Blood-feeding adaptations and virome assessment of the poultry red mite Dermanyssus gallinae guided by RNA-seq

Abstract

Dermanyssus gallinae is a blood-feeding mite that parasitises wild birds and farmed poultry. Its remarkably swift processing of blood, together with the capacity to blood-feed during most developmental stages, makes this mite a highly debilitating pest. To identify specific adaptations to digestion of a haemoglobin-rich diet, we constructed and compared transcriptomes from starved and blood-fed stages of the parasite and identified midgut-enriched transcripts. We noted that midgut transcripts encoding cysteine proteases were upregulated with a blood meal. Mapping the full proteolytic apparatus, we noted a reduction in the suite of cysteine proteases, missing homologues for Cathepsin B and C. We have further identified and phylogenetically analysed three distinct transcripts encoding vitellogenins that facilitate the reproductive capacity of the mites. We also fully mapped transcripts for haem biosynthesis and the ferritin-based system of iron storage and inter-tissue trafficking. Additionally, we identified transcripts encoding proteins implicated in immune signalling (Toll and IMD pathways) and activity (defensins and thioester-containing proteins), RNAi, and ion channelling (with targets for commercial acaricides such as Fluralaner, Fipronil, and Ivermectin). Viral sequences were filtered from the Illumina reads and we described, in part, the RNA-virome of D. gallinae with identification of a novel virus, Red mite quaranjavirus 1.

Genome sequences of fourIxodesspecies expands understanding of tick evolution

“…The most abundant TEs found in these tick species were long interspersed nuclear elements (LINEs), with 397,287 elements on average (∼7% of the elements identified). Interspersed sequences represented only 9.5% of the genome of Amblyomma maculatum (Ribeiro et al 2023), whereas they accounted for over 50% of the genome of all Ixodes ticks. However, the relative frequencies of each TE family were similar between the genomes of A. maculatum (Jose M. C. Ribeiro et al 2023) and I. scapularis (De et al 2023).…”

“…Interspersed sequences represented only 9.5% of the genome of Amblyomma maculatum (Ribeiro et al 2023), whereas they accounted for over 50% of the genome of all Ixodes ticks. However, the relative frequencies of each TE family were similar between the genomes of A. maculatum (Jose M. C. Ribeiro et al 2023) and I. scapularis (De et al 2023). For example, the Gypsy/DIRS family in the long terminal repeat (LTR) class has one of the highest coverages in both A. maculatum (Ribeiro et al 2023) and I. scapularis , (Nuss et al 2023, De et al 2023), and represent ∼5% of the genome in the four Ixodes species sequenced in the present study.…”

“…The search for heme synthesis and degrading enzymes in the I. ricinus genome was performed by BLAST, with the tblastn or blastp algorithms, using the sequences of Dermanyssus gallinae (Ribeiro et al 2023) as queries. The Alphafold2 algorithm was used to predict the monomeric structure of ferritin-1 and ferritin-2 identified in the I. ricinus genome.…”

One health approach to study human health risks associated with Dermanyssus gallinae mites

“…Some of the microorganisms detected here may be endosymbionts, such as Bartonella -like bacteria, which covered between 30 % and 70 % of the sequences in the microbiome of D. gallinae collected from poultry houses in Czechia [ 7 , 20 ]. However, it has been previously demonstrated that Dermanyssus is capable of carrying and transmitting pathogenic Bartonella species to humans, such as Bartonella quintana [ 22 ].…”

“…Dermanyssus gallinae is often considered a vector for several bacterial pathogens, such as Salmonella Gallinarum, Salmonella Enteritidis, Pasteurella multocida , Coxiella burnetii , and Spirochetes, as well as viral pathogens including Western equine encephalitis virus, and Venezuelan equine encephalitis virus [ [6] , [7] , [8] ]. Additionally, the poultry red mite has been found to test positive for various tick-borne pathogens (TBPs), although its ability to transmit them to other hosts has not been conclusively demonstrated [ 4 ].…”