Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social in
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RESEARCH ARTICLE
Open Access
Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect Matteo Antoine Negroni1†, Francisca H. I. D. Segers1,2,3†, Fanny Vogelweith1,4 and Susanne Foitzik1*
Abstract Background: The gut microbiome can influence life history traits associated with host fitness such as fecundity and longevity. In most organisms, these two life history traits are traded-off, while they are positively linked in social insects. In ants, highly fecund queens can live for decades, while their non-reproducing workers exhibit much shorter lifespans. Yet, when fertility is induced in workers by death or removal of the queen, worker lifespan can increase. It is unclear how this positive link between fecundity and longevity is achieved and what role the gut microbiome and the immune system play in this. To gain insights into the molecular regulation of lifespan in social insects, we investigated fat body gene expression and gut microbiome composition in workers of the ant Temnothorax rugatulus in response to an experimental induction of fertility and an immune challenge. Results: Fertile workers upregulated several molecular repair mechanisms, which could explain their extended lifespan. The immune challenge altered the expression of several thousand genes in the fat body, including many immune genes, and, interestingly, this transcriptomic response depended on worker fertility. For example, only fertile, immunechallenged workers upregulated genes involved in the synthesis of alpha-ketoglutarate, an immune system regulator, which extends the lifespan in Caenorhabditis elegans by down-regulating the TOR pathway and reducing oxidant production. Additionally, we observed a dramatic loss in bacterial diversity in the guts of the ants within a day of the immune challenge. Yet, bacterial density did not change, so that the gut microbiomes of many immune challenged workers consisted of only a single or a few bacterial strains. Moreover, the expression of immune genes was linked to the gut microbiome composition, suggesting that the ant host can regulate the microbiome in its gut. Conclusions: Immune system flare-ups can have negative consequence on gut microbiome diversity, pointing to a previously underrated cost of immunity. Moreover, our results provide important insights into shifts in the molecular regulation of fertility and longevity associated with insect sociality. Keywords: Immunity, Gut microbiome, Fecundity, Aging, Senescence, Longevity, Social insects
* Correspondence: [email protected] † Matteo Antoine Negroni and Francisca H. I. D. Segers contributed equally to this work. 1 Institute of Molecular and Organismic Evolution, Johannes Gutenberg University, Hanns-Dieter-Hüsch-Weg 15, 55128 Mainz, Germany Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, dis
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