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Serotonin modulates insect gut bacterial community homeostasis

BACKGROUND: Metazoan guts are in permanent contact with microbial communities. However, the host mechanisms that have developed to manage the dynamic changes of these microorganisms and maintain homeostasis remain largely unknown. RESULTS: Serotonin (5-hydroxytryptamine [5-HT]) was found to modulate...

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Autores principales: Zeng, Tian, Su, Hong-ai, Liu, Ya-lan, Li, Jian-fang, Jiang, Ding-xin, Lu, Yong-yue, Qi, Yi-xiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9103294/
https://www.ncbi.nlm.nih.gov/pubmed/35550116
http://dx.doi.org/10.1186/s12915-022-01319-x
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author Zeng, Tian
Su, Hong-ai
Liu, Ya-lan
Li, Jian-fang
Jiang, Ding-xin
Lu, Yong-yue
Qi, Yi-xiang
author_facet Zeng, Tian
Su, Hong-ai
Liu, Ya-lan
Li, Jian-fang
Jiang, Ding-xin
Lu, Yong-yue
Qi, Yi-xiang
author_sort Zeng, Tian
collection PubMed
description BACKGROUND: Metazoan guts are in permanent contact with microbial communities. However, the host mechanisms that have developed to manage the dynamic changes of these microorganisms and maintain homeostasis remain largely unknown. RESULTS: Serotonin (5-hydroxytryptamine [5-HT]) was found to modulate gut microbiome homeostasis via regulation of a dual oxidase (Duox) gene expression in both Bactrocera dorsalis and Aedes aegypti. The knockdown of the peripheral 5-HT biosynthetic gene phenylalanine hydroxylase (TPH) increased the expression of Duox and the activity of reactive oxygen species, leading to a decrease in the gut microbiome load. Moreover, the TPH knockdown reduced the relative abundance of the bacterial genera Serratia and Providencia, including the opportunistic pathogens, S. marcescens and P. alcalifaciens in B. dorsalis. Treatment with 5-hydroxytryptophan, a precursor of 5-HT synthesis, fully rescued the TPH knockdown-induced phenotype. CONCLUSIONS: The findings reveal the important contribution of 5-HT in regulating gut homeostasis, providing new insights into gut–microbe interactions in metazoans. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01319-x.
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spelling pubmed-91032942022-05-14 Serotonin modulates insect gut bacterial community homeostasis Zeng, Tian Su, Hong-ai Liu, Ya-lan Li, Jian-fang Jiang, Ding-xin Lu, Yong-yue Qi, Yi-xiang BMC Biol Research Article BACKGROUND: Metazoan guts are in permanent contact with microbial communities. However, the host mechanisms that have developed to manage the dynamic changes of these microorganisms and maintain homeostasis remain largely unknown. RESULTS: Serotonin (5-hydroxytryptamine [5-HT]) was found to modulate gut microbiome homeostasis via regulation of a dual oxidase (Duox) gene expression in both Bactrocera dorsalis and Aedes aegypti. The knockdown of the peripheral 5-HT biosynthetic gene phenylalanine hydroxylase (TPH) increased the expression of Duox and the activity of reactive oxygen species, leading to a decrease in the gut microbiome load. Moreover, the TPH knockdown reduced the relative abundance of the bacterial genera Serratia and Providencia, including the opportunistic pathogens, S. marcescens and P. alcalifaciens in B. dorsalis. Treatment with 5-hydroxytryptophan, a precursor of 5-HT synthesis, fully rescued the TPH knockdown-induced phenotype. CONCLUSIONS: The findings reveal the important contribution of 5-HT in regulating gut homeostasis, providing new insights into gut–microbe interactions in metazoans. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01319-x. BioMed Central 2022-05-13 /pmc/articles/PMC9103294/ /pubmed/35550116 http://dx.doi.org/10.1186/s12915-022-01319-x 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 Article
Zeng, Tian
Su, Hong-ai
Liu, Ya-lan
Li, Jian-fang
Jiang, Ding-xin
Lu, Yong-yue
Qi, Yi-xiang
Serotonin modulates insect gut bacterial community homeostasis
title Serotonin modulates insect gut bacterial community homeostasis
title_full Serotonin modulates insect gut bacterial community homeostasis
title_fullStr Serotonin modulates insect gut bacterial community homeostasis
title_full_unstemmed Serotonin modulates insect gut bacterial community homeostasis
title_short Serotonin modulates insect gut bacterial community homeostasis
title_sort serotonin modulates insect gut bacterial community homeostasis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9103294/
https://www.ncbi.nlm.nih.gov/pubmed/35550116
http://dx.doi.org/10.1186/s12915-022-01319-x
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