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

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 dif...

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Autores principales: Bruno, Daniele, Montali, Aurora, Mastore, Maristella, Brivio, Maurizio Francesco, Mohamed, Amr, Tian, Ling, Grimaldi, Annalisa, Casartelli, Morena, Tettamanti, Gianluca
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8636706/
https://www.ncbi.nlm.nih.gov/pubmed/34867970
http://dx.doi.org/10.3389/fimmu.2021.745160
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author Bruno, Daniele
Montali, Aurora
Mastore, Maristella
Brivio, Maurizio Francesco
Mohamed, Amr
Tian, Ling
Grimaldi, Annalisa
Casartelli, Morena
Tettamanti, Gianluca
author_facet Bruno, Daniele
Montali, Aurora
Mastore, Maristella
Brivio, Maurizio Francesco
Mohamed, Amr
Tian, Ling
Grimaldi, Annalisa
Casartelli, Morena
Tettamanti, Gianluca
author_sort Bruno, Daniele
collection PubMed
description 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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spelling pubmed-86367062021-12-03 Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria Bruno, Daniele Montali, Aurora Mastore, Maristella Brivio, Maurizio Francesco Mohamed, Amr Tian, Ling Grimaldi, Annalisa Casartelli, Morena Tettamanti, Gianluca Front Immunol Immunology 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. Frontiers Media S.A. 2021-11-18 /pmc/articles/PMC8636706/ /pubmed/34867970 http://dx.doi.org/10.3389/fimmu.2021.745160 Text en Copyright © 2021 Bruno, Montali, Mastore, Brivio, Mohamed, Tian, Grimaldi, Casartelli and Tettamanti https://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 Immunology
Bruno, Daniele
Montali, Aurora
Mastore, Maristella
Brivio, Maurizio Francesco
Mohamed, Amr
Tian, Ling
Grimaldi, Annalisa
Casartelli, Morena
Tettamanti, Gianluca
Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria
title Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria
title_full Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria
title_fullStr Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria
title_full_unstemmed Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria
title_short Insights Into the Immune Response of the Black Soldier Fly Larvae to Bacteria
title_sort insights into the immune response of the black soldier fly larvae to bacteria
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8636706/
https://www.ncbi.nlm.nih.gov/pubmed/34867970
http://dx.doi.org/10.3389/fimmu.2021.745160
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