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Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila
Resilience to short-term perturbations, like inflammation, is a fundamental feature of microbiota, yet the underlying mechanisms of microbiota resilience are incompletely understood. Here, we show that Lactiplantibacillus plantarum, a major Drosophila commensal, stably colonizes the fruit fly gut du...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10483595/ https://www.ncbi.nlm.nih.gov/pubmed/37639605 http://dx.doi.org/10.1073/pnas.2305649120 |
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author | Arias-Rojas, Aranzazu Frahm, Dagmar Hurwitz, Robert Brinkmann, Volker Iatsenko, Igor |
author_facet | Arias-Rojas, Aranzazu Frahm, Dagmar Hurwitz, Robert Brinkmann, Volker Iatsenko, Igor |
author_sort | Arias-Rojas, Aranzazu |
collection | PubMed |
description | Resilience to short-term perturbations, like inflammation, is a fundamental feature of microbiota, yet the underlying mechanisms of microbiota resilience are incompletely understood. Here, we show that Lactiplantibacillus plantarum, a major Drosophila commensal, stably colonizes the fruit fly gut during infection and is resistant to Drosophila antimicrobial peptides (AMPs). By transposon screening, we identified L. plantarum mutants sensitive to AMPs. These mutants were impaired in peptidoglycan O-acetylation or teichoic acid D-alanylation, resulting in increased negative cell surface charge and higher affinity to cationic AMPs. AMP-sensitive mutants were cleared from the gut after infection and aging-induced gut inflammation in wild-type, but not in AMP-deficient flies, suggesting that resistance to host AMPs is essential for commensal resilience in an inflamed gut environment. Thus, our work reveals that in addition to the host immune tolerance to the microbiota, commensal-encoded resilience mechanisms are necessary to maintain the stable association between host and microbiota during inflammation. |
format | Online Article Text |
id | pubmed-10483595 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-104835952023-09-08 Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila Arias-Rojas, Aranzazu Frahm, Dagmar Hurwitz, Robert Brinkmann, Volker Iatsenko, Igor Proc Natl Acad Sci U S A Biological Sciences Resilience to short-term perturbations, like inflammation, is a fundamental feature of microbiota, yet the underlying mechanisms of microbiota resilience are incompletely understood. Here, we show that Lactiplantibacillus plantarum, a major Drosophila commensal, stably colonizes the fruit fly gut during infection and is resistant to Drosophila antimicrobial peptides (AMPs). By transposon screening, we identified L. plantarum mutants sensitive to AMPs. These mutants were impaired in peptidoglycan O-acetylation or teichoic acid D-alanylation, resulting in increased negative cell surface charge and higher affinity to cationic AMPs. AMP-sensitive mutants were cleared from the gut after infection and aging-induced gut inflammation in wild-type, but not in AMP-deficient flies, suggesting that resistance to host AMPs is essential for commensal resilience in an inflamed gut environment. Thus, our work reveals that in addition to the host immune tolerance to the microbiota, commensal-encoded resilience mechanisms are necessary to maintain the stable association between host and microbiota during inflammation. National Academy of Sciences 2023-08-28 2023-09-05 /pmc/articles/PMC10483595/ /pubmed/37639605 http://dx.doi.org/10.1073/pnas.2305649120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Biological Sciences Arias-Rojas, Aranzazu Frahm, Dagmar Hurwitz, Robert Brinkmann, Volker Iatsenko, Igor Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila |
title | Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila |
title_full | Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila |
title_fullStr | Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila |
title_full_unstemmed | Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila |
title_short | Resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in Drosophila |
title_sort | resistance to host antimicrobial peptides mediates resilience of gut commensals during infection and aging in drosophila |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10483595/ https://www.ncbi.nlm.nih.gov/pubmed/37639605 http://dx.doi.org/10.1073/pnas.2305649120 |
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