Fig. 7.

Transition of gut mucosal surface in chordates and its implication for animal–microbe association. This figure summarizes results of this comparative study of chordates. For animal groups, shown as pictograms, intestinal barrier structures are illustrated above. These illustrations focus on physical, but not cellular or humoral, components of barrier immunity. Arthropods and annelids share chitinous barrier membranes (blue dotted line) that allow movement of nutrients, but not luminal microbes (black ovals), onto the ciliated gut epithelium. This so-called peritrophic matrix (PM) is widely observed in other invertebrates, although the presence of chitin remains unclear. Tunicates possess chitinous membranes embedded in a matrix of gel-forming mucin (yellow circle). This membrane confines food microbes into the luminal space and keeps the ciliated epithelium almost axenic. In ray-finned fish, the mucosal surface is covered with a layer of gel-forming mucin that is secreted from goblet cells. This mucus layer is separated from the luminal, indigenous microbial community by chitinous barrier membranes. In mammals, chitinous membranes no longer exist, and gut microbes directly interact with the surrounding layer of gel-forming mucin. Note that the mammalian mucus system has multiple physiological roles, and there exists regional variation in mucus conditions. This illustration depicts the mouse colon, in which the mucosal surface is covered with two layers of gel-forming mucin, with the outer layer forming a distinct niche for dense microbial colonization (red ovals). “Yes” or “No” indicate the presence or absence of the items listed on the right, respectively. Previously, invertebrate PMs and mammalian mucus layers were not believed to share common descent. New data on tunicates and ray-finned fish, however, fill this gap and suggest a transition from a chitin-based ancestral condition to a mucin-based derived state (top). A tree diagram of animal phylogeny (bottom) helps to infer events that account for the transition (black circles on branches). Mucus colonization in mammalian guts appears to be a novel type of animal–microbe association that was established upon loss of chitin