Rhodnius prolixus: Identification of missing components of the IMD immune signaling pathway and functional characterization of its role in eliminating bacteria

Abstract

The innate immune system in insects is regulated by specific signalling pathways. Most immune related pathways were identified and characterized in holometabolous insects such as Drosophila melanogaster , and it was assumed they would be highly conserved in all insects. The hemimetabolous insect, Rhodnius prolixus , has served as a model to study basic insect physiology, but also is a major vector of the human parasite, Trypanosoma cruzi , that causes 10,000 deaths annually. The publication of the R . prolixus genome revealed that one of the main immune pathways, the Immune-deficiency pathway (IMD), was incomplete and probably non-functional, an observation shared with other hemimetabolous insects including the pea aphid ( Acyrthosiphon pisum ) and the bedbug ( Cimex lectularius ). It was proposed that the IMD pathway is inactive in R . prolixus as an adaptation to prevent eliminating beneficial symbiont gut bacteria. We used bioinformatic analyses based on reciprocal BLAST and HMM-profile searches to find orthologs for most of the “missing” elements of the IMD pathway and provide data that these are regulated in response to infection with Gram-negative bacteria. We used RNAi strategies to demonstrate the role of the IMD pathway in regulating the expression of specific antimicrobial peptides (AMPs) in the fat body of R . prolixus . The data indicate that the IMD pathway is present and active in R . prolixus , which opens up new avenues of research on R . prolixus-T . cruzi interactions.

What happens after a blood meal? A transcriptome analysis of the main tissues involved in egg production in Rhodnius prolixus, an insect vector of Chagas disease

“…prolixus genome was published [ 16 ]. However, recently, Salcedo-Porras et al [ 169 ] found orthologues for most of the “missing” elements of the IMD pathway in R . prolixus and reported that these are regulated in response to infection with Gram-negative bacteria.…”

Brown marmorated stink bug, Halyomorpha halys (Stål), genome: putative underpinnings of polyphagy, insecticide resistance potential and biology of a top worldwide pest

“…The lack of IMD is not necessarily unusual, as it has also not been found in the pea aphid, A. pisum; the body louse, Pediculus humanus corporis; or the deer tick, Ixodes scapularis. Indeed, recent evidence suggests IMD is absent among hempiterans [116,117], although its absence indicates an as-yet-uncharacterized means for transducing a PGRPinitiated signal in response to bacterial challenge.…”

The genome sequence of the grape phylloxera provides insights into the evolution, adaptation, and invasion routes of an iconic pest

“…The lack of an intact IMD pathway in psyllids and aphids has been suggested to relate to their obligate symbiotic associations [ 31 , 32 ]; however, this hypothesis does not explain the apparent lack of intact IMD pathway in phylloxera, which lacks obligate symbionts. We however note the possibility of divergent genes that would represent a functional pathway as recently shown fo r R. prolixus [ 33 ].…”