Systemic Infection Generates a Local-Like Immune Response of the Bacteriome Organ in Insect Symbiosis

Abstract

Endosymbiosis is common in insects thriving in nutritionally unbalanced habitats. The cereal weevil, Sitophilus oryzae, houses Sodalis pierantonius, a Gram-negative intracellular symbiotic bacterium (endosymbiont), within a dedicated organ called a bacteriome. Recent data have shown that the bacteriome expresses certain immune genes that result in local symbiont tolerance and control. Here, we address the question of whether and how the bacteriome responds to insect infections involving exogenous bacteria. We have established an infection model by challenging weevil larvae with the Gram-negative bacterium Dickeya dadantii. We showed that D. dadantii infects host tissues and triggers a systemic immune response. Gene transcript analysis indicated that the bacteriome is also immune responsive, but it expresses immune effector genes to a lesser extent than the systemic and intestinal responses. Most genes putatively involved in immune pathways remain weakly expressed in the bacteriome following D. dadantii infection. Moreover, quantitative PCR experiments showed that the endosymbiont load is not affected by insect infection or the resulting bacteriome immune activation. Thus, the contained immune effector gene expression in the bacteriome may prevent potentially harmful effects of the immune response on endosymbionts, whilst efficiently protecting them from bacterial intruders.

Antimicrobial peptides and cell processes tracking endosymbiont dynamics

“…However, no orthologues of known negative immune regulators have been shown to be highly expressed in the S. oryzae bacteriome. As an example, pirk and caudal basal expression levels are, respectively, two and three times lower in the bacteriome than in other weevil tissues ( [49] and unpublished RNAseq data).…”

“…Lastly, the expression of colA in the bacteriome is also modulated by systemic challenges of insects by exogenous bacteria [49]. An injection of Gram-negative or Gram-positive bacteria into the weevil's haemolymph triggers an immune response of the bacteriome, attested by the induction of several AMP coding genes, including colB and colA [49].…”

“…PGRP-LB and -SC2 may degrade endosymbiont immunogenic peptidoglycan, highlighting a possible mechanism of tolerance that would rely on a low detection of endosymbionts by the immune system [50]. In cereal weevils, the findings that an immune response is activated in the bacteriome following larval challenge with exogenous free-living bacteria [49] indicate that immune pathways are functional in this organ, supporting the idea of an active mechanism of AMP gene repression under physiological conditions, a repression that would be cancelled in case of infections, allowing the defence of the bacteriome and its associated endosymbionts. Genetic negative regulations of local immune responses in tissues in contact with beneficial bacterial communities, such as the gut epithelium, are well described in insects.…”

The evolutionary development of plant‐feeding insects and their nutritional endosymbionts

“…This decrease corresponds to the drop in symbiont densities that occurs from day 1 to day 6, until the gut bacteriome is completely eliminated by 14 d (Vigneron et al ., ). Additionally, at day 6 after adult emergence the expression of genes that belong to the KEGG categories associated with degradation of bacterial components had significantly increased (Masson et al ., ). Masson et al .…”

“…(F) Symbiont titer in the weevil Sitophilus oryzae from Masson et al . (), spanning late larval (L4), pupal (P), and adult stages 1–14 d (D1–14).…”