Small Intestinal Microbiota Oscillations, Host Effects and Regulation—A Zoom into Three Key Effector Molecules

Karina Ratiner; Tahel Fachler-Sharp; Eran Elinav

doi:10.3390/biology12010142

Small Intestinal Microbiota Oscillations, Host Effects and Regulation—A Zoom into Three Key Effector Molecules

Karina Ratiner, Tahel Fachler-Sharp, Eran Elinav^*

^*Corresponding author for this work

Department of Systems Immunology

Research output: Contribution to journal › Review article › peer-review

5 Citations (Scopus)

Abstract

The gut microbiota features a unique diurnal rhythmicity which contributes to modulation of host physiology and homeostasis. The composition and activity of the microbiota and its secreted molecules influence the intestinal milieu and neighboring organs, such as the liver. Multiple immune-related molecules have been linked to the diurnal microbiota-host interaction, including Reg3γ, IgA, and MHCII, which are secreted or expressed on the gut surface and directly interact with intestinal bacteria. These molecules are also strongly influenced by dietary patterns, such as high-fat diet and time-restricted feeding, which are already known to modulate microbial rhythms and peripheral clocks. Herein, we use Reg3γ, IgA, and MHCII as test cases to highlight the divergent effects mediated by the diurnal activity of the gut microbiota and their downstream host effects. We further highlight current challenges and conflicts, remaining questions, and perspectives toward a holistic understanding of the microbiome’s impacts on circadian human behavior.

Original language	English
Article number	142
Number of pages	17
Journal	Biology (Basel, Switzerland)
Volume	12
Issue number	1
DOIs	https://doi.org/10.3390/biology12010142
Publication status	Published - 16 Jan 2023

Bibliographical note

K.R. is the recipient of the Nehemia Levtzion Scholarship for Outstanding Doctoral Students. E.E. is supported by the Leona M. and Harry B. Helmsley Charitable Trust; the Adelis Foundation; the Ben B. And Joyce E. Eisenberg Foundation; the Estate of Bernard Bishin for the WIS-Clalit Program; the Jeanne and Joseph Nissim Center for Life Sciences Research; Miel de Botton; the Swiss Society Institute for Cancer Prevention Research; the Belle S. and Irving E. Meller Center for the Biology of Aging; the Sagol Institute for Longevity Research; the Sagol Weizmann-MIT Bridge Program; the Norman E. Alexander Family M Foundation Coronavirus Research Fund; the Mike and Valeria Rosenbloom Foundation; the Daniel Morris Trust; the Isidore and Penny Myers Foundation; the Vainboim Family; and by grants funded by the European Research Council; the Israel Science Foundation; the Israel Ministry of Science and Technology; the Israel Ministry of Health; the German–Israeli Helmholtz International Research School: Cancer-TRAX (HIRS-0003); the Helmholtz Association’s Initiative and Networking Fund; the Minerva Foundation; the Garvan Institute; the European Crohn’s and Colitis Organization; DeutschIsraelische Projektkooperation; the IDSA Foundation; a WIS-MIT grant; Emulate; the Charlie Teo Foundation; the Mark Foundation for Cancer Research, and the Wellcome Trust. E.E. is the incumbent of the Sir Marc and Lady Tania Feldmann Professorial Chair of Immunology; a senior fellow of the Canadian Institute of Advanced Research; and an international scholar of the Bill & Melinda Gates Foundation and the Howard Hughes Medical Institute.

Publisher Copyright:
© 2023 by the authors.

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title = "Small Intestinal Microbiota Oscillations, Host Effects and Regulation—A Zoom into Three Key Effector Molecules",

abstract = "The gut microbiota features a unique diurnal rhythmicity which contributes to modulation of host physiology and homeostasis. The composition and activity of the microbiota and its secreted molecules influence the intestinal milieu and neighboring organs, such as the liver. Multiple immune-related molecules have been linked to the diurnal microbiota-host interaction, including Reg3γ, IgA, and MHCII, which are secreted or expressed on the gut surface and directly interact with intestinal bacteria. These molecules are also strongly influenced by dietary patterns, such as high-fat diet and time-restricted feeding, which are already known to modulate microbial rhythms and peripheral clocks. Herein, we use Reg3γ, IgA, and MHCII as test cases to highlight the divergent effects mediated by the diurnal activity of the gut microbiota and their downstream host effects. We further highlight current challenges and conflicts, remaining questions, and perspectives toward a holistic understanding of the microbiome{\textquoteright}s impacts on circadian human behavior.",

