Symbiotic bacteria of the gall-inducing mite Fragariocoptes setiger (Eriophyoidea) and phylogenomic resolution of the eriophyoid position among Acari

Abstract

Eriophyoid mites represent a hyperdiverse, phytophagous lineage with an unclear phylogenetic position. These mites have succeeded in colonizing nearly every seed plant species, and this evolutionary success was in part due to the mites' ability to induce galls in plants. A gall is a unique niche that provides the inducer of this modification with vital resources. The exact mechanism of gall formation is still not understood, even as to whether it is endogenic (mites directly cause galls) or exogenic (symbiotic microorganisms are involved). Here we (i) investigate the phylogenetic affinities of eriophyoids and (ii) use comparative metagenomics to test the hypothesis that the endosymbionts of eriophyoid mites are involved in gall formation. Our phylogenomic analysis robustly inferred eriophyoids as closely related to Nematalycidae, a group of deep-soil mites belonging to Endeostigmata. Our comparative metagenomics, fluorescence in situ hybridization, and electron microscopy experiments identified two candidate endosymbiotic bacteria shared across samples, however, it is unlikely that they are gall inducers (morphotype1: novel Wolbachia, morphotype2: possibly Agrobacterium tumefaciens). We also detected an array of plant pathogens associated with galls that may be vectored by the mites, and we determined a mite pathogenic virus (Betabaculovirus) that could be tested for using in biocontrol of agricultural pest mites.

Atypically Shaped Setae in Gall Mites (Acariformes, Eriophyoidea) and Mitogenomics of the Genus Leipothrix Keifer (Eriophyidae)

“…The four new mitogenomes of Leipothrix spp. comprise the same constant blocks I, II, III and variable zones A,B,C ( Figure 5 ), recently defined in other published mitogenomes of Eriophyidae [ 18 , 32 , 40 , 43 , 44 , 45 ]. They share the following unique traits: (1) the trn K gene precedes the COX1 gene, (2) two tRNA genes coding leucine are located on different chains of mitochondrial DNA, (3) a cluster of tRNA genes W–V precedes the 12s rRNA gene, (4) genes 16s rRNA and COX1 flank a group of uniquely arranged genes and the control region Y–L–( CR )– NAD2 – Q–C –M–K (genes located on the negative chain are underlined).…”

“…Synapomorphic status of bifurcating setae. Based on a consensus of molecular and morphological phylogenetic analyses, there is now very strong support for a close relationship between Eriophyoidea and Nematalycidae [ 4 , 5 , 44 , 51 , 52 , 53 ]. The bifurcating form of setae in Eriophyoidea provides additional evidence for this affiliation.…”

“…The remaining 166 sequences were aligned and modified as described in [ 40 ]. The mitogenomic dataset included 11 complete sequences of mitochondrial genomes, among them 7 sequences from Genbank [ 18 , 32 , 40 , 43 , 44 , 45 ] and 4 sequences obtained in this study ( Table 1 ).…”

Molecular Aspects of Gall Formation Induced by Mites and Insects

“…On the other hand, Hearn et al [ 16 ] reported that they did not detect the expression of genes encoding for phytohormones in the young larvae of the gall wasp, B. pallida . In addition, in the genome of the mite, Fragariocoptes setiger (Nalepa, 1894) (Phytoptidae), which causes galls on strawberry leaves, phytohormone genes and any other genes that could have entered the mite genome from the plant as a result of horizontal transfer were not found [ 48 ]. Therefore, if there are parasite–plant pairs in which gallogenesis is induced by the endogenous phytohormones of parasitic arthropods, then there are other cases, e.g., the pairs involving the wasp B. pallida or the mite F. setiger , in which gallogenesis is initiated by a different but yet unexplained mechanism.…”

Microbiome and plant cell transformation trigger insect gall induction in cassava

“…Insect-associated microorganisms could be important mediators of interactions between insects and plants ( Hammer and Bowers, 2015 ; Sugio et al., 2015 ; Wielkopolan and Jakubowska, 2021 ; Coolen et al., 2022 ). Symbiotic relationships between inducing insects and microorganisms have been hypothesised to be involved in plant gall development ( Hansen and Moran, 2014 ; Tooker and Helms, 2014 ; Gätjens-Boniche, 2019 ; Klimov et al., 2022 ). Delivery of bacteria under natural or artificial conditions by insect vectors has been reported in many insect–plant interactions ( Zeidan and Czosnek, 1994 ; Galambos et al., 2021 ; Wielkopolan and Jakubowska, 2021 ; Ratcliffe et al., 2022 ).…”