transmission electron microscopy (TEM) have revealed that the host cells to which SFB are anchored do not show any cytopathologic changes, and no inflammatory reactions have been observed in the lamina...

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Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut

“…Molecular analyses revealed a diverse bacterial composition in the small intestinal contents (data not shown), yet the repertoire of bacteria adherent to the gut epithelium was rather limited and dominated by uncultured anaerobes. Among these, SFB seem to be a major population that activates the immune system because (i) SFB strongly attach to the gut epithelium (19,20) and are the main (if not the only) bacterial species that could be detected in IEC suspension (data not shown).…”

Segmented Filamentous Bacteria Interact with Intraepithelial Mononuclear Cells

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