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

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 took the mealworm beetle Tenebrio molitor as a biological model, and 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 (Bt) and the Gram-negative Serratia entomophila (Se). We demonstrated 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 clearly reject 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 the power of combining global multidisciplinary approaches 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.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Tenebrio Molitor

TISSUE(S): Egg

SUBMITTER: Sebastien Voisin

LAB HEAD: Philippe Bulet

PROVIDER: PXD018772 | Pride | 2020-10-08

REPOSITORIES: Pride

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Project description:Slimming is globally prevalent especially in young women, and it may contribute to the metabolic health of their offspring. Whereas some Lamarckian ideas about environmental inheritance have been dismissed, increasing evidence suggest that certain acquired traits can be transmitted to the next generation. It is therefore of great interest to determine how and to what extent a maternal lifestyle change contributes to their offspring. Here we show that enriched environment (EE) induced maternal slimming improves general health and reprograms metabolic gene expression in mice offspring. EE in mothers induced decreased body weight, adiposity, and improved glucose tolerance and insulin sensitivity. Relative to controls, their offspring exhibited improved general health such as reduced fat accumulation, enhanced metabolic parameters as well as glucose tolerance and insulin sensitivity. Maternal slimming altered the expression of 1,732 genes in the liver of offspring, with coherent downregulation of genes involved in lipid and cholesterol biosynthesis. Epigenomic profiling in offspring revealed numerous changes in cytosine methylation depending on maternal slimming, including hypermethylation of several genes involved in lipid biosynthesis, correlated with the downregulation of these genes. Maternal slimming also altered overall transcriptome patterns in mature oocytes, which contributes largely to the metabolic health and gene expression patterns in offspring. Overall, our studies suggest that maternal slimming have a beneficial role in regulating metabolic profiles in offspring, implying that it might be considered as a potential strategy to reverse the global prevalence of obesity and related metabolic syndromes. Female F0 founders were raised on a standard diet in a normal cage until 12 weeks of age, at which point they were placed into the enriched environmental cage or stayed in the normal cage (chosen at random) for 4 weeks. Males were always raised on a standard diet in the standard cage. At 16 weeks, female F0 founders were mated with males in standard conditions. After 1 or 2 days, males were removed, and pregnant females were left alone with a standard diet in the standard cage until their litters were 3 weeks of age. Note that we always used virgin males to avoid confounding effects brought about by the males. Moreover, males mated with two female groups did not differ in phenotypic data (body weight, adiposity, fasting blood glucose and insulin levels). At 3 weeks of age, partial offspring were sacrificed and the median lobe of liver was rapidly dissected out and flash-frozen in liquid N2, each from an independent mother. Samples from five control and four slimming offspring, each from different mothers, were chosen for microarray analysis.

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

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