Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect
- Publikationstyp:
- Zeitschriftenaufsatz
- Metadaten:
-
- Autoren
- Matteo Antoine Negroni
- Francisca HID Segers
- Fanny Vogelweith
- Susanne Foitzik
- Autoren-URL
- https://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=fis-test-1&SrcAuth=WosAPI&KeyUT=WOS:000595710900006&DestLinkType=FullRecord&DestApp=WOS_CPL
- DOI
- 10.1186/s12864-020-07191-9
- Externe Identifier
- Clarivate Analytics Document Solution ID: PA5YN
- PubMed Identifier: 33225893
- ISSN
- 1471-2164
- Ausgabe der Veröffentlichung
- 1
- Zeitschrift
- BMC GENOMICS
- Schlüsselwörter
- Immunity
- Gut microbiome
- Fecundity
- Aging
- Senescence
- Longevity
- Social insects
- Artikelnummer
- ARTN 816
- Datum der Veröffentlichung
- 2020
- Status
- Published
- Titel
- Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect
- Sub types
- Article
- Ausgabe der Zeitschrift
- 21
Datenquelle: Web of Science (Lite)
- Andere Metadatenquellen:
-
- Abstract
- <jats:title>Abstract</jats:title><jats:sec><jats:title>Background</jats:title><jats:p>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<jats:italic>Temnothorax rugatulus</jats:italic>in response to an experimental induction of fertility and an immune challenge.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>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, immune-challenged workers upregulated genes involved in the synthesis of<jats:italic>alpha-ketoglutarate</jats:italic>, an immune system regulator, which extends the lifespan in<jats:italic>Caenorhabditis elegans</jats:italic>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.</jats:p></jats:sec><jats:sec><jats:title>Conclusions</jats:title><jats:p>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.</jats:p></jats:sec>
- Autoren
- Matteo Antoine Negroni
- Francisca HID Segers
- Fanny Vogelweith
- Susanne Foitzik
- DOI
- 10.1186/s12864-020-07191-9
- eISSN
- 1471-2164
- Ausgabe der Veröffentlichung
- 1
- Zeitschrift
- BMC Genomics
- Sprache
- en
- Artikelnummer
- 816
- Online publication date
- 2020
- Datum der Veröffentlichung
- 2020
- Status
- Published
- Herausgeber
- Springer Science and Business Media LLC
- Herausgeber URL
- http://dx.doi.org/10.1186/s12864-020-07191-9
- Datum der Datenerfassung
- 2021
- Titel
- Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect
- Ausgabe der Zeitschrift
- 21
Datenquelle: Crossref
- Abstract
- <h4>Background</h4>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.<h4>Results</h4>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, immune-challenged 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.<h4>Conclusions</h4>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.
- Addresses
- Institute of Molecular and Organismic Evolution, Johannes Gutenberg University, Hanns-Dieter-Hüsch-Weg 15, 55128, Mainz, Germany.
- Autoren
- Matteo Antoine Negroni
- Francisca HID Segers
- Fanny Vogelweith
- Susanne Foitzik
- DOI
- 10.1186/s12864-020-07191-9
- eISSN
- 1471-2164
- Externe Identifier
- PubMed Identifier: 33225893
- PubMed Central ID: PMC7682046
- Funding acknowledgements
- Deutsche Forschungsgemeinschaft: FO 298/19-1
- Open access
- true
- ISSN
- 1471-2164
- Ausgabe der Veröffentlichung
- 1
- Zeitschrift
- BMC genomics
- Schlüsselwörter
- Animals
- Humans
- Ants
- Social Behavior
- Longevity
- Fertility
- Gastrointestinal Microbiome
- Sprache
- eng
- Medium
- Electronic
- Online publication date
- 2020
- Open access status
- Open Access
- Paginierung
- 816
- Datum der Veröffentlichung
- 2020
- Status
- Published
- Publisher licence
- CC BY
- Datum der Datenerfassung
- 2020
- Titel
- Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect.
- Sub types
- research-article
- Journal Article
- Ausgabe der Zeitschrift
- 21
Files
https://bmcgenomics.biomedcentral.com/track/pdf/10.1186/s12864-020-07191-9 https://europepmc.org/articles/PMC7682046?pdf=render
Datenquelle: Europe PubMed Central
- 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, immune-challenged 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.
- Date of acceptance
- 2020
- Autoren
- Matteo Antoine Negroni
- Francisca HID Segers
- Fanny Vogelweith
- Susanne Foitzik
- Autoren-URL
- https://www.ncbi.nlm.nih.gov/pubmed/33225893
- DOI
- 10.1186/s12864-020-07191-9
- eISSN
- 1471-2164
- Externe Identifier
- PubMed Central ID: PMC7682046
- Funding acknowledgements
- Deutsche Forschungsgemeinschaft: FO 298/19-1
- Ausgabe der Veröffentlichung
- 1
- Zeitschrift
- BMC Genomics
- Schlüsselwörter
- Aging
- Fecundity
- Gut microbiome
- Immunity
- Longevity
- Senescence
- Social insects
- Animals
- Ants
- Fertility
- Gastrointestinal Microbiome
- Humans
- Longevity
- Social Behavior
- Sprache
- eng
- Country
- England
- Paginierung
- 816
- PII
- 10.1186/s12864-020-07191-9
- Datum der Veröffentlichung
- 2020
- Status
- Published online
- Datum, an dem der Datensatz öffentlich gemacht wurde
- 2021
- Titel
- Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect.
- Sub types
- Journal Article
- Ausgabe der Zeitschrift
- 21
Datenquelle: PubMed
- Author's licence
- CC-BY
- Autoren
- Matteo Antoine Negroni
- Francisca HID Segers
- Fanny Vogelweith
- Susanne Foitzik
- Hosting institution
- Universitätsbibliothek Mainz
- Sammlungen
- JGU-Publikationen
- Resource version
- Published version
- DOI
- 10.1186/s12864-020-07191-9
- File(s) embargoed
- false
- Open access
- true
- ISSN
- 1471-2164
- Zeitschrift
- BMC genomics
- Schlüsselwörter
- 570 Biowissenschaften
- 570 Life sciences
- Sprache
- eng
- Open access status
- Open Access
- Paginierung
- 816
- Datum der Veröffentlichung
- 2020
- Public URL
- https://openscience.ub.uni-mainz.de/handle/20.500.12030/5800
- Herausgeber
- BioMed Central
- Herausgeber URL
- https://doi.org/10.1186/s12864-020-07191-9
- Datum der Datenerfassung
- 2021
- Datum, an dem der Datensatz öffentlich gemacht wurde
- 2021
- Zugang
- Public
- Titel
- Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect
- Ausgabe der Zeitschrift
- 21
Files
negroni_matteo...-immune_challen-20210421123124230.pdf
Datenquelle: OPENSCIENCE.UB
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