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Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps

Trained immunity is the enhanced response of the innate immune system to a secondary infection after an initial encounter with a microorganism. This non-specific response to reinfection is a primitive form of adaptation that has been shown to be conserved from plants to mammals. Insects lack an acqu...

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Autores principales: Meriggi, Niccolò, Di Paola, Monica, Vitali, Francesco, Rivero, Damariz, Cappa, Federico, Turillazzi, Francesco, Gori, Agnese, Dapporto, Leonardo, Beani, Laura, Turillazzi, Stefano, Cavalieri, Duccio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6803456/
https://www.ncbi.nlm.nih.gov/pubmed/31681197
http://dx.doi.org/10.3389/fmicb.2019.02320
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author Meriggi, Niccolò
Di Paola, Monica
Vitali, Francesco
Rivero, Damariz
Cappa, Federico
Turillazzi, Francesco
Gori, Agnese
Dapporto, Leonardo
Beani, Laura
Turillazzi, Stefano
Cavalieri, Duccio
author_facet Meriggi, Niccolò
Di Paola, Monica
Vitali, Francesco
Rivero, Damariz
Cappa, Federico
Turillazzi, Francesco
Gori, Agnese
Dapporto, Leonardo
Beani, Laura
Turillazzi, Stefano
Cavalieri, Duccio
author_sort Meriggi, Niccolò
collection PubMed
description Trained immunity is the enhanced response of the innate immune system to a secondary infection after an initial encounter with a microorganism. This non-specific response to reinfection is a primitive form of adaptation that has been shown to be conserved from plants to mammals. Insects lack an acquired immune component and rely solely on an innate one, and they have expanded it upon traits of plasticity and adaptation against pathogens in the form of immune priming. The recent discoveries of the role of Saccharomyces cerevisiae in the insect’s ecology and the ability of this yeast to induce trained immunity in different organisms suggest that insects could have developed mechanisms of adaptation and immune enhancing. Here, we report that two yeast strains of S. cerevisiae, previously shown to induce trained immunity in mammals, enhance resistance to Escherichia coli infection in the paper wasp Polistes dominula. The reduction of injected E. coli load by S. cerevisiae strains was statistically significant in future foundresses but not in workers, and this occurs before and after hibernation. We thus investigated if the effect on E. coli was mirrored by variation in the gut microbiota composition. Foundresses, showing immune enhancing, had statistically significant changes in composition and diversity of gut bacterial communities but not in the fungal communities. Our results demonstrate that S. cerevisiae can prime insect responses against bacterial infections, providing an advantage to future foundress wasps to carry these microorganisms. Understanding the mechanisms involved in the generation of specific and long-lasting immune response against pathogenic infections in insects and the influence of the induction of trained immunity on the commensal gut microbiota could have a major impact on modern immunology.
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spelling pubmed-68034562019-11-03 Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps Meriggi, Niccolò Di Paola, Monica Vitali, Francesco Rivero, Damariz Cappa, Federico Turillazzi, Francesco Gori, Agnese Dapporto, Leonardo Beani, Laura Turillazzi, Stefano Cavalieri, Duccio Front Microbiol Microbiology Trained immunity is the enhanced response of the innate immune system to a secondary infection after an initial encounter with a microorganism. This non-specific response to reinfection is a primitive form of adaptation that has been shown to be conserved from plants to mammals. Insects lack an acquired immune component and rely solely on an innate one, and they have expanded it upon traits of plasticity and adaptation against pathogens in the form of immune priming. The recent discoveries of the role of Saccharomyces cerevisiae in the insect’s ecology and the ability of this yeast to induce trained immunity in different organisms suggest that insects could have developed mechanisms of adaptation and immune enhancing. Here, we report that two yeast strains of S. cerevisiae, previously shown to induce trained immunity in mammals, enhance resistance to Escherichia coli infection in the paper wasp Polistes dominula. The reduction of injected E. coli load by S. cerevisiae strains was statistically significant in future foundresses but not in workers, and this occurs before and after hibernation. We thus investigated if the effect on E. coli was mirrored by variation in the gut microbiota composition. Foundresses, showing immune enhancing, had statistically significant changes in composition and diversity of gut bacterial communities but not in the fungal communities. Our results demonstrate that S. cerevisiae can prime insect responses against bacterial infections, providing an advantage to future foundress wasps to carry these microorganisms. Understanding the mechanisms involved in the generation of specific and long-lasting immune response against pathogenic infections in insects and the influence of the induction of trained immunity on the commensal gut microbiota could have a major impact on modern immunology. Frontiers Media S.A. 2019-10-15 /pmc/articles/PMC6803456/ /pubmed/31681197 http://dx.doi.org/10.3389/fmicb.2019.02320 Text en Copyright © 2019 Meriggi, Di Paola, Vitali, Rivero, Cappa, Turillazzi, Gori, Dapporto, Beani, Turillazzi and Cavalieri. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Meriggi, Niccolò
Di Paola, Monica
Vitali, Francesco
Rivero, Damariz
Cappa, Federico
Turillazzi, Francesco
Gori, Agnese
Dapporto, Leonardo
Beani, Laura
Turillazzi, Stefano
Cavalieri, Duccio
Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps
title Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps
title_full Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps
title_fullStr Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps
title_full_unstemmed Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps
title_short Saccharomyces cerevisiae Induces Immune Enhancing and Shapes Gut Microbiota in Social Wasps
title_sort saccharomyces cerevisiae induces immune enhancing and shapes gut microbiota in social wasps
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6803456/
https://www.ncbi.nlm.nih.gov/pubmed/31681197
http://dx.doi.org/10.3389/fmicb.2019.02320
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