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

Nature Communications
Keisuke NakashimaNoriyuki Satoh

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.

References

Jul 26, 2000·Molecular Biology and Evolution·J L DesseynA Laine
Dec 4, 2003·Bioscience, Biotechnology, and Biochemistry·Minoru UjitaAkira Hara
Jan 24, 2004·Development Genes and Evolution·Keisuke NakashimaNori Satoh
Jan 1, 1997·Annual Review of Entomology·M J Lehane
Feb 1, 2005·Basic & Clinical Pharmacology & Toxicology·Tom C MartinsenHelge L Waldum
Jan 12, 2007·Nature·Margaret McFall-Ngai
Apr 29, 2008·Nucleic Acids Research·Mark JohnsonThomas L Madden
Jun 20, 2008·Cellular Microbiology·Carlos J RosadoMichelle A Dunstone
Sep 6, 2008·Development Genes and Evolution·Jr-Kai YuYutaka Satou
Sep 23, 2008·Proceedings of the National Academy of Sciences of the United States of America·Malin E V JohanssonGunnar C Hansson
Dec 11, 2008·Annual Review of Entomology·Dwayne HegedusUmut Toprak
Mar 23, 2010·Cell·Wendy S GarrettLaurie H Glimcher
Oct 26, 2010·Cellular and Molecular Life Sciences : CMLS·Keisuke NakashimaNori Satoh
Apr 8, 2011·The ISME Journal·Guus RoeselersJohn F Rawls
Sep 21, 2011·Proceedings of the National Academy of Sciences of the United States of America·Larry J DishawMaria Rosaria Pinto
Mar 28, 2012·Proceedings of the National Academy of Sciences of the United States of America·Daniel AmbortGunnar C Hansson
Apr 12, 2012·Blood·Yan-Feng ZhouTimothy A Springer
Apr 12, 2012·Nature Reviews. Microbiology·Nicole M KoropatkinEric C Martens
Jun 8, 2012·Science·Lora V HooperAndrew J Macpherson
Sep 14, 2012·Nature·Craig L MaynardCasey T Weaver
Feb 9, 2013·Proceedings of the National Academy of Sciences of the United States of America·Margaret McFall-NgaiJennifer J Wernegreen
Feb 26, 2013·Nature Reviews. Microbiology·Felix Sommer, Fredrik Bäckhed
Mar 13, 2013·Nature Reviews. Gastroenterology & Hepatology·Malin E V JohanssonGunnar C Hansson
Apr 18, 2013·Genes & Development·Aleksandar D KosticWendy S Garrett
May 31, 2013·The ISME Journal·Adam C-N WongAngela E Douglas
May 31, 2013·Glycobiology·Angela MarcobalJustin L Sonnenburg
Oct 9, 2013·Fish & Shellfish Immunology·Daniela GomezIrene Salinas
Dec 7, 2013·Proceedings. Biological Sciences·L Filipe C CastroJonathan M Wilson
Jan 18, 2014·Fungal Biology·Whitney M HoldenLouise A Rollins-Smith
Jan 21, 2014·Genome Biology and Evolution·Anne-C ZakrzewskiHarald Hausen
Mar 13, 2014·Molecular Ecology·Kendall D ClementsJ Howard Choat
Apr 1, 2014·Cell·Yasmine Belkaid, Timothy W Hand
Sep 19, 2014·Proceedings. Biological Sciences·Noriyuki SatohTeruaki Nishikawa
Mar 17, 2015·Current Biology : CB·W Joyce TangChris T Amemiya
Sep 6, 2015·Gut·R H HuntJ Tack
Sep 24, 2015·Nature Communications·Hai LiAndrew J Macpherson
Oct 27, 2015·Nature Reviews. Microbiology·Gregory P DonaldsonSarkis K Mazmanian
Feb 16, 2016·Microbial Pathogenesis·Muriel DerrienWillem M de Vos
Aug 9, 2016·Nature Reviews. Immunology·Malin E V Johansson, Gunnar C Hansson

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Citations

May 3, 2019·Cell and Tissue Research·Satoshi NakayamaMichio Ogasawara
Jul 17, 2019·The Journal of Experimental Biology·Chris N Glover, Alyssa M Weinrauch
Jun 3, 2021·Mucosal Immunology·Eva ClootsMichael J Grey

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Datasets Mentioned

BETA
-LC411764
PXD010503

Methods Mentioned

BETA
dissection
light microscopy
PCR
X-ray
glycosylation
electrophoresis
affinity purification
confocal microscopy

Software Mentioned

SEQUEST
MASCOT
tblastn
Ci
blastp
Photoshop

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