Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model

ABSTRACT A growing body of data suggests that the microbiome of a species can vary considerably from individual to individual, but the reasons for this variation—and the consequences for the ecology of these communities—remain only partially explained. In mammals, the emerging picture is that the me...

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Autores principales: Megan Taylor, N. M. Vega
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Publicado: American Society for Microbiology 2021
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Acceso en línea:https://doaj.org/article/d4157f8f658042d6a9890251d7714376
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spelling oai:doaj.org-article:d4157f8f658042d6a9890251d77143762021-12-02T19:22:27ZHost Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model10.1128/mSystems.00608-202379-5077https://doaj.org/article/d4157f8f658042d6a9890251d77143762021-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00608-20https://doaj.org/toc/2379-5077ABSTRACT A growing body of data suggests that the microbiome of a species can vary considerably from individual to individual, but the reasons for this variation—and the consequences for the ecology of these communities—remain only partially explained. In mammals, the emerging picture is that the metabolic state and immune system status of the host affect the composition of the microbiome, but quantitative ecological microbiome studies are challenging to perform in higher organisms. Here, we show that these phenomena can be quantitatively analyzed in the tractable nematode host Caenorhabditis elegans. Mutants in innate immunity, in particular the DAF-2/insulin growth factor (IGF) pathway, are shown to contain a microbiome that differs from that of wild-type nematodes. We analyzed the underlying basis of these differences from the perspective of community ecology by comparing experimental observations to the predictions of a neutral sampling model and concluded that fundamental differences in microbiome ecology underlie the observed differences in microbiome composition. We tested this hypothesis by introducing a minor perturbation into the colonization conditions, allowing us to assess stability of communities in different host strains. Our results show that altering host immunity changes the importance of interspecies interactions within the microbiome, resulting in differences in community composition and stability that emerge from these differences in host-microbe ecology. IMPORTANCE Here, we used a Caenorhabditis elegans microbiome model to demonstrate how genetic differences in innate immunity alter microbiome composition, diversity, and stability by changing the ecological processes that shape these communities. These results provide insight into the role of host genetics in controlling the ecology of the host-associated microbiota, resulting in differences in community composition, successional trajectories, and response to perturbation.Megan TaylorN. M. VegaAmerican Society for MicrobiologyarticleCaenorhabditis elegansimmunocompromised hostsmicrobial communitiesmicrobial ecologyMicrobiologyQR1-502ENmSystems, Vol 6, Iss 2 (2021)
institution DOAJ
collection DOAJ
language EN
topic Caenorhabditis elegans
immunocompromised hosts
microbial communities
microbial ecology
Microbiology
QR1-502
spellingShingle Caenorhabditis elegans
immunocompromised hosts
microbial communities
microbial ecology
Microbiology
QR1-502
Megan Taylor
N. M. Vega
Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model
description ABSTRACT A growing body of data suggests that the microbiome of a species can vary considerably from individual to individual, but the reasons for this variation—and the consequences for the ecology of these communities—remain only partially explained. In mammals, the emerging picture is that the metabolic state and immune system status of the host affect the composition of the microbiome, but quantitative ecological microbiome studies are challenging to perform in higher organisms. Here, we show that these phenomena can be quantitatively analyzed in the tractable nematode host Caenorhabditis elegans. Mutants in innate immunity, in particular the DAF-2/insulin growth factor (IGF) pathway, are shown to contain a microbiome that differs from that of wild-type nematodes. We analyzed the underlying basis of these differences from the perspective of community ecology by comparing experimental observations to the predictions of a neutral sampling model and concluded that fundamental differences in microbiome ecology underlie the observed differences in microbiome composition. We tested this hypothesis by introducing a minor perturbation into the colonization conditions, allowing us to assess stability of communities in different host strains. Our results show that altering host immunity changes the importance of interspecies interactions within the microbiome, resulting in differences in community composition and stability that emerge from these differences in host-microbe ecology. IMPORTANCE Here, we used a Caenorhabditis elegans microbiome model to demonstrate how genetic differences in innate immunity alter microbiome composition, diversity, and stability by changing the ecological processes that shape these communities. These results provide insight into the role of host genetics in controlling the ecology of the host-associated microbiota, resulting in differences in community composition, successional trajectories, and response to perturbation.
format article
author Megan Taylor
N. M. Vega
author_facet Megan Taylor
N. M. Vega
author_sort Megan Taylor
title Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model
title_short Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model
title_full Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model
title_fullStr Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model
title_full_unstemmed Host Immunity Alters Community Ecology and Stability of the Microbiome in a <named-content content-type="genus-species">Caenorhabditis elegans</named-content> Model
title_sort host immunity alters community ecology and stability of the microbiome in a <named-content content-type="genus-species">caenorhabditis elegans</named-content> model
publisher American Society for Microbiology
publishDate 2021
url https://doaj.org/article/d4157f8f658042d6a9890251d7714376
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