Abstract

Animals are inhabited by a diverse community of microorganisms. The relevance of such microbiota is increasingly being recognized across a broad spectrum of species, ranging from sponges to primates, revealing various beneficial roles that microbes can play. The red flour beetle Tribolium castaneum represents a well-established experimental model organism for studying questions in ecology and evolution, however, the relevance of its microbial community is still largely unknown. T. castaneum larvae orally exposed to bacterial components of the entomopathogen Bacillus thuringiensis bv. tenebrionis showed increased survival upon a subsequent challenge with spores of this bacterium. To investigate whether T. castaneum microbiota plays a role in this phenomenon, we established a protocol for raising microbe-free larvae and subsequently tested whether they differ in their ability to mount such a priming response. Here we demonstrate that larvae with significantly lowered microbial loads, show decreased survival upon secondary challenge with B. thuringiensis bv. tenebrionis spores, compared to animals that were allowed to regain their microbiota before priming. Although the exact mechanism of oral immune priming is unclear, we here suggest that microbiota plays a crucial role in oral immune priming in this species.

Highlights

  • Parasites and infectious diseases impose a serious threat to the fitness of their hosts

  • Contrary to earlier dogma that invertebrates are incapable of adaptive immune responses, evidence has accumulated that many arthropod species show a phenomenon named “immune priming” (Schmid-Hempel, 2005), i.e., enhanced protection following a prior exposure to a pathogen, which is today recognized as a form of immune memory (Kurtz and Franz, 2003)

  • Our results show that host-associated microbiota plays a crucial role in the mediation of oral priming in T. castaneum with Btt: priming larvae with Btt-derived components only provided protection against a subsequent exposure to Btt spores when the microbiota was present in the larval gut

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Summary

Introduction

Parasites and infectious diseases impose a serious threat to the fitness of their hosts. The degree to which invertebrates possess a form of immune memory has been an intensively debated topic over the last decade (Kurtz, 2004; Little et al, 2005; Rowley and Powell, 2007). Contrary to earlier dogma that invertebrates are incapable of adaptive immune responses, evidence has accumulated that many arthropod species show a phenomenon named “immune priming” (Schmid-Hempel, 2005), i.e., enhanced protection following a prior exposure to a pathogen, which is today recognized as a form of immune memory (Kurtz and Franz, 2003). A phenomenon not generally characteristic for all invertebrate-parasite systems that have been studied, immune priming has been repeatedly shown in a number of arthropod species, especially insects. Evidence for a range of specificities in immune priming, including highly specific responses, has been found

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