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Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor

Transgenerational immune priming (TGIP) is an intriguing form of parental care which leads to the plastic adjustment of the progeny’s immunity according to parental immune experience. Such parental effect has been described in several vertebrate and invertebrate taxa. However, very few empirical stu...

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Autores principales: Bernier, Clémentine, Boidin-Wichlacz, Céline, Tasiemski, Aurélie, Hautekèete, Nina, Massol, François, Cuvillier-Hot, Virginie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6947409/
https://www.ncbi.nlm.nih.gov/pubmed/31805627
http://dx.doi.org/10.3390/genes10120989
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author Bernier, Clémentine
Boidin-Wichlacz, Céline
Tasiemski, Aurélie
Hautekèete, Nina
Massol, François
Cuvillier-Hot, Virginie
author_facet Bernier, Clémentine
Boidin-Wichlacz, Céline
Tasiemski, Aurélie
Hautekèete, Nina
Massol, François
Cuvillier-Hot, Virginie
author_sort Bernier, Clémentine
collection PubMed
description Transgenerational immune priming (TGIP) is an intriguing form of parental care which leads to the plastic adjustment of the progeny’s immunity according to parental immune experience. Such parental effect has been described in several vertebrate and invertebrate taxa. However, very few empirical studies have been conducted from the field, with natural host-parasite systems and real ecological settings, especially in invertebrates. We investigated TGIP in wild populations of the marine annelid Hediste diversicolor. Females laid eggs in a mud tube and thus shared the local microbial threats with the first developmental stages, thus meeting expectations for the evolution of TGIP. We evidenced that a maternal bacterial challenge led to the higher antibacterial defense of the produced oocytes, with higher efficiency in the case of Gram-positive bacterial challenge, pointing out a prevalent role of these bacteria in the evolutionary history of TGIP in this species. Underlying mechanisms might involve the antimicrobial peptide hedistin that was detected in the cytoplasm of oocytes and whose mRNAs were selectively stored in higher quantity in mature oocytes, after a maternal immune challenge. Finally, maternal immune transfer was significantly inhibited in females living in polluted areas, suggesting associated costs and the possible trade-off with female’s protection.
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spelling pubmed-69474092020-01-13 Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor Bernier, Clémentine Boidin-Wichlacz, Céline Tasiemski, Aurélie Hautekèete, Nina Massol, François Cuvillier-Hot, Virginie Genes (Basel) Article Transgenerational immune priming (TGIP) is an intriguing form of parental care which leads to the plastic adjustment of the progeny’s immunity according to parental immune experience. Such parental effect has been described in several vertebrate and invertebrate taxa. However, very few empirical studies have been conducted from the field, with natural host-parasite systems and real ecological settings, especially in invertebrates. We investigated TGIP in wild populations of the marine annelid Hediste diversicolor. Females laid eggs in a mud tube and thus shared the local microbial threats with the first developmental stages, thus meeting expectations for the evolution of TGIP. We evidenced that a maternal bacterial challenge led to the higher antibacterial defense of the produced oocytes, with higher efficiency in the case of Gram-positive bacterial challenge, pointing out a prevalent role of these bacteria in the evolutionary history of TGIP in this species. Underlying mechanisms might involve the antimicrobial peptide hedistin that was detected in the cytoplasm of oocytes and whose mRNAs were selectively stored in higher quantity in mature oocytes, after a maternal immune challenge. Finally, maternal immune transfer was significantly inhibited in females living in polluted areas, suggesting associated costs and the possible trade-off with female’s protection. MDPI 2019-12-01 /pmc/articles/PMC6947409/ /pubmed/31805627 http://dx.doi.org/10.3390/genes10120989 Text en © 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Bernier, Clémentine
Boidin-Wichlacz, Céline
Tasiemski, Aurélie
Hautekèete, Nina
Massol, François
Cuvillier-Hot, Virginie
Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
title Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
title_full Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
title_fullStr Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
title_full_unstemmed Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
title_short Transgenerational Immune Priming in the Field: Maternal Environmental Experience Leads to Differential Immune Transfer to Oocytes in the Marine Annelid Hediste diversicolor
title_sort transgenerational immune priming in the field: maternal environmental experience leads to differential immune transfer to oocytes in the marine annelid hediste diversicolor
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6947409/
https://www.ncbi.nlm.nih.gov/pubmed/31805627
http://dx.doi.org/10.3390/genes10120989
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