Oral immune priming with Bacillus thuringiensis induces a shift in the gene expression of Tribolium castaneum larvae

Abstract

BackgroundThe phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has now been demonstrated in a wide range of invertebrate species. Despite accumulating phenotypic evidence, knowledge of its mechanistic underpinnings is currently very limited. Here we used the system of the red flour beetle, Tribolium castaneum and the insect pathogen Bacillus thuringiensis (Bt) to further our molecular understanding of the oral immune priming phenomenon. We addressed how ingestion of bacterial cues (derived from spore supernatants) of an orally pathogenic and non-pathogenic Bt strain affects gene expression upon later challenge exposure, using a whole-transcriptome sequencing approach.ResultsWhereas gene expression of individuals primed with the orally non-pathogenic strain showed minor changes to controls, we found that priming with the pathogenic strain induced regulation of a large set of distinct genes, many of which are known immune candidates. Intriguingly, the immune repertoire activated upon priming and subsequent challenge qualitatively differed from the one mounted upon infection with Bt without previous priming. Moreover, a large subset of priming-specific genes showed an inverse regulation compared to their regulation upon challenge only.ConclusionsOur data demonstrate that gene expression upon infection is strongly affected by previous immune priming. We hypothesise that this shift in gene expression indicates activation of a more targeted and efficient response towards a previously encountered pathogen, in anticipation of potential secondary encounter.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3705-7) contains supplementary material, which is available to authorized users.

Innate immune memory: An evolutionary perspective

“…Interestingly a new and unexpected regulatory process has been described recently for invertebrates. Two recent studies reveal that the primary and the secondary immune responses, developed against the same parasite, involve different immune effector systems resulting in a transcriptional shift . This transcriptional shift was highlighted in mollusk and insect and involved a substantial set of differentially expressed transcripts that were over or under‐represented exclusively following the secondary immune challenge.…”

“…This transcriptional shift was highlighted in mollusk and insect and involved a substantial set of differentially expressed transcripts that were over or under‐represented exclusively following the secondary immune challenge. In Biomphalaria snails, this immune shift will changed the immune cellular encapsulation response toward a humoral immune response while in the coleopteran Tribolium, immune shift results in an enhanced pleiotropic immune capabilities …”

“…These changes are driven by the recruitment of stimulation‐responsive transcription factors like NF‐κB, AP‐1, and STAT family members. It is to note that such major immune signaling pathways (ie, IMD, Toll, JAK/STAT, NF‐κB) are also well conserved across invertebrate phyla re‐inforcing the chance to highlight an overall ancestral mechanism of innate immune memory from plants to vertebrates . Further research is now needed to test if whether epigenetic reprogramming appeared as an overall molecular process that can be found in invertebrates displaying innate immune memory phenotype.…”

Pathogen susceptibility and fitness costs explain variation in immune priming across natural populations of flour beetles

“…The lack of associations between priming and different immune components was surprising, given prior work with other insects showing that priming is beneficial because it induces more efficient immune responses (Barribeau, Schmid-Hempel, & Sadd, 2016, but also see Greenwood et al, 2017; and that components of innate and external immunity (quinone secretion outside the body; Joop et al, 2014) trade off (Cotter et al, 2013).…”

Pathogen susceptibility and fitness costs explain variation in immune priming across natural populations of flour beetles

“…Overall, antibacterial activity did not explain the observed variation in primimg response, highlighting that the association between innate immune responses and survival after priming may not be straightforward in wild populations. This is surprising since previous studies with Tribolium beetles found that priming with B. thuringiensis increases expression of a large set of immune related genes (Greenwood et al 2017), correlating strongly with survival after reinfection (Milutinović et al 2013). We note that whereas our hemolymph antibacterial activity assay may reflect the impact of several immune pathways such as antimicrobial peptides, it is possible that other aspects of innate immunity such as cellular defence (e.g.…”