Cargando…

Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity

The microbiome has a crucial influence on host phenotype and is of broad interest to ecological and evolutionary research. Yet, the extent of variation that occurs in the microbiome within and between populations is unclear. We characterized the skin and gut microbiomes of seven populations of juven...

Descripción completa

Detalles Bibliográficos
Autores principales: Uren Webster, Tamsyn M., Consuegra, Sofia, Hitchings, Matthew, Garcia de Leaniz, Carlos
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6070748/
https://www.ncbi.nlm.nih.gov/pubmed/29915104
http://dx.doi.org/10.1128/AEM.00691-18
_version_ 1783343728431202304
author Uren Webster, Tamsyn M.
Consuegra, Sofia
Hitchings, Matthew
Garcia de Leaniz, Carlos
author_facet Uren Webster, Tamsyn M.
Consuegra, Sofia
Hitchings, Matthew
Garcia de Leaniz, Carlos
author_sort Uren Webster, Tamsyn M.
collection PubMed
description The microbiome has a crucial influence on host phenotype and is of broad interest to ecological and evolutionary research. Yet, the extent of variation that occurs in the microbiome within and between populations is unclear. We characterized the skin and gut microbiomes of seven populations of juvenile Atlantic salmon (Salmo salar) inhabiting a diverse range of environments, including hatchery-reared and wild populations. We found shared skin operational taxonomic units (OTUs) across all populations and core gut microbiota for all wild fish, but the diversity and structure of both skin and gut microbial communities were distinct between populations. There was a marked difference between the gut microbiomes of wild and captive fish. Hatchery-reared fish had lower intestinal microbial diversity, lacked core microbiota found in wild fish, and showed altered community structure and function. Skin and gut microbiomes were also less varied within captive populations, reflecting more uniform artificial rearing conditions. The surrounding water influenced the microbiome of the gut and, especially, the skin, but could not explain the degree of variation observed between populations. For both gut and skin, we found that there was greater difference in microbiome structures between more genetically distinct fish populations, and that population genetic diversity was positively correlated with microbiome diversity. However, diet is likely to be the major factor contributing to the large differences in gut microbiota between wild and captive fish. Our results highlight the scope of interpopulation variation in the Atlantic salmon microbiome and offer insights into the deterministic factors contributing to microbiome diversity and structure. IMPORTANCE Variation in the microbiome has a fundamental influence on host health, ecology, and evolution, but the scope and basis of this variation are not fully understood. We identified considerable variation in skin and gut microbial communities between seven wild and captive populations of Atlantic salmon, reflecting divergent environmental conditions and fish genetic diversity. In particular, we found very pronounced differences in the intestinal microbiomes of wild and hatchery-reared fish, likely reflecting differences in diet. Our results offer an insight into how the microbiome potentially contributes to the generation of local adaptations in this species and how domestication alters intestinal microbial communities, highlighting future research directions in these areas.
format Online
Article
Text
id pubmed-6070748
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-60707482018-08-16 Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity Uren Webster, Tamsyn M. Consuegra, Sofia Hitchings, Matthew Garcia de Leaniz, Carlos Appl Environ Microbiol Microbial Ecology The microbiome has a crucial influence on host phenotype and is of broad interest to ecological and evolutionary research. Yet, the extent of variation that occurs in the microbiome within and between populations is unclear. We characterized the skin and gut microbiomes of seven populations of juvenile Atlantic salmon (Salmo salar) inhabiting a diverse range of environments, including hatchery-reared and wild populations. We found shared skin operational taxonomic units (OTUs) across all populations and core gut microbiota for all wild fish, but the diversity and structure of both skin and gut microbial communities were distinct between populations. There was a marked difference between the gut microbiomes of wild and captive fish. Hatchery-reared fish had lower intestinal microbial diversity, lacked core microbiota found in wild fish, and showed altered community structure and function. Skin and gut microbiomes were also less varied within captive populations, reflecting more uniform artificial rearing conditions. The surrounding water influenced the microbiome of the gut and, especially, the skin, but could not explain the degree of variation observed between populations. For both gut and skin, we found that there was greater difference in microbiome structures between more genetically distinct fish populations, and that population genetic diversity was positively correlated with microbiome diversity. However, diet is likely to be the major factor contributing to the large differences in gut microbiota between wild and captive fish. Our results highlight the scope of interpopulation variation in the Atlantic salmon microbiome and offer insights into the deterministic factors contributing to microbiome diversity and structure. IMPORTANCE Variation in the microbiome has a fundamental influence on host health, ecology, and evolution, but the scope and basis of this variation are not fully understood. We identified considerable variation in skin and gut microbial communities between seven wild and captive populations of Atlantic salmon, reflecting divergent environmental conditions and fish genetic diversity. In particular, we found very pronounced differences in the intestinal microbiomes of wild and hatchery-reared fish, likely reflecting differences in diet. Our results offer an insight into how the microbiome potentially contributes to the generation of local adaptations in this species and how domestication alters intestinal microbial communities, highlighting future research directions in these areas. American Society for Microbiology 2018-08-01 /pmc/articles/PMC6070748/ /pubmed/29915104 http://dx.doi.org/10.1128/AEM.00691-18 Text en Copyright © 2018 Uren Webster et al. https://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Microbial Ecology
Uren Webster, Tamsyn M.
Consuegra, Sofia
Hitchings, Matthew
Garcia de Leaniz, Carlos
Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity
title Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity
title_full Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity
title_fullStr Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity
title_full_unstemmed Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity
title_short Interpopulation Variation in the Atlantic Salmon Microbiome Reflects Environmental and Genetic Diversity
title_sort interpopulation variation in the atlantic salmon microbiome reflects environmental and genetic diversity
topic Microbial Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6070748/
https://www.ncbi.nlm.nih.gov/pubmed/29915104
http://dx.doi.org/10.1128/AEM.00691-18
work_keys_str_mv AT urenwebstertamsynm interpopulationvariationintheatlanticsalmonmicrobiomereflectsenvironmentalandgeneticdiversity
AT consuegrasofia interpopulationvariationintheatlanticsalmonmicrobiomereflectsenvironmentalandgeneticdiversity
AT hitchingsmatthew interpopulationvariationintheatlanticsalmonmicrobiomereflectsenvironmentalandgeneticdiversity
AT garciadeleanizcarlos interpopulationvariationintheatlanticsalmonmicrobiomereflectsenvironmentalandgeneticdiversity