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Background  Insects thriving on nutritionally poor habitats have integrated mutualistic intracellular symbiotic bacteria (endosymbionts) in a bacteria-bearing tissue (the bacteriome) that isolates the endosymbionts and protects them against a host systemic immune response. Whilst the metabolic and physiological features of long-term insect associations have been investigated in detail over the past decades, cellular and immune regulations that determine the host response to endosymbionts and pathogens have attracted interest more recently.    Results  To investigate bacteriome cellular specificities and weevil immune responses to bacteria, we have constructed and sequenced 7 cDNA libraries from  Sitophilus oryzae  whole larvae and bacteriomes. Bioinformatic analysis of 26,886 ESTs led to the generation of 8,941 weevil unigenes. Based on  in silico  analysis and on the examination of genes involved in the cellular pathways of potential interest to intracellular symbiosis ( i.e.  cell growth and apoptosis, autophagy, immunity), we have selected and analyzed 29 genes using qRT-PCR, taking into consideration bacteriome specificity and symbiosis impact on the host response to pathogens. We show that the bacteriome tissue accumulates transcripts from genes involved in cellular development and survival, such as the apoptotic inhibitors  iap2  and  iap3 , and endosomal fusion and trafficking, such as  Rab7 ,  Hrs , and  SNARE . As regards our investigation into immunity, we first strengthen the bacteriome immunomodulation previously reported in  S. zeamais.  We show that the sarcotoxin, the c-type lysozyme, and the  wpgrp2  genes are downregulated in the  S. oryzae  bacteriome, when compared to aposymbiotic insects and insects challenged with  E. coli . Secondly, transcript level comparison between symbiotic and aposymbiotic larvae provides evidence that the immune systemic response to pathogens is decreased in symbiotic insects, as shown by the relatively high expression of  wpgrp2 ,  wpgrp3 , coleoptericin-B, diptericin, and sarcotoxin genes in aposymbiotic insects.    Conclusions  Library sequencing significantly increased the number of unigenes, allowing for improved functional and genetic investigations in the cereal weevil  S. oryzae . Transcriptomic analyses support selective and local immune gene expression in the bacteriome tissue and uncover cellular pathways that are of potential interest to bacteriocyte survival and homeostasis. Bacterial challenge experiments have revealed that the systemic immune response would be less induced in a symbiotic insect, thus highlighting new perspectives on host immunity in long-term invertebrate co-evolutionary associations.

Host gene response to endosymbiont and pathogen in the cereal weevil Sitophilus oryzae