Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor

Type Article
Date 2020-10
Language English
Author(s) Tetreau Guillaume1, Dhinaut Julien2, Galinier Richard7, Audant-Lacour Pascaline3, Voisin Sébastien N4, Arafah Karim4, Chogne Manon2, Hilliou Frédérique3, Bordes Anaïs1, Sabarly Camille2, Chan Philippe5, Walet-Balieu Marie-Laure5, Vaudry David5, Duval David1, Bulet Philippe4, 6, Coustau Christine3, Moret Yannick2, Gourbal Benjamin1
Affiliation(s) 1 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, France
2 : Equipe Ecologie Evolutive, UMR CNRS 6282 BioGeoSciences, Universite Bourgogne-Franche Comte, Dijon, France
3 : CNRS, INRAE, Universite´ Nice Coˆte d’Azur, UMR 1355–7254 Institut Sophia Agrobiotech, Sophia Antipolis, France
4 : Plateforme BioPark d’Archamps, ArchParc, Saint Julien en Genevois, France
5 : PISSARO Proteomic Platform, Institute for Research and Innovation in Biomedicine, University of Rouen, Rouen, France
6 : CR Universite Grenoble Alpes, Institute for Advanced Biosciences, INSERM U1209, CNRS UMR5309, La Tronche, France
7 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, Perpignan, France
Source Plos Pathogens (1553-7366) (Public Library of Science (PLoS)), 2020-10 , Vol. 16 , N. 10 , P. e1008935 (30p.)
DOI 10.1371/journal.ppat.1008935
WOS© Times Cited 1
Abstract

In a number of species, individuals exposed to pathogens can mount an immune response and transmit this immunological experience to their offspring, thereby protecting them against persistent threats. Such vertical transfer of immunity, named trans-generational immune priming (TGIP), has been described in both vertebrates and invertebrates. Although increasingly studied during the last decade, the mechanisms underlying TGIP in invertebrates are still elusive, especially those protecting the earliest offspring life stage, i.e. the embryo developing in the egg. In the present study, we combined different proteomic and transcriptomic approaches to determine whether mothers transfer a “signal” (such as fragments of infecting bacteria), mRNA and/or protein/peptide effectors to protect their eggs against two natural bacterial pathogens, namely the Gram-positive Bacillus thuringiensis and the Gram-negative Serratia entomophila. By taking the mealworm beetle Tenebrio molitor as a biological model, our results suggest that eggs are mainly protected by an active direct transfer of a restricted number of immune proteins and of antimicrobial peptides. In contrast, the present data do not support the involvement of mRNA transfer while the transmission of a “signal”, if it happens, is marginal and only occurs within 24h after maternal exposure to bacteria. This work exemplifies how combining global approaches helps to disentangle the different scenarios of a complex trait, providing a comprehensive characterization of TGIP mechanisms in T. molitor. It also paves the way for future alike studies focusing on TGIP in a wide range of invertebrates and vertebrates to identify additional candidates that could be specific to TGIP and to investigate whether the TGIP mechanisms found herein are specific or common to all insect species.

Author summary

 

All living organisms are regularly exposed to a wide and diverse range of pathogens. To protect themselves, many species have developed an immune system able to detect and eradicate these pathogens. Most interestingly, this immunological experience can be transferred by parents to their offspring to protect them from pathogens that may persist in the environment and to which they could be exposed during their life. While extensively studied in vertebrates, this phenomenon–called trans-generational immune priming (TGIP)–has only been identified a decade ago in invertebrates and the supporting molecular mechanisms are still largely unknown. Recently, we proposed four different scenarios as a practical framework to investigate the mechanisms supporting this complex phenomenon. In the present study, we combined different molecular approaches to disentangle these different scenarios and provide a comprehensive characterization of maternal TGIP mechanisms in a model insect, the mealworm beetle Tenebrio molitor.

Full Text
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Publisher's official version 30 2 MB Open access
S1 Fig. Representative examples of variations in AMPs expression levels in primed adult females exposed to dsRNA 1 MB Open access
S1 Table. Selected families of proteins involved in immune and stress responses. 117 KB Open access
S2 Table. List of manually annotated cytochrome P450. 54 KB Open access
S3 Table. List of the proteins identified for each spot differentially abundant in the 2D-DiGE analysis. 34 KB Open access
S4 Table. Proteome Discoverer report of the proteins identified in the five egg samples. 3 MB Open access
S5 Table. Identified peptides in egg samples for the AMP proteins presented in Table 3. 22 KB Open access
S6 Table. Details of the priming dates, females used and eggs sampled for each experiment. 32 KB Open access
S7 Table. List of the primers used for the RT-qPCR experiment. 14 KB Open access
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How to cite 

Tetreau Guillaume, Dhinaut Julien, Galinier Richard, Audant-Lacour Pascaline, Voisin Sébastien N, Arafah Karim, Chogne Manon, Hilliou Frédérique, Bordes Anaïs, Sabarly Camille, Chan Philippe, Walet-Balieu Marie-Laure, Vaudry David, Duval David, Bulet Philippe, Coustau Christine, Moret Yannick, Gourbal Benjamin (2020). Deciphering the molecular mechanisms of mother-to-egg immune protection in the mealworm beetle Tenebrio molitor. Plos Pathogens, 16(10), e1008935 (30p.). Publisher's official version : https://doi.org/10.1371/journal.ppat.1008935 , Open Access version : https://archimer.ifremer.fr/doc/00655/76684/