Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Arias-Rojas, Aranzazu, Frahm, Dagmar, Hurwitz, Robert, Brinkmann, Volker, Iatsenko, Igor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
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
_version_ 1785102420326481920
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
work_keys_str_mv AT ariasrojasaranzazu resistancetohostantimicrobialpeptidesmediatesresilienceofgutcommensalsduringinfectionandagingindrosophila
AT frahmdagmar resistancetohostantimicrobialpeptidesmediatesresilienceofgutcommensalsduringinfectionandagingindrosophila
AT hurwitzrobert resistancetohostantimicrobialpeptidesmediatesresilienceofgutcommensalsduringinfectionandagingindrosophila
AT brinkmannvolker resistancetohostantimicrobialpeptidesmediatesresilienceofgutcommensalsduringinfectionandagingindrosophila
AT iatsenkoigor resistancetohostantimicrobialpeptidesmediatesresilienceofgutcommensalsduringinfectionandagingindrosophila