Abstract
BackgroundPersistent infections with mutualistic intracellular bacteria (endosymbionts) are well represented in insects and are considered to be a driving force in evolution. However, while pathogenic relationships have been well studied over the last decades very little is known about the recognition of the endosymbionts by the host immune system and the mechanism that limits their infection to the bacteria-bearing host tissue (the bacteriome).ResultsTo study bacteriome immune specificity, we first identified immune-relevant genes of the weevil Sitophilus zeamais by using suppressive subtractive hybridization (SSH) and then analyzed their full-length coding sequences obtained by RACE-PCR experiments. We then measured immune gene expression in the bacteriome, and in the aposymbiotic larvae following S. zeamais primary endosymbiont (SZPE) injection into the hemolymph, in order to consider the questions of bacteriome immune specificity and the insect humoral response to symbionts. We show that larval challenge with the endosymbiont results in a significant induction of antibacterial peptide genes, providing evidence that, outside the bacteriome, SZPE are recognized as microbial intruders by the host. In the bacteriome, gene expression analysis shows the overexpression of one antibacterial peptide from the coleoptericin family and, intriguingly, homologs to genes described as immune modulators (that is, PGRP-LB, Tollip) were also shown to be highly expressed in the bacteriome.ConclusionThe current data provide the first description of immune gene expression in the insect bacteriome. Compared with the insect humoral response to SZPE, the bacteriome expresses few genes among those investigated in this work. This local immune gene expression may help to maintain the endosymbiont in the bacteriome and prevent its invasion into insect tissues. Further investigations of the coleoptericin, the PGRP and the Tollip genes should elucidate the role of the host immune system in the maintenance and regulation of endosymbiosis.
Highlights
Persistent infections with mutualistic intracellular bacteria are well represented in insects and are considered to be a driving force in evolution
Compared with the insect humoral response to S. zeamais primary endosymbiont (SZPE), the bacteriome expresses few genes among those investigated in this work
Further investigations of the coleoptericin, the peptidoglycan recognition proteins (PGRPs) and the Tollip genes should elucidate the role of the host immune system in the maintenance and regulation of endosymbiosis
Summary
Persistent infections with mutualistic intracellular bacteria (endosymbionts) are well represented in insects and are considered to be a driving force in evolution. Activation of the humoral pathway consists of microbe-associated molecular pattern recognition by pattern recognition receptors, such as peptidoglycan recognition proteins (PGRPs), and the activation of intracellular signaling pathways, such as the Toll and the Immune deficiency (Imd) pathways These pathways activate, in particular, the production and the secretion of a panel of antimicrobial peptides (AMPs) in response to Gram-positive and Gram-negative bacteria. In addition to AMP production, the insect humoral response involves a proteolytic cascade leading to prophenoloxidase (PPO) activation and subsequent melanin synthesis at the site of cuticular injury This reaction, called melanization, plays a key role in wound healing, encapsulation, sequestration of microbes and production of toxic intermediates [10]. It has been shown that these PGRPs, which scavenge peptidoglycan released by commensal bacteria, reduce gut immune reactivity and avoid a state of permanent immune activation in this tissue [12,13]
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