Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota

The microbiome is essential for development, health and homeostasis throughout an animal’s life. Yet, the origins and transmission processes governing animal microbiomes remain elusive for non-human vertebrates, oviparous vertebrates in particular. Eggs may function as transgenerational carriers of...

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Published in:The ISME Journal
Main Authors: van Veelen, H. Pieter J., Salles, Joana Falcão, Tieleman, B. Irene
Format: Text
Language:English
Published: Nature Publishing Group UK 2018
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932060/
http://www.ncbi.nlm.nih.gov/pubmed/29445132
https://doi.org/10.1038/s41396-018-0067-3
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spelling ftpubmed:oai:pubmedcentral.nih.gov:5932060 2023-05-15T13:10:06+02:00 Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota van Veelen, H. Pieter J. Salles, Joana Falcão Tieleman, B. Irene 2018-02-14 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932060/ http://www.ncbi.nlm.nih.gov/pubmed/29445132 https://doi.org/10.1038/s41396-018-0067-3 en eng Nature Publishing Group UK http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932060/ http://www.ncbi.nlm.nih.gov/pubmed/29445132 http://dx.doi.org/10.1038/s41396-018-0067-3 © International Society for Microbial Ecology 2018 Article Text 2018 ftpubmed https://doi.org/10.1038/s41396-018-0067-3 2019-05-05T00:13:55Z The microbiome is essential for development, health and homeostasis throughout an animal’s life. Yet, the origins and transmission processes governing animal microbiomes remain elusive for non-human vertebrates, oviparous vertebrates in particular. Eggs may function as transgenerational carriers of the maternal microbiome, warranting characterisation of egg microbiome assembly. Here, we investigated maternal and environmental contributions to avian eggshell microbiota in wild passerine birds: woodlark Lullula arborea and skylark Alauda arvensis. Using 16S rRNA gene sequencing, we demonstrated in both lark species, at the population and within-nest levels, that bacterial communities of freshly laid eggs were distinct from the female cloacal microbiome. Instead, soil-borne bacteria appeared to thrive on freshly laid eggs, and eggshell microbiota composition strongly resembled maternal skin, body feather and nest material communities, sources in direct contact with laid eggs. Finally, phylogenetic structure analysis and microbial source tracking underscored species sorting from directly contacting sources rather than in vivo-transferred symbionts. The female-egg-nest system allowed an integrative assessment of avian egg microbiome assembly, revealing mixed modes of symbiont acquisition not previously documented for vertebrate eggs. Our findings illuminated egg microbiome origins, which suggested a limited potential of eggshells for transgenerational transmission, encouraging further investigation of eggshell microbiome functions in vertebrates. Text Alauda arvensis PubMed Central (PMC) The ISME Journal 12 5 1375 1388
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Article
spellingShingle Article
van Veelen, H. Pieter J.
Salles, Joana Falcão
Tieleman, B. Irene
Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
topic_facet Article
description The microbiome is essential for development, health and homeostasis throughout an animal’s life. Yet, the origins and transmission processes governing animal microbiomes remain elusive for non-human vertebrates, oviparous vertebrates in particular. Eggs may function as transgenerational carriers of the maternal microbiome, warranting characterisation of egg microbiome assembly. Here, we investigated maternal and environmental contributions to avian eggshell microbiota in wild passerine birds: woodlark Lullula arborea and skylark Alauda arvensis. Using 16S rRNA gene sequencing, we demonstrated in both lark species, at the population and within-nest levels, that bacterial communities of freshly laid eggs were distinct from the female cloacal microbiome. Instead, soil-borne bacteria appeared to thrive on freshly laid eggs, and eggshell microbiota composition strongly resembled maternal skin, body feather and nest material communities, sources in direct contact with laid eggs. Finally, phylogenetic structure analysis and microbial source tracking underscored species sorting from directly contacting sources rather than in vivo-transferred symbionts. The female-egg-nest system allowed an integrative assessment of avian egg microbiome assembly, revealing mixed modes of symbiont acquisition not previously documented for vertebrate eggs. Our findings illuminated egg microbiome origins, which suggested a limited potential of eggshells for transgenerational transmission, encouraging further investigation of eggshell microbiome functions in vertebrates.
format Text
author van Veelen, H. Pieter J.
Salles, Joana Falcão
Tieleman, B. Irene
author_facet van Veelen, H. Pieter J.
Salles, Joana Falcão
Tieleman, B. Irene
author_sort van Veelen, H. Pieter J.
title Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
title_short Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
title_full Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
title_fullStr Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
title_full_unstemmed Microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
title_sort microbiome assembly of avian eggshells and their potential as transgenerational carriers of maternal microbiota
publisher Nature Publishing Group UK
publishDate 2018
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932060/
http://www.ncbi.nlm.nih.gov/pubmed/29445132
https://doi.org/10.1038/s41396-018-0067-3
genre Alauda arvensis
genre_facet Alauda arvensis
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5932060/
http://www.ncbi.nlm.nih.gov/pubmed/29445132
http://dx.doi.org/10.1038/s41396-018-0067-3
op_rights © International Society for Microbial Ecology 2018
op_doi https://doi.org/10.1038/s41396-018-0067-3
container_title The ISME Journal
container_volume 12
container_issue 5
container_start_page 1375
op_container_end_page 1388
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