Abstract
Many insects developing on nutritionally unbalanced diets have evolved symbiotic associations with vertically transmitted intracellular bacteria (endosymbionts) that provide them with metabolic components, thereby improving the host’s abilities to thrive on such poor ecological niches. While host-endosymbiont coevolutionary constraints are known to entail massive genomic changes in the microbial partner, host’s genomic evolution remains elusive, particularly with regard to the immune system. In the cereal weevil Sitophilus spp., which houses Sodalis pierantonius, endosymbionts are secluded in specialized host cells, the bacteriocytes that group together as an organ, the bacteriome. We previously reported that at standard conditions, the bacteriome highly expresses the coleoptericin A (colA) antimicrobial peptide (AMP), which was shown to prevent endosymbiont escape from the bacteriocytes. However, following the insect systemic infection by pathogens, the bacteriome upregulates a cocktail of AMP encoding genes, including colA. The regulations that allow these contrasted immune responses remain unknown. In this short report, we provide evidence that an IMD-like pathway is conserved in two sibling species of cereal weevils, Sitophilus oryzae and Sitophilus zeamais. RNA interference (RNAi) experiments showed that imd and relish genes are essential for (i) colA expression in the bacteriome under standard conditions, (ii) AMP up-regulation in the bacteriome following a systemic immune challenge, and (iii) AMP systemic induction following an immune challenge. Histological analyses also showed that relish inhibition by RNAi resulted in endosymbiont escape from the bacteriome, strengthening the involvement of an IMD-like pathway in endosymbiont control. We conclude that Sitophilus’ IMD-like pathway mediates both the bacteriome immune program involved in endosymbiont seclusion within the bacteriocytes and the systemic and local immune responses to exogenous challenges. This work provides a striking example of how a conserved immune pathway, initially described as essential in pathogen clearance, also functions in the control of mutualistic associations.
Highlights
Host-symbiont associations are widespread in nature and exhibit a variety of interactions ranging from parasitism to mutualism
On the host’s side, many insects have selected a compartmentalization strategy that consists in secluding endosymbionts within specialized host cells, the bacteriocytes, limiting thereby their direct contact with the host systemic immune response [5, 10, 13,14,15,16]
Because immune deficiency (IMD) appears to control two distinct responses in the weevil bacteriome, i.e. the “internal” symbiosisrelated program and the “external” immune response to tracheal cytotoxin (TCT) injection, we wondered whether this pathway could split into two distinct transduction signals downstream of IMD, leading to the differential recruitment of transcription factors that could account for the two responses
Summary
Host-symbiont associations are widespread in nature and exhibit a variety of interactions ranging from parasitism to mutualism. Because IMD appears to control two distinct responses in the weevil bacteriome, i.e. the “internal” symbiosisrelated program and the “external” immune response to TCT injection, we wondered whether this pathway could split into two distinct transduction signals downstream of IMD, leading to the differential recruitment of transcription factors that could account for the two responses To test this hypothesis, we inhibited relish expression by RNAi (Additional file 2) and monitored AMP expression in PBS-injected and TCT-injected larvae. Symbionts were seen “leaking” from the bacteriome 6 days after relish dsRNA injection (Fig. 4b), and many bacteria were seen in the larval fat body 10 days after relish dsRNA injection (Fig. 4c) This phenotype is similar to what was previously observed following colA inhibition [20] and confirms that, by regulating colA expression, this IMD-like pathway is directly involved in symbiosis compartmentalization. Recent studies in insects have shown that several microRNAs target and regulate immune genes, including AMPs [71, 72], and can mediate host-symbiont interactions as shown in the Aedes aegypti-Wolbachia association [73]
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