Gut bacteria induce heterologous immune priming in Rhodnius prolixus encompassing both humoral and cellular immune responses

Abstract

Insects lack the adaptive, antibody mediated responses of vertebrates, yet they possess a robust innate immune system capable of defending the host against pathogens. Immune priming has been observed in multiple insect species, wherein exposure to a pathogen provides protection against subsequent infections by the pathogen. Less frequently, heterologous immune priming has been observed where exposure to one bacterial species provides protection against other species. We determined that Rhodococcus rhodnii, a gut symbiont of the kissing bug Rhodnius prolixus, induces a strong heterologous immune priming effect, while axenic bugs lacking any gut bacteria are highly susceptible to pathogens in their hemolymph. Commensal Escherichia coli provides a less robust protective effect than R. rhodnii. R. rhodnii must be alive within the insect as dead bacteria do not stimulate immune priming and pathogen resistance. Removal of R. rhodnii from the gut reduces resistance to pathogens while restoring it to otherwise axenic bugs improves resistance to pathogens, though not completely. R. rhodnii and E. coli activate both the Imd and Toll pathways, indicating cross-activation of the pathways and demonstrating the canonical Drosophila immune response has diverged in Hemiptera. Silencing of either pathway leads to a loss of the protective effect. Several antimicrobial peptides are induced in the fat body by presence of gut bacteria. When E. coli is in the gut, expression of antimicrobial peptides is often higher than when R. rhodnii, though R. rhodnii stimulates proliferation of hemocytes and induce a stronger melanization response. Hemolymph from R. rhodnii bugs has a greater ability to convert the melanin precursor DOPA to melanization products than axenic or E. coli-harboring bugs. These results demonstrate that R. rhodnii’s benefits to its host extend beyond nutritional provisioning, playing an important role in the host immune system.

Competing Interest Statement

The authors have declared no competing interest.