<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance

ABSTRACT The gut microbiota affects the physiology and metabolism of animals and its alteration can lead to diseases such as gut dysplasia or metabolic disorders. Several reports have shown that the immune system plays an important role in shaping both bacterial community composition and abundance i...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	A. Marra, M. A. Hanson, S. Kondo, B. Erkosar, B. Lemaitre
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	microbiota innate immunity aging gnotobiotic animals immune effectors gut Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/60bab017b7a14f58839e71e821830946
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:60bab017b7a14f58839e71e821830946
record_format	dspace
spelling	oai:doaj.org-article:60bab017b7a14f58839e71e8218309462021-11-10T18:37:50Z<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance10.1128/mBio.00824-212150-7511https://doaj.org/article/60bab017b7a14f58839e71e8218309462021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00824-21https://doaj.org/toc/2150-7511ABSTRACT The gut microbiota affects the physiology and metabolism of animals and its alteration can lead to diseases such as gut dysplasia or metabolic disorders. Several reports have shown that the immune system plays an important role in shaping both bacterial community composition and abundance in Drosophila, and that immune deficit, especially during aging, negatively affects microbiota richness and diversity. However, there has been little study at the effector level to demonstrate how immune pathways regulate the microbiota. A key set of Drosophila immune effectors are the antimicrobial peptides (AMPs), which confer defense upon systemic infection. AMPs and lysozymes, a group of digestive enzymes with antimicrobial properties, are expressed in the gut and are good candidates for microbiota regulation. Here, we take advantage of the model organism Drosophila melanogaster to investigate the role of AMPs and lysozymes in regulation of gut microbiota structure and diversity. Using flies lacking AMPs and newly generated lysozyme mutants, we colonized gnotobiotic flies with a defined set of commensal bacteria and analyzed changes in microbiota composition and abundance in vertical transmission and aging contexts through 16S rRNA gene amplicon sequencing. Our study shows that AMPs and, to a lesser extent, lysozymes are necessary to regulate the total and relative abundance of bacteria in the gut microbiota. We also decouple the direct function of AMPs from the immune deficiency (IMD) signaling pathway that regulates AMPs but also many other processes, more narrowly defining the role of these effectors in the microbial dysbiosis observed in IMD-deficient flies upon aging. IMPORTANCE This study advances current knowledge in the field of host-microbe interactions by demonstrating that the two families of immune effectors, antimicrobial peptides and lysozymes, actively regulate the gut microbiota composition and abundance. Consequences of the loss of these antimicrobial peptides and lysozymes are exacerbated during aging, and their loss contributes to increased microbiota abundance and shifted composition in old flies. This work shows that immune effectors, typically associated with resistance to pathogenic infections, also help shape the beneficial gut community, consistent with the idea that host-symbiont interactions use the same “language” typically associated with pathogenesis.A. MarraM. A. HansonS. KondoB. ErkosarB. LemaitreAmerican Society for Microbiologyarticlemicrobiotainnate immunityaginggnotobiotic animalsimmune effectorsgutMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	microbiota innate immunity aging gnotobiotic animals immune effectors gut Microbiology QR1-502
spellingShingle	microbiota innate immunity aging gnotobiotic animals immune effectors gut Microbiology QR1-502 A. Marra M. A. Hanson S. Kondo B. Erkosar B. Lemaitre <italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance
description	ABSTRACT The gut microbiota affects the physiology and metabolism of animals and its alteration can lead to diseases such as gut dysplasia or metabolic disorders. Several reports have shown that the immune system plays an important role in shaping both bacterial community composition and abundance in Drosophila, and that immune deficit, especially during aging, negatively affects microbiota richness and diversity. However, there has been little study at the effector level to demonstrate how immune pathways regulate the microbiota. A key set of Drosophila immune effectors are the antimicrobial peptides (AMPs), which confer defense upon systemic infection. AMPs and lysozymes, a group of digestive enzymes with antimicrobial properties, are expressed in the gut and are good candidates for microbiota regulation. Here, we take advantage of the model organism Drosophila melanogaster to investigate the role of AMPs and lysozymes in regulation of gut microbiota structure and diversity. Using flies lacking AMPs and newly generated lysozyme mutants, we colonized gnotobiotic flies with a defined set of commensal bacteria and analyzed changes in microbiota composition and abundance in vertical transmission and aging contexts through 16S rRNA gene amplicon sequencing. Our study shows that AMPs and, to a lesser extent, lysozymes are necessary to regulate the total and relative abundance of bacteria in the gut microbiota. We also decouple the direct function of AMPs from the immune deficiency (IMD) signaling pathway that regulates AMPs but also many other processes, more narrowly defining the role of these effectors in the microbial dysbiosis observed in IMD-deficient flies upon aging. IMPORTANCE This study advances current knowledge in the field of host-microbe interactions by demonstrating that the two families of immune effectors, antimicrobial peptides and lysozymes, actively regulate the gut microbiota composition and abundance. Consequences of the loss of these antimicrobial peptides and lysozymes are exacerbated during aging, and their loss contributes to increased microbiota abundance and shifted composition in old flies. This work shows that immune effectors, typically associated with resistance to pathogenic infections, also help shape the beneficial gut community, consistent with the idea that host-symbiont interactions use the same “language” typically associated with pathogenesis.
format	article
author	A. Marra M. A. Hanson S. Kondo B. Erkosar B. Lemaitre
author_facet	A. Marra M. A. Hanson S. Kondo B. Erkosar B. Lemaitre
author_sort	A. Marra
title	<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance
title_short	<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance
title_full	<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance
title_fullStr	<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance
title_full_unstemmed	<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance
title_sort	<italic toggle="yes">drosophila</italic> antimicrobial peptides and lysozymes regulate gut microbiota composition and abundance
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/60bab017b7a14f58839e71e821830946
work_keys_str_mv	AT amarra italictoggleyesdrosophilaitalicantimicrobialpeptidesandlysozymesregulategutmicrobiotacompositionandabundance AT mahanson italictoggleyesdrosophilaitalicantimicrobialpeptidesandlysozymesregulategutmicrobiotacompositionandabundance AT skondo italictoggleyesdrosophilaitalicantimicrobialpeptidesandlysozymesregulategutmicrobiotacompositionandabundance AT berkosar italictoggleyesdrosophilaitalicantimicrobialpeptidesandlysozymesregulategutmicrobiotacompositionandabundance AT blemaitre italictoggleyesdrosophilaitalicantimicrobialpeptidesandlysozymesregulategutmicrobiotacompositionandabundance
_version_	1718439871817711616

<italic toggle="yes">Drosophila</italic> Antimicrobial Peptides and Lysozymes Regulate Gut Microbiota Composition and Abundance

Ejemplares similares