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Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding

BACKGROUND: The ability of animals and their microbiomes to adapt to starvation and then restore homeostasis after refeeding is fundamental to their continued survival and symbiosis. The intestine is the primary site of nutrient absorption and microbiome interaction, however our understanding of int...

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Autores principales: Jawahar, Jayanth, McCumber, Alexander W., Lickwar, Colin R., Amoroso, Caroline R., de la Torre Canny, Sol Gomez, Wong, Sandi, Morash, Margaret, Thierer, James H., Farber, Steven A., Bohannan, Brendan J. M., Guillemin, Karen, Rawls, John F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8941736/
https://www.ncbi.nlm.nih.gov/pubmed/35317738
http://dx.doi.org/10.1186/s12864-022-08447-2
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author Jawahar, Jayanth
McCumber, Alexander W.
Lickwar, Colin R.
Amoroso, Caroline R.
de la Torre Canny, Sol Gomez
Wong, Sandi
Morash, Margaret
Thierer, James H.
Farber, Steven A.
Bohannan, Brendan J. M.
Guillemin, Karen
Rawls, John F.
author_facet Jawahar, Jayanth
McCumber, Alexander W.
Lickwar, Colin R.
Amoroso, Caroline R.
de la Torre Canny, Sol Gomez
Wong, Sandi
Morash, Margaret
Thierer, James H.
Farber, Steven A.
Bohannan, Brendan J. M.
Guillemin, Karen
Rawls, John F.
author_sort Jawahar, Jayanth
collection PubMed
description BACKGROUND: The ability of animals and their microbiomes to adapt to starvation and then restore homeostasis after refeeding is fundamental to their continued survival and symbiosis. The intestine is the primary site of nutrient absorption and microbiome interaction, however our understanding of intestinal adaptations to starvation and refeeding remains limited. Here we used RNA sequencing and 16S rRNA gene sequencing to uncover changes in the intestinal transcriptome and microbiome of zebrafish subjected to long-term starvation and refeeding compared to continuously fed controls. RESULTS: Starvation over 21 days led to increased diversity and altered composition in the intestinal microbiome compared to fed controls, including relative increases in Vibrio and reductions in Plesiomonas bacteria. Starvation also led to significant alterations in host gene expression in the intestine, with distinct pathways affected at early and late stages of starvation. This included increases in the expression of ribosome biogenesis genes early in starvation, followed by decreased expression of genes involved in antiviral immunity and lipid transport at later stages. These effects of starvation on the host transcriptome and microbiome were almost completely restored within 3 days after refeeding. Comparison with published datasets identified host genes responsive to starvation as well as high-fat feeding or microbiome colonization, and predicted host transcription factors that may be involved in starvation response. CONCLUSIONS: Long-term starvation induces progressive changes in microbiome composition and host gene expression in the zebrafish intestine, and these changes are rapidly reversed after refeeding. Our identification of bacterial taxa, host genes and host pathways involved in this response provides a framework for future investigation of the physiological and ecological mechanisms underlying intestinal adaptations to food restriction. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08447-2.
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spelling pubmed-89417362022-03-24 Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding Jawahar, Jayanth McCumber, Alexander W. Lickwar, Colin R. Amoroso, Caroline R. de la Torre Canny, Sol Gomez Wong, Sandi Morash, Margaret Thierer, James H. Farber, Steven A. Bohannan, Brendan J. M. Guillemin, Karen Rawls, John F. BMC Genomics Research BACKGROUND: The ability of animals and their microbiomes to adapt to starvation and then restore homeostasis after refeeding is fundamental to their continued survival and symbiosis. The intestine is the primary site of nutrient absorption and microbiome interaction, however our understanding of intestinal adaptations to starvation and refeeding remains limited. Here we used RNA sequencing and 16S rRNA gene sequencing to uncover changes in the intestinal transcriptome and microbiome of zebrafish subjected to long-term starvation and refeeding compared to continuously fed controls. RESULTS: Starvation over 21 days led to increased diversity and altered composition in the intestinal microbiome compared to fed controls, including relative increases in Vibrio and reductions in Plesiomonas bacteria. Starvation also led to significant alterations in host gene expression in the intestine, with distinct pathways affected at early and late stages of starvation. This included increases in the expression of ribosome biogenesis genes early in starvation, followed by decreased expression of genes involved in antiviral immunity and lipid transport at later stages. These effects of starvation on the host transcriptome and microbiome were almost completely restored within 3 days after refeeding. Comparison with published datasets identified host genes responsive to starvation as well as high-fat feeding or microbiome colonization, and predicted host transcription factors that may be involved in starvation response. CONCLUSIONS: Long-term starvation induces progressive changes in microbiome composition and host gene expression in the zebrafish intestine, and these changes are rapidly reversed after refeeding. Our identification of bacterial taxa, host genes and host pathways involved in this response provides a framework for future investigation of the physiological and ecological mechanisms underlying intestinal adaptations to food restriction. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08447-2. BioMed Central 2022-03-22 /pmc/articles/PMC8941736/ /pubmed/35317738 http://dx.doi.org/10.1186/s12864-022-08447-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Jawahar, Jayanth
McCumber, Alexander W.
Lickwar, Colin R.
Amoroso, Caroline R.
de la Torre Canny, Sol Gomez
Wong, Sandi
Morash, Margaret
Thierer, James H.
Farber, Steven A.
Bohannan, Brendan J. M.
Guillemin, Karen
Rawls, John F.
Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
title Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
title_full Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
title_fullStr Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
title_full_unstemmed Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
title_short Starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
title_sort starvation causes changes in the intestinal transcriptome and microbiome that are reversed upon refeeding
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8941736/
https://www.ncbi.nlm.nih.gov/pubmed/35317738
http://dx.doi.org/10.1186/s12864-022-08447-2
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