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

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          Abstract

          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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          Most cited references34

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          AMPLIFICATION AND DIRECT SEQUENCING OF FUNGAL RIBOSOMAL RNA GENES FOR PHYLOGENETICS

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            Population genomics of domestic and wild yeasts

            Since the completion of the genome sequence of Saccharomyces cerevisiae in 19961,2, there has been an exponential increase in complete genome sequences accompanied by great advances in our understanding of genome evolution. Although little is known about the natural and life histories of yeasts in the wild, there are an increasing number of studies looking at ecological and geographic distributions3,4, population structure5-8, and sexual versus asexual reproduction9,10. Less well understood at the whole genome level are the evolutionary processes acting within populations and species leading to adaptation to different environments, phenotypic differences and reproductive isolation. Here we present one- to four-fold or more coverage of the genome sequences of over seventy isolates of the baker's yeast, S. cerevisiae, and its closest relative, S. paradoxus. We examine variation in gene content, SNPs, indels, copy numbers and transposable elements. We find that phenotypic variation broadly correlates with global genome-wide phylogenetic relationships. Interestingly, S. paradoxus populations are well delineated along geographic boundaries while the variation among worldwide S. cerevisiae isolates shows less differentiation and is comparable to a single S. paradoxus population. Rather than one or two domestication events leading to the extant baker's yeasts, the population structure of S. cerevisiae consists of a few well-defined geographically isolated lineages and many different mosaics of these lineages, supporting the idea that human influence provided the opportunity for cross-breeding and production of new combinations of pre-existing variation.
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              Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes.

              Immunological memory in vertebrates is often exclusively attributed to T and B cell function. Recently it was proposed that the enhanced and sustained innate immune responses following initial infectious exposure may also afford protection against reinfection. Testing this concept of "trained immunity," we show that mice lacking functional T and B lymphocytes are protected against reinfection with Candida albicans in a monocyte-dependent manner. C. albicans and fungal cell wall β-glucans induced functional reprogramming of monocytes, leading to enhanced cytokine production in vivo and in vitro. The training required the β-glucan receptor dectin-1 and the noncanonical Raf-1 pathway. Monocyte training by β-glucans was associated with stable changes in histone trimethylation at H3K4, which suggests the involvement of epigenetic mechanisms in this phenomenon. The functional reprogramming of monocytes, reminiscent of similar NK cell properties, supports the concept of "trained immunity" and may be employed for the design of improved vaccination strategies. Copyright © 2012 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                15 October 2019
                2019
                : 10
                : 2320
                Affiliations
                [1] 1Dipartimento di Biologia, Università degli Studi di Firenze , Firenze, Italy
                [2] 2Istituto di Biologia e Biotecnologia Agraria, Consiglio Nazionale delle Ricerche , Pisa, Italy
                Author notes

                Edited by: Lia Danelishvili, Oregon State University, United States

                Reviewed by: Nathan T. Mortimer, Illinois State University, United States; Michael Poulsen, University of Copenhagen, Denmark

                *Correspondence: Stefano Turillazzi, stefano.turillazzi@ 123456unifi.it

                This article was submitted to Microbial Immunology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.02320
                6803456
                cbc122da-2224-4efb-b7ad-795e77d1138d
                Copyright © 2019 Meriggi, Di Paola, Vitali, Rivero, Cappa, Turillazzi, Gori, Dapporto, Beani, Turillazzi and Cavalieri.

                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.

                History
                : 10 June 2019
                : 23 September 2019
                Page count
                Figures: 7, Tables: 3, Equations: 0, References: 62, Pages: 14, Words: 0
                Funding
                Funded by: Università degli Studi di Firenze 10.13039/501100004434
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                innate immunity,immune training,saccharomyces cerevisiae,gut microbiota,polistes dominula

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