author = "Karina Ratiner and Tahel Fachler-Sharp and Eran Elinav",

note = "K.R. is the recipient of the Nehemia Levtzion Scholarship for Outstanding Doctoral Students. E.E. is supported by the Leona M. and Harry B. Helmsley Charitable Trust; the Adelis Foundation; the Ben B. And Joyce E. Eisenberg Foundation; the Estate of Bernard Bishin for the WIS-Clalit Program; the Jeanne and Joseph Nissim Center for Life Sciences Research; Miel de Botton; the Swiss Society Institute for Cancer Prevention Research; the Belle S. and Irving E. Meller Center for the Biology of Aging; the Sagol Institute for Longevity Research; the Sagol Weizmann-MIT Bridge Program; the Norman E. Alexander Family M Foundation Coronavirus Research Fund; the Mike and Valeria Rosenbloom Foundation; the Daniel Morris Trust; the Isidore and Penny Myers Foundation; the Vainboim Family; and by grants funded by the European Research Council; the Israel Science Foundation; the Israel Ministry of Science and Technology; the Israel Ministry of Health; the German–Israeli Helmholtz International Research School: Cancer-TRAX (HIRS-0003); the Helmholtz Association{\textquoteright}s Initiative and Networking Fund; the Minerva Foundation; the Garvan Institute; the European Crohn{\textquoteright}s and Colitis Organization; DeutschIsraelische Projektkooperation; the IDSA Foundation; a WIS-MIT grant; Emulate; the Charlie Teo Foundation; the Mark Foundation for Cancer Research, and the Wellcome Trust. E.E. is the incumbent of the Sir Marc and Lady Tania Feldmann Professorial Chair of Immunology; a senior fellow of the Canadian Institute of Advanced Research; and an international scholar of the Bill & Melinda Gates Foundation and the Howard Hughes Medical Institute. Publisher Copyright: {\textcopyright} 2023 by the authors.",

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N2 - The gut microbiota features a unique diurnal rhythmicity which contributes to modulation of host physiology and homeostasis. The composition and activity of the microbiota and its secreted molecules influence the intestinal milieu and neighboring organs, such as the liver. Multiple immune-related molecules have been linked to the diurnal microbiota-host interaction, including Reg3γ, IgA, and MHCII, which are secreted or expressed on the gut surface and directly interact with intestinal bacteria. These molecules are also strongly influenced by dietary patterns, such as high-fat diet and time-restricted feeding, which are already known to modulate microbial rhythms and peripheral clocks. Herein, we use Reg3γ, IgA, and MHCII as test cases to highlight the divergent effects mediated by the diurnal activity of the gut microbiota and their downstream host effects. We further highlight current challenges and conflicts, remaining questions, and perspectives toward a holistic understanding of the microbiome’s impacts on circadian human behavior.

AB - The gut microbiota features a unique diurnal rhythmicity which contributes to modulation of host physiology and homeostasis. The composition and activity of the microbiota and its secreted molecules influence the intestinal milieu and neighboring organs, such as the liver. Multiple immune-related molecules have been linked to the diurnal microbiota-host interaction, including Reg3γ, IgA, and MHCII, which are secreted or expressed on the gut surface and directly interact with intestinal bacteria. These molecules are also strongly influenced by dietary patterns, such as high-fat diet and time-restricted feeding, which are already known to modulate microbial rhythms and peripheral clocks. Herein, we use Reg3γ, IgA, and MHCII as test cases to highlight the divergent effects mediated by the diurnal activity of the gut microbiota and their downstream host effects. We further highlight current challenges and conflicts, remaining questions, and perspectives toward a holistic understanding of the microbiome’s impacts on circadian human behavior.

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DO - 10.3390/biology12010142

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ER -

Small Intestinal Microbiota Oscillations, Host Effects and Regulation—A Zoom into Three Key Effector Molecules

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