Rewired RNAi-Mediated Genome Surveillance in House Dust Mites

Abstract

House dust mites are common pests with an unusual evolutionary history, being descendants of a parasitic ancestor. Transition to parasitism is frequently accompanied by genome rearrangements, possibly to accommodate the genetic change needed to access new ecology. Transposable element (TE) activity is a source of genomic instability that can trigger large-scale genomic alterations. Eukaryotes have multiple transposon control mechanisms, one of which is RNA interference (RNAi). Investigation of the dust mite genome failed to identify a major RNAi pathway: the Piwi-associated RNA (piRNA) pathway, which has been replaced by a novel small-interfering RNA (siRNA)-like pathway. Co-opting of piRNA function by dust mite siRNAs is extensive, including establishment of TE control master loci that produce siRNAs. Interestingly, other members of the Acari have piRNAs indicating loss of this mechanism in dust mites is a recent event. Flux of RNAi-mediated control of TEs highlights the unusual arc of dust mite evolution. Author summaryInvestigation of small RNA populations in dust mites revealed absence of the piwi-associated RNA (piRNA) pathway. Apart from several nematode and platyhelminths lineages, piRNAs are an essential component of animal genome surveillance, actively targeting and silencing transposable elements. In dust mites, expansion of Dicer produced small-interfering RNA (siRNA) biology compensates for loss of piRNAs. The dramatic difference we find in dust mites is likely a consequence of their evolutionary history, which is marked by descent from a parasite to the current free-living form. Our study highlights a correlation between perturbation of transposon surveillance and shifts in ecology.

A genome-wide screening for RNAi pathway proteins in Acari

“…This assumption is supported by phylogenetic analysis of Dicer proteins which showed two Dicer paralogs with distinct functions in Acari: Dicer1 and Dicer2 involved in miRNA and siRNA biosynthesis, respectively (Table 3, Fig. 1A, B) as was previously shown in other two Acari species: P. ovis [52] and D. farina [51].…”

“…farina [51]. Overall, this and previous genomic studies indicate that RdRP amplification activity seems to occur in Acari species studied to date, which may result in efficient gene silencing throughout the organisms as was suggested for Arthropod species in which this protein was found [81].…”

“…and Rrf-1) [37] and other Acari species e. g. D. farinae [51] and Psoroptes ovis [52] had the characteristic conserved RdRP domain [34]. In order to infer the evolutionary history of Acari RdRP proteins, we conducted a phylogenetic analysis based on the amino acid alignment of RdRP domain using C. elegans as outgroup, as described in the methods section.…”

A genome-wide screening for RNAi pathway proteins in Acari

“…It is supported by the phylogenetic analysis of Dicer proteins which showed two Dicer paralogs with distinct functions in Acari: Dicer1 and Dicer2 involved in miRNA and siRNA biosynthesis, respectively (Table 3, Fig. 1A, B) as was previously shown in the other two Acari species: P. ovis [52] and D. farina [51]. Two Dicer paralogs were also found in insect species [33,[58][59][60] and crustaceans [57,61] analyzed so far, but only one (Dicer1) was so far detected in nematodes and mammals [19].…”

siRNAs and piRNAs collaborate for transposon control in the two-spotted spider mite

“…Investigation of RNAi biology in another mite, Dermatophagoides farinae, found a complete loss of piRNA pathways and replacement with Dicer produced, siRNAmediated genome surveillance, complete with siRNA-based master loci (ML-siRNA) (Mondal et al 2018). While spider mites clearly have an intact piRNA pathway, they appear to share ML-siRNA loci with dust mites.…”