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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...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2019
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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. |
format | Online Article Text |
id | pubmed-6803456 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
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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