Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity

Social immune behaviors are described in a great variety of insect societies and their role in preventing emerging infectious diseases has become a major topic in insect research. The social immune system consists of multiple layers, ranging from the synthesis of external immune molecules to the coo...

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Main Authors: M. Alejandra Esparza-Mora, Hannah E. Davis, Stefania Meconcelli, Rudy Plarre, Dino P. McMahon
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Ecology and Evolution
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fevo.2020.00075/full
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author M. Alejandra Esparza-Mora
M. Alejandra Esparza-Mora
Hannah E. Davis
Stefania Meconcelli
Rudy Plarre
Dino P. McMahon
Dino P. McMahon
author_facet M. Alejandra Esparza-Mora
M. Alejandra Esparza-Mora
Hannah E. Davis
Stefania Meconcelli
Rudy Plarre
Dino P. McMahon
Dino P. McMahon
author_sort M. Alejandra Esparza-Mora
collection DOAJ
description Social immune behaviors are described in a great variety of insect societies and their role in preventing emerging infectious diseases has become a major topic in insect research. The social immune system consists of multiple layers, ranging from the synthesis of external immune molecules to the coordination of individual behaviors into sophisticated collective defensive tasks. But our understanding of how complex group-level behavioral defenses are orchestrated has remained limited. We sought to address this gap in knowledge by investigating the relationship between the external activity of an important immune effector molecule in termites, Gram negative binding protein 2 (GNBP-2) and collective grooming and cannibalism. We reasoned that as an external enzyme capable of degrading entomopathogenic fungi, GNBP-2 can facilitate the spread of pathogenic molecules in the colony, and thus serve to trigger collective defenses in a manner analogous to pathogen-associated molecular signatures (PAMPs) of the individual immune system. To test whether GNBP-2 could play a role in regulating social immune behavior, we experimentally inhibited its fungicidal activity using the glycomimetic molecule, D-d-gluconolactone (GDL) and recorded collective behavioral responses to an infected nestmate. Contrary to expectations, GNBP-2 inhibition did not influence the rate or intensity of grooming of either control or fungus-infected nestmates. By contrast, we found that the probability of being harmed through defensive cannibalistic behaviors was significantly reduced by the inhibition of GNBP-2. Our findings indicate that the regulation of collective immune behaviors may depend in part on the external secretion of an enzyme originating from the individual immune system, but that other cues are also necessary.
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spelling doaj.art-b865a000ad254796af3d99c9f1bae7f12022-12-21T18:58:45ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2020-04-01810.3389/fevo.2020.00075506918Inhibition of a Secreted Immune Molecule Interferes With Termite Social ImmunityM. Alejandra Esparza-Mora0M. Alejandra Esparza-Mora1Hannah E. Davis2Stefania Meconcelli3Rudy Plarre4Dino P. McMahon5Dino P. McMahon6Institut für Biologie, Freie Universität Berlin, Berlin, GermanyAbteilung 4 Material und Umwelt, Bundesanstalt f r Materialforschung und -prüfung (BAM), Berlin, GermanyDepartment of Biology, Carleton University, Ottawa, ON, CanadaAbteilung 4 Material und Umwelt, Bundesanstalt f r Materialforschung und -prüfung (BAM), Berlin, GermanyAbteilung 4 Material und Umwelt, Bundesanstalt f r Materialforschung und -prüfung (BAM), Berlin, GermanyInstitut für Biologie, Freie Universität Berlin, Berlin, GermanyAbteilung 4 Material und Umwelt, Bundesanstalt f r Materialforschung und -prüfung (BAM), Berlin, GermanySocial immune behaviors are described in a great variety of insect societies and their role in preventing emerging infectious diseases has become a major topic in insect research. The social immune system consists of multiple layers, ranging from the synthesis of external immune molecules to the coordination of individual behaviors into sophisticated collective defensive tasks. But our understanding of how complex group-level behavioral defenses are orchestrated has remained limited. We sought to address this gap in knowledge by investigating the relationship between the external activity of an important immune effector molecule in termites, Gram negative binding protein 2 (GNBP-2) and collective grooming and cannibalism. We reasoned that as an external enzyme capable of degrading entomopathogenic fungi, GNBP-2 can facilitate the spread of pathogenic molecules in the colony, and thus serve to trigger collective defenses in a manner analogous to pathogen-associated molecular signatures (PAMPs) of the individual immune system. To test whether GNBP-2 could play a role in regulating social immune behavior, we experimentally inhibited its fungicidal activity using the glycomimetic molecule, D-d-gluconolactone (GDL) and recorded collective behavioral responses to an infected nestmate. Contrary to expectations, GNBP-2 inhibition did not influence the rate or intensity of grooming of either control or fungus-infected nestmates. By contrast, we found that the probability of being harmed through defensive cannibalistic behaviors was significantly reduced by the inhibition of GNBP-2. Our findings indicate that the regulation of collective immune behaviors may depend in part on the external secretion of an enzyme originating from the individual immune system, but that other cues are also necessary.https://www.frontiersin.org/article/10.3389/fevo.2020.00075/fulltermitesocial immunitycannibalismhygienic behaviorGNBP-2GDL
spellingShingle M. Alejandra Esparza-Mora
M. Alejandra Esparza-Mora
Hannah E. Davis
Stefania Meconcelli
Rudy Plarre
Dino P. McMahon
Dino P. McMahon
Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity
Frontiers in Ecology and Evolution
termite
social immunity
cannibalism
hygienic behavior
GNBP-2
GDL
title Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity
title_full Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity
title_fullStr Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity
title_full_unstemmed Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity
title_short Inhibition of a Secreted Immune Molecule Interferes With Termite Social Immunity
title_sort inhibition of a secreted immune molecule interferes with termite social immunity
topic termite
social immunity
cannibalism
hygienic behavior
GNBP-2
GDL
url https://www.frontiersin.org/article/10.3389/fevo.2020.00075/full
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