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

PLoS Pathog. 2020 Oct 15;16(10):e1008935. doi: 10.1371/journal.ppat.1008935. eCollection 2020 Oct.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bacillus thuringiensis / pathogenicity
  • Bacterial Infections / immunology*
  • Immunity / immunology
  • Larva / microbiology*
  • Ovum / immunology*
  • Proteomics / methods
  • Serratia / pathogenicity*
  • Tenebrio / immunology
  • Tenebrio / microbiology*

Supplementary concepts

  • Serratia entomophila

Grants and funding

This work was funded by the MATER-IMMUNITY Project (ANR-14-CE02-0009) from the French National Research Agency (ANR; https://anr.fr/) granted to YM, BG and CC. The PISSARO Proteomic Platform gets funding from Normandy Region (https://www.normandie.fr/) and ERDF (https://www.enedis.fr/). Peptidomics and a part of proteomics studies were funded by the R&D budget from the Plateforme BioPark d’Archamps (http://www.biopark-archamps.org/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.