Chitin-based barrier immunity and its loss predated mucus-colonization by indigenous gut microbiota

Keisuke Nakashima (), Satoshi Kimura, Yu Ogawa, Soichi Watanabe, Satoshi Soma, Toyoji Kaneko, Lixy Yamada, Hitoshi Sawada, Che-Huang Tung, Tsai-Ming Lu, Jr-Kai Yu, Alejandro Villar-Briones, Sakura Kikuchi and Noriyuki Satoh
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Keisuke Nakashima: Okinawa Institute of Science and Technology Graduate University
Satoshi Kimura: The University of Tokyo
Yu Ogawa: The University of Tokyo
Soichi Watanabe: The University of Tokyo
Satoshi Soma: The University of Tokyo
Toyoji Kaneko: The University of Tokyo
Lixy Yamada: Nagoya University
Hitoshi Sawada: Nagoya University
Che-Huang Tung: Academia Sinica
Tsai-Ming Lu: Academia Sinica
Jr-Kai Yu: Academia Sinica
Alejandro Villar-Briones: Okinawa Institute of Science and Technology Graduate University
Sakura Kikuchi: Okinawa Institute of Science and Technology Graduate University
Noriyuki Satoh: Okinawa Institute of Science and Technology Graduate University

Nature Communications, 2018, vol. 9, issue 1, 1-13

Abstract: Abstract Mammalian gut microbiota are integral to host health. However, how this association began remains unclear. We show that in basal chordates the gut space is radially compartmentalized into a luminal part where food microbes pass and an almost axenic peripheral part, defined by membranous delamination of the gut epithelium. While this membrane, framed with chitin nanofibers, structurally resembles invertebrate peritrophic membranes, proteome supports its affinity to mammalian mucus layers, where gut microbiota colonize. In ray-finned fish, intestines harbor indigenous microbes, but chitinous membranes segregate these luminal microbes from the surrounding mucus layer. These data suggest that chitin-based barrier immunity is an ancient system, the loss of which, at least in mammals, provided mucus layers as a novel niche for microbial colonization. These findings provide a missing link for intestinal immune systems in animals, revealing disparate mucosal environment in model organisms and highlighting the loss of a proven system as innovation.

Date: 2018
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DOI: 10.1038/s41467-018-05884-0

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