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maximally coated wild-type B. fragilis compared with the Accf and APSB/C strains(Fig 3G). IgA induced by B. fragilis Accf exhibited reduced binding to wild-type bacteria(Fig 3G). The addition of IgA to in vivo-adapted, IgA-free bacteria increased adherence of B fragilis to intestinal epithelial cells in tissue culture(Fig. 3H), yet had no effect on bacterial viability(fig. S4E). Cell lines known to produce more mucus(36 )exhibited a greater capacity for IgA-enhanced B. fragilis adherence(fig. S4F), consistent with prior work showing that Iga binds mucus (36-38). Importantly, IgA-enhanced adherence was decreased if targeted bacteria lack ccfor PSB/C, or if the Iga tested was induced by a ccf mutant or Bacteroides thetaiotaomicron( Fig. 3H and S4G). While pathogenic bacteria elaborate capsular polysaccharides for immune evasion, these results suggest B. fragil deploys specific capsules for immune attraction, potentially enabling stable mucosa We determined whether IgA coating promotes B. fragilis colonization in mice. Using the horizontal transmission paradigm, Rag/ mice colonized with wild-type B. fragilis were eadily co-colonized by an isogenic strain from a co-housed animal (fig. S5A and B), showing loss of colonization resistance in the absence of adaptive immunity. We next treated wild-type mice with an anti-CD20 antibody (fig. S5C)(39)to deplete B cells (fig. S5D-F thus reducing total fecal IgA levels(fig. S5G)and eliminating IgA coating of wild-type B fragilis during mono-colonization(Fig 4A). IgA recovered from isotype control treated so mono-colonized with B fragilis, adherence of wild-type bacteria to epithelial cells in vitro, while IgA from anti-CD20 treated mice had no effect despite being exposed to B. fragilis antigens(Fig. 4B ). In the horizontal transmission assay, B cell depleted mice mono-colonized with B. fragilis were readily invaded by wild-type bacteria, while isotype control-injected animals retained colonization resistance(Fig. 4C and S5H) Therefore, active B cell responses to B. fragilis colonization enhance single-strain stability As B cell depletion eliminates all antibody isotypes, germ-free IgA mice(40)were IgM(fig. S6A). In a horizontal transmission assay with wild-type(BALB/c)and gA x gby generated and mono-colonized with B. fragilis. We did not observe compensatory coatin mice, lack of Iga allowed co-colonization by challenge strains(Fig. 4D, S6B-D), indicating that IgA specifically contributes to single-strain stability. This feature was reproduced in mice with a full microbial community"spiked"with genetically marked B. fragilis strains (fig. S6E and F), revealing that single-strain stability of an individual bacterial species occurs in the context of a complex community. Mono-colonized IgA-/- mice harbored reduced levels of live bacteria in the colon mucus compared to wild-type mice(Fig. 4E) though they had greater numbers of bacteria in the colon lumen(fig. S6G). TEM images of ascending colon tissues reveal that in IgA/ animals, wild-type B. fragilis failed to aggregate on the epithelial surface(Fig. 4F and 4G), similar to the ccfand PSB/C mutants in presence of (fig. S7), indicating that enhanced mucosal colonization may be due to increased aggregation or growth(41)within mucus. These findings converge to support a model whereby ccfregulates of specific capsular polysaccharides to attract Iga bindin allowing for robust mucosal colonization and single-strain stability cience. Author manuscript; available in PMC 2018 November 18maximally coated wild-type B. fragilis compared with the Δccf and ΔPSB/C strains (Fig. 3G). IgA induced by B. fragilis Δccf exhibited reduced binding to wild-type bacteria (Fig. 3G). The addition of IgA to in vivo-adapted, IgA-free bacteria increased adherence of B. fragilis to intestinal epithelial cells in tissue culture (Fig. 3H), yet had no effect on bacterial viability (fig. S4E). Cell lines known to produce more mucus (36) exhibited a greater capacity for IgA-enhanced B. fragilis adherence (fig. S4F), consistent with prior work showing that IgA binds mucus (36–38). Importantly, IgA-enhanced adherence was decreased if targeted bacteria lack ccf or PSB/C, or if the IgA tested was induced by a ccf mutant or Bacteroides thetaiotaomicron (Fig. 3H and S4G). While pathogenic bacteria elaborate capsular polysaccharides for immune evasion, these results suggest B. fragilis deploys specific capsules for immune attraction, potentially enabling stable mucosal colonization. We determined whether IgA coating promotes B. fragilis colonization in mice. Using the horizontal transmission paradigm, Rag1 −/− mice colonized with wild-type B. fragilis were readily co-colonized by an isogenic strain from a co-housed animal (fig. S5A and B), showing loss of colonization resistance in the absence of adaptive immunity. We next treated wild-type mice with an anti-CD20 antibody (fig. S5C) (39) to deplete B cells (fig. S5D–F), thus reducing total fecal IgA levels (fig. S5G) and eliminating IgA coating of wild-type B. fragilis during mono-colonization (Fig. 4A). IgA recovered from isotype control treated mice, also mono-colonized with B. fragilis, promoted adherence of wild-type bacteria to epithelial cells in vitro, while IgA from anti-CD20 treated mice had no effect despite being exposed to B. fragilis antigens (Fig. 4B). In the horizontal transmission assay, B cell depleted mice mono-colonized with B. fragilis were readily invaded by wild-type bacteria, while isotype control-injected animals retained colonization resistance (Fig. 4C and S5H). Therefore, active B cell responses to B. fragilis colonization enhance single-strain stability. As B cell depletion eliminates all antibody isotypes, germ-free IgA−/− mice (40) were generated and mono-colonized with B. fragilis. We did not observe compensatory coating by IgM (fig. S6A). In a horizontal transmission assay with wild-type (BALB/c) and IgA−/− mice, lack of IgA allowed co-colonization by challenge strains (Fig. 4D, S6B–D), indicating that IgA specifically contributes to single-strain stability. This feature was reproduced in mice with a full microbial community “spiked” with genetically marked B. fragilis strains (fig. S6E and F), revealing that single-strain stability of an individual bacterial species occurs in the context of a complex community. Mono-colonized IgA−/− mice harbored reduced levels of live bacteria in the colon mucus compared to wild-type mice (Fig. 4E), though they had greater numbers of bacteria in the colon lumen (fig. S6G). TEM images of ascending colon tissues reveal that in IgA−/− animals, wild-type B. fragilis failed to aggregate on the epithelial surface (Fig. 4F and 4G), similar to the ccf and PSB/C mutants in wild-type animals. B. fragilis cells also formed aggregates in feces in the presence of IgA (fig. S7), indicating that enhanced mucosal colonization may be due to increased aggregation or growth (41) within mucus. These findings converge to support a model whereby ccf regulates expression of specific capsular polysaccharides to attract IgA binding, allowing for robust mucosal colonization and single-strain stability. Donaldson et al. Page 4 Science. Author manuscript; available in PMC 2018 November 18. Author Manuscript Author Manuscript Author Manuscript Author Manuscript
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