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.

Highlights

  • The phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has been demonstrated in a wide range of invertebrate species

  • Priming with Bacillus thuringiensis bv. tenebrionis (Btt) elicits a differential gene expression response in T. castaneum We performed RNA-seq experiments to identify the molecular basis of oral immune priming in T. castaneum larvae [15]

  • 51.6 million raw reads were generated per sample and 46 million reads per sample remained after filtering, of which 78% could be mapped to the T. castaneum genome. 12288 of the 12777 annotated genes were detected

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Summary

Introduction

The phenomenon of immune priming, i.e. enhanced protection following a secondary exposure to a pathogen, has been demonstrated in a wide range of invertebrate species. Strategies for finding resistance genes involved a time- and knowledge-intensive candidate gene approach, but with the recent advances in sequencing technologies it has become tractable to efficiently explore insect immunity on a genome-wide basis [18, 19]. T. castaneum is a major pest of food grain [22] This species has become a powerful model organism for studies of insect immunity, with a fully-sequenced genome [23] and more recently, established protocols for studying host-parasite interactions using the pathogen B. thuringiensis [9, 24, 25]. Further analysis revealed a number of candidate genes, which provide a new basis to study the molecular underpinnings of immune priming in insects

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