Cargando…

Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system

The immune equilibrium model suggests that exposure to microbes during early life primes immune responses for pathogen exposure later in life. While recent studies using a range of gnotobiotic (germ-free) model organisms offer support for this theory, we currently lack a tractable model system for i...

Descripción completa

Detalles Bibliográficos
Autores principales: Miller, Abigail J., Gass, Jordan, Jo, Myung Chul, Bishop, Lucas, Petereit, Juli, Woodhams, Douglas C., Voyles, Jamie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258664/
https://www.ncbi.nlm.nih.gov/pubmed/37305911
http://dx.doi.org/10.1098/rstb.2022.0125
_version_ 1785057514629365760
author Miller, Abigail J.
Gass, Jordan
Jo, Myung Chul
Bishop, Lucas
Petereit, Juli
Woodhams, Douglas C.
Voyles, Jamie
author_facet Miller, Abigail J.
Gass, Jordan
Jo, Myung Chul
Bishop, Lucas
Petereit, Juli
Woodhams, Douglas C.
Voyles, Jamie
author_sort Miller, Abigail J.
collection PubMed
description The immune equilibrium model suggests that exposure to microbes during early life primes immune responses for pathogen exposure later in life. While recent studies using a range of gnotobiotic (germ-free) model organisms offer support for this theory, we currently lack a tractable model system for investigating the influence of the microbiome on immune system development. Here, we used an amphibian species (Xenopus laevis) to investigate the importance of the microbiome in larval development and susceptibility to infectious disease later in life. We found that experimental reductions of the microbiome during embryonic and larval stages effectively reduced microbial richness, diversity and altered community composition in tadpoles prior to metamorphosis. In addition, our antimicrobial treatments resulted in few negative effects on larval development, body condition, or survival to metamorphosis. However, contrary to our predictions, our antimicrobial treatments did not alter susceptibility to the lethal fungal pathogen Batrachochytrium dendrobatidis (Bd) in the adult life stage. While our treatments to reduce the microbiome during early development did not play a critical role in determining susceptibility to disease caused by Bd in X. laevis, they nevertheless indicate that developing a gnotobiotic amphibian model system may be highly useful for future immunological investigations. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’.
format Online
Article
Text
id pubmed-10258664
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher The Royal Society
record_format MEDLINE/PubMed
spelling pubmed-102586642023-06-13 Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system Miller, Abigail J. Gass, Jordan Jo, Myung Chul Bishop, Lucas Petereit, Juli Woodhams, Douglas C. Voyles, Jamie Philos Trans R Soc Lond B Biol Sci Articles The immune equilibrium model suggests that exposure to microbes during early life primes immune responses for pathogen exposure later in life. While recent studies using a range of gnotobiotic (germ-free) model organisms offer support for this theory, we currently lack a tractable model system for investigating the influence of the microbiome on immune system development. Here, we used an amphibian species (Xenopus laevis) to investigate the importance of the microbiome in larval development and susceptibility to infectious disease later in life. We found that experimental reductions of the microbiome during embryonic and larval stages effectively reduced microbial richness, diversity and altered community composition in tadpoles prior to metamorphosis. In addition, our antimicrobial treatments resulted in few negative effects on larval development, body condition, or survival to metamorphosis. However, contrary to our predictions, our antimicrobial treatments did not alter susceptibility to the lethal fungal pathogen Batrachochytrium dendrobatidis (Bd) in the adult life stage. While our treatments to reduce the microbiome during early development did not play a critical role in determining susceptibility to disease caused by Bd in X. laevis, they nevertheless indicate that developing a gnotobiotic amphibian model system may be highly useful for future immunological investigations. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’. The Royal Society 2023-07-31 2023-06-12 /pmc/articles/PMC10258664/ /pubmed/37305911 http://dx.doi.org/10.1098/rstb.2022.0125 Text en © 2023 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Miller, Abigail J.
Gass, Jordan
Jo, Myung Chul
Bishop, Lucas
Petereit, Juli
Woodhams, Douglas C.
Voyles, Jamie
Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
title Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
title_full Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
title_fullStr Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
title_full_unstemmed Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
title_short Towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
title_sort towards the generation of gnotobiotic larvae as a tool to investigate the influence of the microbiome on the development of the amphibian immune system
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10258664/
https://www.ncbi.nlm.nih.gov/pubmed/37305911
http://dx.doi.org/10.1098/rstb.2022.0125
work_keys_str_mv AT millerabigailj towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem
AT gassjordan towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem
AT jomyungchul towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem
AT bishoplucas towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem
AT petereitjuli towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem
AT woodhamsdouglasc towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem
AT voylesjamie towardsthegenerationofgnotobioticlarvaeasatooltoinvestigatetheinfluenceofthemicrobiomeonthedevelopmentoftheamphibianimmunesystem