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Open Access Research article

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

Sarah Behrens1*, Robert Peuß1, Barbara Milutinović1, Hendrik Eggert1, Daniela Esser2, Philip Rosenstiel2, Hinrich Schulenburg3, Erich Bornberg-Bauer1 and Joachim Kurtz1*

Author Affiliations

1 Institute for Evolution and Biodiversity, University of Münster, Hüfferstr. 1, 48149 Münster, Germany

2 Institute of Clinical Molecular Biology, Christian-Albrechts University Kiel, Schittenhelmstr. 12, 24105 Kiel, Germany

3 Zoological Institute, Christian-Albrechts University Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany

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BMC Genomics 2014, 15:445  doi:10.1186/1471-2164-15-445

Published: 7 June 2014

Abstract

Background

Pathogens 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.

Results

The 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.

Conclusions

Our 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.

Keywords:
Tribolium castaneum; Bacillus thuringiensis; Host-parasite interactions; Oral infection; Pricking infection; RNA sequencing; Transcriptome