Habitat, Succession, Attachment, and Morphology of Segmented, Filamentous Microbes Indigenous to the Murine Gastrointestinal Tract

Abstract

Some indigenous microorganisms localize on epithelial surfaces in various areas of the digestive tracts of animals. One of these, a segmented, filamentous microbe, localizes on the epithelium in the small bowels of mice and rats. These filamentous microbes colonize mice at weaning time and persist in adult animals for at least 2 months. Results of the study of light and electron micrographs suggest that the microorganisms are procaryotic, and that they interact with small bowel epithelial cells to form an attachment site. This site consists of modified epithelial cell membrane and apical cytoplasm adjacent to the attached bacterium. The microbe fills the site with part of its first segment. This segment has a nipple-like appendage on the end inserted into the epithelial cell. The other segments, which compose the rest of the filament, are usually separated by septa. Many of the individual segments contain intrasegmental bodies that appear to be procaryotic cells. Some of these intrasegmental bodies are similar in morphology to the first segment of each filament inserted into an epithelial cell. These intracellular bodies may be components in the life cycle of the microorganism. The organism has not yet been cultured in recognizable form. Therefore, such a hypothesis cannot be proved as yet, nor can the microbe be classified with certainty. Because it localizes in an epithelial habitat in the small bowel, however, it may be a particularly important microbial type in the gastrointestinal ecosystem of laboratory rodents. Adult murine gastrointestinal tracts contain many types of indigenous microorganisms living in relatively stable communities localized in specific regions of the tract (5, 7, 10, 15, 16, 18). The various microbial types in these communities colonize the tracts of neonatal mice in a characteristic and reproducible succession. The succession in suckling mice has been reported for lactic acid bacteria, coliforms, enterococci, bacteroides, fusiform, and spiral-shaped microbes. The habitats of these microorganisms in suckling and adult mice have been described (4, 7, 17, 19). Another microbial type can be found on the epithelial surfaces of villi in the small intestines of adult rats (13, 14), mice (11; C. P. Davis, S. Erlandsen, and D. C. Savage, Abstr. Annu. Meet. Amer. Soc. Microbiol. 1973, p. 57), and chickens (8). This organism has never been identified with certainty. Moreover, little is known about its morphology, habitat, and ecology. In this report, we detail the ultrastructure, habitat, succession, and attachment to epithe-lial cells of these segmented, filamentous microbes in the small bowels of laboratory rodents. MATERIALS AND METHODS Animals. Specific pathogen-free male young adult rats were purchased from four different suppliers

The Role of Mucosal Microbiota in the Development, Maintenance, and Pathologies of the Mucosal Immune System

“…This SFB was tentatively named Arthromitis (jointed thread), and similar morphotypes have been found in the chicken, rat, mouse, pig, and trout (Snel et al, 1995;Meyerholz et al, 2003;Yamauchi and Snel, 2000;Urdaci et al, 2001).The vertebrate versions of this morphotype are gram-positive, segmented, obligate anaerobes that are spore formers (Davis and Savage, 1974). Savage and coworkers recognized SFB as a major component of the gut microbiota of mice and were able to enrich for these noncultivatable bacteria by isolating intestinal epithelial cells, to which the 5-to 20-μm SFB attached firmly via a holdfast segment that interdigitated with but did not penetrate the brush border (Davis and Savage, 1974;Tannock et al, 1987). The SFB of mice has recently been isolated by the Nijmegen group, using treatment of fecal material with organic solvents to kill vegetative organisms, followed by limiting dilution to colonize formerly GF mice (Klaasen et al, 1991).…”

“…These early studies have led to the development of mice with a defined intestinal flora-"altered Schaedler's flora"and these represent oligo-associated, gnotobiotic mice carrying eight benign commensal enteric bacteria (Dewhirst et al, 1999). Further definition of the normal intestinal microbiota of mice has led to discovery of a major colonizer, segmented filamentous bacteria (SFB) (Davis and Savage, 1974). These SFB have been shown to be related to clostridia (Snel et al, 1995), and variants have been found in rats, pigs, chickens, and trout (Snel et al, 1995;Meyerholz et al, 2002;Yamauchi and Snel, 2000;Urdaci et al, 2001).…”

“…Indigenous bacteria, such as SFB, can induce expression of MHC class II molecules on small intestinal ECs and strongly stimulate the mucosal immune system (Umesaki et al, 1995;Klaasen et al, 1993;Talham et al, 1999). SFB are in intimate contact with intestinal ECs, and the attachment induces apparent morphological changes at the apical surface of ECs, including indented, thickened, and more electron-dense membrane and accumulation of actin filaments (Davis and Savage, 1974;Jepson et al, 1993). Recently, Yamauchi and Snel (2000) have presented evidence strongly suggesting that SFB are phagocytosed and intracellularly processed in intestinal ECs of chicken ileum.…”

Microbiology and immunology: An ideal partnership for a tango at the gut surface—A tribute toPhilippe Sansonetti

“…Unexpectedly, however, only colonisation by the spore-enriched fraction of the mouse microbiota was Several clues led us to select SFB as a likely candidate. SFB are spore-forming Clostridia-related bacteria that colonise the mouse intestine at time of weaning concurrently to the initiation of the post-natal maturation of the gut immune barrier (Davis & Savage, 1974). SFB display tight adherence to ileal epithelial cells (Chase & Erlandsen, 1976;Davis & Savage, 1974;Ferguson & Birch-Andersen, 1979).…”

“…SFB are spore-forming Clostridia-related bacteria that colonise the mouse intestine at time of weaning concurrently to the initiation of the post-natal maturation of the gut immune barrier (Davis & Savage, 1974). SFB display tight adherence to ileal epithelial cells (Chase & Erlandsen, 1976;Davis & Savage, 1974;Ferguson & Birch-Andersen, 1979). Although SFB have been observed in many vertebrates, attachment has been shown to be species specific, suggesting that SFB species have coevolved with their respective hosts (Tannock, Miller, & Savage, 1984).…”