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A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival

BACKGROUND: Commensal microorganisms have a significant impact on the physiology of host animals, including Drosophila. Lactobacillus and Acetobacter, the two most common commensal bacteria in Drosophila, stimulate fly development and growth, but the mechanisms underlying their functional interactio...

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Autores principales: Lee, Jaegeun, Yun, Hyun Myoung, Han, Gangsik, Lee, Gang Jun, Jeon, Che Ok, Hyun, Seogang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9670437/
https://www.ncbi.nlm.nih.gov/pubmed/36397042
http://dx.doi.org/10.1186/s12915-022-01458-1
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author Lee, Jaegeun
Yun, Hyun Myoung
Han, Gangsik
Lee, Gang Jun
Jeon, Che Ok
Hyun, Seogang
author_facet Lee, Jaegeun
Yun, Hyun Myoung
Han, Gangsik
Lee, Gang Jun
Jeon, Che Ok
Hyun, Seogang
author_sort Lee, Jaegeun
collection PubMed
description BACKGROUND: Commensal microorganisms have a significant impact on the physiology of host animals, including Drosophila. Lactobacillus and Acetobacter, the two most common commensal bacteria in Drosophila, stimulate fly development and growth, but the mechanisms underlying their functional interactions remain elusive. RESULTS: We found that imaginal morphogenesis protein-Late 2 (Imp-L2), a Drosophila homolog of insulin-like growth factor binding protein 7, is expressed in gut enterocytes in a bacteria-dependent manner, determining host dependence on specific bacteria for host development. Imp-L2 mutation abolished the stimulatory effects of Lactobacillus, but not of Acetobacter, on fly larval development. The lethality of the Imp-L2 mutant markedly increased under axenic conditions, which was reversed by Acetobacter, but not Lactobacillus, re-association. The host dependence on specific bacteria was determined by Imp-L2 expressed in enterocytes, which was repressed by Acetobacter, but not Lactobacillus. Mechanistically, Lactobacillus and Acetobacter differentially affected steroid hormone-mediated Imp-L2 expression and Imp-L2-specific FOXO regulation. CONCLUSIONS: Our finding may provide a way how host switches dependence between different bacterial species when benefiting from varying microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01458-1.
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spelling pubmed-96704372022-11-18 A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival Lee, Jaegeun Yun, Hyun Myoung Han, Gangsik Lee, Gang Jun Jeon, Che Ok Hyun, Seogang BMC Biol Research Article BACKGROUND: Commensal microorganisms have a significant impact on the physiology of host animals, including Drosophila. Lactobacillus and Acetobacter, the two most common commensal bacteria in Drosophila, stimulate fly development and growth, but the mechanisms underlying their functional interactions remain elusive. RESULTS: We found that imaginal morphogenesis protein-Late 2 (Imp-L2), a Drosophila homolog of insulin-like growth factor binding protein 7, is expressed in gut enterocytes in a bacteria-dependent manner, determining host dependence on specific bacteria for host development. Imp-L2 mutation abolished the stimulatory effects of Lactobacillus, but not of Acetobacter, on fly larval development. The lethality of the Imp-L2 mutant markedly increased under axenic conditions, which was reversed by Acetobacter, but not Lactobacillus, re-association. The host dependence on specific bacteria was determined by Imp-L2 expressed in enterocytes, which was repressed by Acetobacter, but not Lactobacillus. Mechanistically, Lactobacillus and Acetobacter differentially affected steroid hormone-mediated Imp-L2 expression and Imp-L2-specific FOXO regulation. CONCLUSIONS: Our finding may provide a way how host switches dependence between different bacterial species when benefiting from varying microbiota. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-022-01458-1. BioMed Central 2022-11-17 /pmc/articles/PMC9670437/ /pubmed/36397042 http://dx.doi.org/10.1186/s12915-022-01458-1 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
Lee, Jaegeun
Yun, Hyun Myoung
Han, Gangsik
Lee, Gang Jun
Jeon, Che Ok
Hyun, Seogang
A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
title A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
title_full A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
title_fullStr A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
title_full_unstemmed A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
title_short A bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
title_sort bacteria-regulated gut peptide determines host dependence on specific bacteria to support host juvenile development and survival
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9670437/
https://www.ncbi.nlm.nih.gov/pubmed/36397042
http://dx.doi.org/10.1186/s12915-022-01458-1
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