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

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...

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Published inNature communications Vol. 9; no. 1; pp. 3402 - 13
Main Authors Nakashima, Keisuke, Kimura, Satoshi, Ogawa, Yu, Watanabe, Soichi, Soma, Satoshi, Kaneko, Toyoji, Yamada, Lixy, Sawada, Hitoshi, Tung, Che-Huang, Lu, Tsai-Ming, Yu, Jr-Kai, Villar-Briones, Alejandro, Kikuchi, Sakura, Satoh, Noriyuki
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 24.08.2018
Nature Publishing Group
Nature Portfolio
Subjects
13/51
14/1
14/19
14/28
14/5
14/63
38/22
38/23
38/39
38/44
38/88
631/181/2481
631/250/347
631/326/2565/2134
64/116
64/60
82/29
82/58
82/80
82/83
Animals
Biodiversity
Chemical Sciences
Chitin
Chitin - immunology
Chordata - immunology
Chordata - microbiology
Ciona - immunology
Ciona - microbiology
Colonization
Digestive system
Epithelium
Fishes - immunology
Fishes - microbiology
Gastrointestinal Microbiome - physiology
Gastrointestinal tract
Humanities and Social Sciences
Immune system
Immunity
Immunology
Innovations
Intestinal microflora
Intestinal Mucosa - immunology
Intestinal Mucosa - microbiology
Intestine
Life Sciences
Male
Mammals
Membranes
Mice
Mice, Inbred C57BL
Microbiota
Microorganisms
Mucosa
Mucus
Mucus - microbiology
multidisciplinary
Nanofibers
Polymers
Populations and Evolution
Proteomes
Science
Science (multidisciplinary)
Online AccessGet full text
ISSN2041-1723
2041-1723
DOI10.1038/s41467-018-05884-0

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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. The coevolution of the animal gut mucosa and the gut microbiota is poorly understood. Here, Nakashima et al. identify intestinal chitinous membranes in basal chordates and ray-finned fish, and propose that the loss of this chitin barrier allowed mucus layers to become colonized by microbes in mammals.
AbstractList 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.
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. The coevolution of the animal gut mucosa and the gut microbiota is poorly understood. Here, Nakashima et al. identify intestinal chitinous membranes in basal chordates and ray-finned fish, and propose that the loss of this chitin barrier allowed mucus layers to become colonized by microbes in mammals.
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.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.
The coevolution of the animal gut mucosa and the gut microbiota is poorly understood. Here, Nakashima et al. identify intestinal chitinous membranes in basal chordates and ray-finned fish, and propose that the loss of this chitin barrier allowed mucus layers to become colonized by microbes in mammals.
ArticleNumber 3402
Author Yamada, Lixy
Kaneko, Toyoji
Kikuchi, Sakura
Satoh, Noriyuki
Watanabe, Soichi
Soma, Satoshi
Lu, Tsai-Ming
Ogawa, Yu
Kimura, Satoshi
Yu, Jr-Kai
Nakashima, Keisuke
Sawada, Hitoshi
Villar-Briones, Alejandro
Tung, Che-Huang
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  organization: Sugashima Marine Biological Laboratory, Graduate School of Science, Nagoya University
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  organization: Sugashima Marine Biological Laboratory, Graduate School of Science, Nagoya University
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  surname: Satoh
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  organization: Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University
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– reference: 30483523 - Microb Cell. 2018 Oct 30;5(11):522-524
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Snippet 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...
The coevolution of the animal gut mucosa and the gut microbiota is poorly understood. Here, Nakashima et al. identify intestinal chitinous membranes in basal...
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SubjectTerms 13/51
14/1
14/19
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14/5
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Animals
Biodiversity
Chemical Sciences
Chitin
Chitin - immunology
Chordata - immunology
Chordata - microbiology
Ciona - immunology
Ciona - microbiology
Colonization
Digestive system
Epithelium
Fishes - immunology
Fishes - microbiology
Gastrointestinal Microbiome - physiology
Gastrointestinal tract
Humanities and Social Sciences
Immune system
Immunity
Immunology
Innovations
Intestinal microflora
Intestinal Mucosa - immunology
Intestinal Mucosa - microbiology
Intestine
Life Sciences
Male
Mammals
Membranes
Mice
Mice, Inbred C57BL
Microbiota
Microorganisms
Mucosa
Mucus
Mucus - microbiology
multidisciplinary
Nanofibers
Polymers
Populations and Evolution
Proteomes
Science
Science (multidisciplinary)
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Title Chitin-based barrier immunity and its loss predated mucus-colonization by indigenous gut microbiota
URI https://link.springer.com/article/10.1038/s41467-018-05884-0
https://www.ncbi.nlm.nih.gov/pubmed/30143642
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Volume 9
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