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      Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria

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          Abstract

          In insects, a complex and effective immune system that can be rapidly activated by a plethora of stimuli has evolved. Although the main cellular and humoral mechanisms and their activation pathways are highly conserved across insects, the timing and the efficacy of triggered immune responses can differ among different species. In this scenario, an insect deserving particular attention is the black soldier fly (BSF), Hermetia illucens (Diptera: Stratiomyidae). Indeed, BSF larvae can be reared on a wide range of decaying organic substrates and, thanks to their high protein and lipid content, they represent a valuable source of macromolecules useful for different applications (e.g., production of feedstuff, bioplastics, and biodiesel), thus contributing to the development of circular economy supply chains for waste valorization. However, decaying substrates bring the larvae into contact with different potential pathogens that can challenge their health status and growth. Although these life strategies have presumably contributed to shape the evolution of a sophisticated and efficient immune system in this dipteran, knowledge about its functional features is still fragmentary. In the present study, we investigated the processes underpinning the immune response to bacteria in H. illucens larvae and characterized their reaction times. Our data demonstrate that the cellular and humoral responses in this insect show different kinetics: phagocytosis and encapsulation are rapidly triggered after the immune challenge, while the humoral components intervene later. Moreover, although both Gram-positive and Gram-negative bacteria are completely removed from the insect body within a few hours after injection, Gram-positive bacteria persist in the hemolymph longer than do Gram-negative bacteria. Finally, the activity of two key actors of the humoral response, i.e., lysozyme and phenoloxidase, show unusual dynamics as compared to other insects. This study represents the first detailed characterization of the immune response to bacteria of H. illucens larvae, expanding knowledge on the defense mechanisms of this insect among Diptera. This information is a prerequisite to manipulating the larval immune response by nutritional and environmental factors to increase resistance to pathogens and optimize health status during mass rearing.

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          Most cited references105

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          Immune pathways and defence mechanisms in honey bees Apis mellifera

          Social insects are able to mount both group-level and individual defences against pathogens. Here we focus on individual defences, by presenting a genome-wide analysis of immunity in a social insect, the honey bee Apis mellifera. We present honey bee models for each of four signalling pathways associated with immunity, identifying plausible orthologues for nearly all predicted pathway members. When compared to the sequenced Drosophila and Anopheles genomes, honey bees possess roughly one-third as many genes in 17 gene families implicated in insect immunity. We suggest that an implied reduction in immune flexibility in bees reflects either the strength of social barriers to disease, or a tendency for bees to be attacked by a limited set of highly coevolved pathogens.
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            From bacterial killing to immune modulation: Recent insights into the functions of lysozyme

            Lysozyme is a cornerstone of innate immunity. The canonical mechanism for bacterial killing by lysozyme occurs through the hydrolysis of cell wall peptidoglycan (PG). Conventional type (c-type) lysozymes are also highly cationic and can kill certain bacteria independently of PG hydrolytic activity. Reflecting the ongoing arms race between host and invading microorganisms, both gram-positive and gram-negative bacteria have evolved mechanisms to thwart killing by lysozyme. In addition to its direct antimicrobial role, more recent evidence has shown that lysozyme modulates the host immune response to infection. The degradation and lysis of bacteria by lysozyme enhance the release of bacterial products, including PG, that activate pattern recognition receptors in host cells. Yet paradoxically, lysozyme is important for the resolution of inflammation at mucosal sites. This review will highlight recent advances in our understanding of the diverse mechanisms that bacteria use to protect themselves against lysozyme, the intriguing immunomodulatory function of lysozyme, and the relationship between these features in the context of infection.
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              Nutritional composition of black soldier fly (Hermetia illucens) prepupae reared on different organic waste substrates.

              Black soldier fly larvae are converters of organic waste into edible biomass, of which the composition may depend on the substrate. In this study, larvae were grown on four substrates: chicken feed, vegetable waste, biogas digestate, and restaurant waste. Samples of prepupae and substrates were freeze-dried and proximate, amino acid, fatty acid and mineral analyses were performed.
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                Author and article information

                Contributors
                Journal
                Front Immunol
                Front Immunol
                Front. Immunol.
                Frontiers in Immunology
                Frontiers Media S.A.
                1664-3224
                18 November 2021
                2021
                : 12
                : 745160
                Affiliations
                [1] 1 Laboratory of Invertebrate Biology, Department of Biotechnology and Life Sciences, University of Insubria , Varese, Italy
                [2] 2 Laboratory of Comparative Immunology, Department of Theoretical and Applied Sciences, University of Insubria , Varese, Italy
                [3] 3 Laboratory of Insect Biochemistry and Molecular Sciences, Department of Entomology, Faculty of Science, Cairo University , Giza, Egypt
                [4] 4 Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding, Guangdong Provincial Sericulture and Mulberry Engineering Research Center, College of Animal Science, South China Agricultural University , Guangzhou, China
                [5] 5 Laboratory of Insect Physiology and Biotechnology, Department of Biosciences, University of Milano , Milan, Italy
                [6] 6 Interuniversity Center for Studies on Bioinspired Agro-Environmental Technology (BAT Center), University of Napoli Federico II , Naples, Italy
                Author notes

                Edited by: Ioannis Eleftherianos, George Washington University, United States

                Reviewed by: Javad Karimi, Ferdowsi University of Mashhad, Iran; Jorge Contreras-Garduño, National Autonomous University of Mexico, Mexico

                *Correspondence: Gianluca Tettamanti, gianluca.tettamanti@ 123456uninsubria.it

                †These authors have contributed equally to this work

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

                Article
                10.3389/fimmu.2021.745160
                8636706
                34867970
                eefc81bf-9ab9-4c50-a5b8-fff6b17c9084
                Copyright © 2021 Bruno, Montali, Mastore, Brivio, Mohamed, Tian, Grimaldi, Casartelli and Tettamanti

                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
                : 21 July 2021
                : 01 November 2021
                Page count
                Figures: 8, Tables: 2, Equations: 0, References: 105, Pages: 17, Words: 8217
                Funding
                Funded by: Fondazione Cariplo , doi 10.13039/501100002803;
                Award ID: 2020-0900
                Categories
                Immunology
                Original Research

                Immunology
                cellular response,hemocytes,hermetia illucens,humoral response,immune system
                Immunology
                cellular response, hemocytes, hermetia illucens, humoral response, immune system

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