Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host.
The concept of a holobiont, a host organism and its associated microbial communities, encapsulates the vital role the microbiome plays in the normal functioning of its host. Parasitic infections can disrupt this relationship, leading to dysbiosis. However, it is increasingly recognized that multicel...
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ftpubmed:35502903 2024-09-15T17:56:13+00:00 Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. Brealey, Jaelle C Lecaudey, Laurène A Kodama, Miyako Rasmussen, Jacob A Sveier, Harald Dheilly, Nolwenn M Martin, Michael D Limborg, Morten T 2022-06-28 https://doi.org/10.1128/mbio.00679-22 https://pubmed.ncbi.nlm.nih.gov/35502903 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239044/ eng eng Atypon https://doi.org/10.1128/mbio.00679-22 https://pubmed.ncbi.nlm.nih.gov/35502903 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239044/ mBio ISSN:2150-7511 Volume:13 Issue:3 Atlantic salmon Cestodes gut dysbiosis holobionts host-parasite-microbiome interactions intestinal microbiomes Journal Article Research Support, Non-U.S. Gov't 2022 ftpubmed https://doi.org/10.1128/mbio.00679-22 2024-08-30T16:03:00Z The concept of a holobiont, a host organism and its associated microbial communities, encapsulates the vital role the microbiome plays in the normal functioning of its host. Parasitic infections can disrupt this relationship, leading to dysbiosis. However, it is increasingly recognized that multicellular parasites are themselves holobionts. Intestinal parasites share space with the host gut microbiome, creating a system of nested microbiomes within the primary host. However, how the parasite, as a holobiont, interacts with the host holobiont remains unclear, as do the consequences of these interactions for host health. Here, we used 16S amplicon and shotgun metagenomics sequencing to characterize the microbiome of the intestinal cestode Eubothrium and its effect on the gut microbiome of its primary host, Atlantic salmon. Our results indicate that cestode infection is associated with salmon gut dysbiosis by acting as a selective force benefiting putative pathogens and potentially introducing novel bacterial species to the host. Our results suggest that parasitic cestodes may themselves be holobionts nested within the microbial community of their holobiont host, emphasizing the importance of also considering microbes associated with parasites when studying intestinal parasitic infections. IMPORTANCE The importance of the parasite microbiome is gaining recognition. Of particular concern is understanding how these parasite microbiomes influence host-parasite interactions and parasite interactions with the vertebrate host microbiome as part of a system of nested holobionts. However, there are still relatively few studies focusing on the microbiome of parasitic helminths in general and almost none on cestodes in particular, despite the significant burden of disease caused by these parasites globally. Our study provides insights into a system of significance to the aquaculture industry, cestode infections of Atlantic salmon and, more broadly, expands our general understanding of parasite-microbiome-host interactions and introduces a new element, the microbiome of the parasite itself, which may play a critical role in modulating the host microbiome, and, therefore, the host response, to parasite infection. Article in Journal/Newspaper Atlantic salmon PubMed Central (PMC) mBio 13 3 |
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Open Polar |
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PubMed Central (PMC) |
op_collection_id |
ftpubmed |
language |
English |
topic |
Atlantic salmon Cestodes gut dysbiosis holobionts host-parasite-microbiome interactions intestinal microbiomes |
spellingShingle |
Atlantic salmon Cestodes gut dysbiosis holobionts host-parasite-microbiome interactions intestinal microbiomes Brealey, Jaelle C Lecaudey, Laurène A Kodama, Miyako Rasmussen, Jacob A Sveier, Harald Dheilly, Nolwenn M Martin, Michael D Limborg, Morten T Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. |
topic_facet |
Atlantic salmon Cestodes gut dysbiosis holobionts host-parasite-microbiome interactions intestinal microbiomes |
description |
The concept of a holobiont, a host organism and its associated microbial communities, encapsulates the vital role the microbiome plays in the normal functioning of its host. Parasitic infections can disrupt this relationship, leading to dysbiosis. However, it is increasingly recognized that multicellular parasites are themselves holobionts. Intestinal parasites share space with the host gut microbiome, creating a system of nested microbiomes within the primary host. However, how the parasite, as a holobiont, interacts with the host holobiont remains unclear, as do the consequences of these interactions for host health. Here, we used 16S amplicon and shotgun metagenomics sequencing to characterize the microbiome of the intestinal cestode Eubothrium and its effect on the gut microbiome of its primary host, Atlantic salmon. Our results indicate that cestode infection is associated with salmon gut dysbiosis by acting as a selective force benefiting putative pathogens and potentially introducing novel bacterial species to the host. Our results suggest that parasitic cestodes may themselves be holobionts nested within the microbial community of their holobiont host, emphasizing the importance of also considering microbes associated with parasites when studying intestinal parasitic infections. IMPORTANCE The importance of the parasite microbiome is gaining recognition. Of particular concern is understanding how these parasite microbiomes influence host-parasite interactions and parasite interactions with the vertebrate host microbiome as part of a system of nested holobionts. However, there are still relatively few studies focusing on the microbiome of parasitic helminths in general and almost none on cestodes in particular, despite the significant burden of disease caused by these parasites globally. Our study provides insights into a system of significance to the aquaculture industry, cestode infections of Atlantic salmon and, more broadly, expands our general understanding of parasite-microbiome-host interactions and introduces a new element, the microbiome of the parasite itself, which may play a critical role in modulating the host microbiome, and, therefore, the host response, to parasite infection. |
format |
Article in Journal/Newspaper |
author |
Brealey, Jaelle C Lecaudey, Laurène A Kodama, Miyako Rasmussen, Jacob A Sveier, Harald Dheilly, Nolwenn M Martin, Michael D Limborg, Morten T |
author_facet |
Brealey, Jaelle C Lecaudey, Laurène A Kodama, Miyako Rasmussen, Jacob A Sveier, Harald Dheilly, Nolwenn M Martin, Michael D Limborg, Morten T |
author_sort |
Brealey, Jaelle C |
title |
Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. |
title_short |
Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. |
title_full |
Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. |
title_fullStr |
Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. |
title_full_unstemmed |
Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host. |
title_sort |
microbiome "inception": an intestinal cestode shapes a hierarchy of microbial communities nested within the host. |
publisher |
Atypon |
publishDate |
2022 |
url |
https://doi.org/10.1128/mbio.00679-22 https://pubmed.ncbi.nlm.nih.gov/35502903 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239044/ |
genre |
Atlantic salmon |
genre_facet |
Atlantic salmon |
op_source |
mBio ISSN:2150-7511 Volume:13 Issue:3 |
op_relation |
https://doi.org/10.1128/mbio.00679-22 https://pubmed.ncbi.nlm.nih.gov/35502903 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9239044/ |
op_doi |
https://doi.org/10.1128/mbio.00679-22 |
container_title |
mBio |
container_volume |
13 |
container_issue |
3 |
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1810432423713832960 |