Infection routes matter in population-specific responses of the red flour beetle to the entomopathogen Bacillus thuringiensis

Abstract

BackgroundPathogens can infect their hosts through different routes. For studying the consequences for host resistance, we here used the entomopathogen Bacillus thuringiensis and the red flour beetle Tribolium castaneum for oral and systemic (i. e. pricking the cuticle) experimental infection. In order to characterize the molecular mechanisms underpinning the two different infection routes, the transcriptomes of beetles of two different T. castaneum populations – one recently collected population (Cro1) and a commonly used laboratory strain (SB) – were analyzed using a next generation RNA sequencing approach.ResultsThe genetically more diverse population Cro1 showed a significantly larger number of differentially expressed genes. While both populations exhibited similar reactions to pricking, their expression patterns in response to oral infection differed remarkably. In particular, the Cro1 population showed a strong response of cuticular proteins and developmental genes, which might indicate an adaptive developmental flexibility that was lost in the SB population presumably as a result of inbreeding. The immune response of SB was primarily based on antimicrobial peptides, while Cro1 relied on responses mediated by phenoloxidase and reactive oxygen species, which may explain the higher resistance of this strain against oral infection.ConclusionsOur data demonstrate that immunological and physiological processes underpinning the two different routes of infection are clearly distinct, and that host populations particularly differ in responses to oral infection. Furthermore, gene expression upon pricking infection entailed a strong signal of wounding, highlighting the importance of pricking controls in future infection studies.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-445) contains supplementary material, which is available to authorized users.

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

“…3, Additional file 2: Figure S1). For example, 292 genes were up-regulated exclusively among larvae challenged with Btt (Control- Btt , Bt407 - - Btt and Btt - Btt ) and 307 were shared exclusively among Btt -challenged larvae that had not been primed or were primed with Bt407 - (Control- Btt and Bt407 - - Btt ), confirming a strong transcriptional response to Btt spore ingestion [19]. Interestingly, 315 genes were specifically up-regulated only in Btt -primed larvae ( Btt -Naive, Btt - Btt ), showing that Btt -priming drastically altered gene expression patterns.…”

“…Larvae were kept on the naive diet for 4 days after which they were similarly exposed to spore-containing (5 × 10 9 mL -1 Btt spores in PBS mixed with flour) or naive diet for 6 h and sampled for the transcriptome analysis. This timepoint was used since our previous study showed that sampling 6 h after the challenge gives a clear expression signature, compared to already weaker expression after 18 h [19]. Hence, the sampled treatments were as follows: Btt primed- Btt challenged ( Btt - Btt ), Bt407 - primed- Btt challenged ( Bt407 - - Btt) , Control- Btt challenged (Control- Btt ), Btt primed-Naïve ( Btt -Naive), Bt407 - primed-Naïve ( Bt407 - -Naïve), Control-Naïve.…”

“…The R package TopGO was then used to generate GO enrichments for each of our treatment comparisons of interest, using the weight01 GO graph algorithm and Fishers exact test for significance [74]. Results of the 20 most significant terms were visualised with Wordle™ after the p -values were scaled according to -log 10 ( p -value) [19, 75]. Subsequently, these results were merged with Gene Ontology terms [76] downloaded from Ensembl Biomart [77] and results of a BlastP search [78] using default parameters, to further add gene information for interpretation of the results.…”

The within‐host dynamics of infection in trans‐generationally primed flour beetles

“…2008; Yokoi et al . 2012), and even characterized differences in gene expression between oral and septic challenge with Bt (Behrens et al . 2014).…”

Sustainable farming of the mealworm Tenebrio molitor for the production of food and feed

“…However, individual immune priming by systemic injection would prove difficult in mass-reared insects due to their relatively small size and great number. In this context, the broad database available for other tenebrionid beetles is valuable because T. castaneum is considered as a model organism for the investigation of immune priming [134][135][136]. One advantage of T. castaneum is that oral priming is possible by adding pathogens or a corresponding supernatant directly to the diet [137].…”