Genomic and metagenomic analyses of the domestic mite Tyrophagus putrescentiae identify it as a widespread environmental contaminant and a host of a basal, mite-specific Wolbachia lineage (supergroup Q)

Abstract

Tyrophagus putrescentiae (mould mite) is a global, microscopic trophic generalist that commonly occurs in various human-created habitats, causing allergies and damaging stored food. Its ubiquity and extraordinary ability to penetrate research samples or cultures through air currents or by active walking through tights spaces (such as treads of screw caps) may lead to sample contamination and introduction of its DNA to research materials in the laboratory. This prompts a thorough investigation into potential sequence contamination in public genomic databases. The trophic success of T. putrescentiae is primarily attributed to the symbiotic bacteria housed in specialized internal mite structures, facilitating adaptation to varied nutritional niches. However, recent work suggests that horizontal transfer of bacterial/fungal genes related to nutritional functionality may also contribute to the mite’s trophic versatility. This aspect requires independent confirmation. Additionally, T. putrescentiae harbors an uncharacterized and genetically divergent bacterium, Wolbachia, displaying blocking and microbiome-modifying effects. The phylogenomic position and supergroup assignment of this bacterium are unknown. Here, we sequenced and assembled the T. putrescentiae genome, analyzed its microbiome, and performed detailed phylogenomic analyses of the mite-specific Wolbachia. We show that T. putrescentiae DNA is a substantial source of contamination of research samples. Its DNA may inadvertently be co-extracted with the DNA of the target organism, eventually leading to sequence contamination in public databases. We identified a diversity of bacterial species associated with T. putrescentiae, including those capable of rapidly developing antibiotic resistance, such as Escherichia coli. Despite the presence of diverse bacterial communities in T. putrescentiae, we did not detect any recent horizontal gene transfers in this mite species and/or in astigmatid (domestic) mites in general. Our phylogenomic analysis of Wolbachia recovered a basal, mite-specific lineage (supergroup Q) represented by two Wolbachia spp. from the mould mite and a gall-inducing plant mite. Fluorescence in situ hybridization confirmed the presence of Wolbachia inside the mould mite. The discovery of an early derivative Wolbachia lineage (supergroup Q) in two phylogenetically unrelated and ecologically dissimilar mites suggests that this endosymbiotic bacterial lineage formed a long-term association with mites. This finding provides a unique insight into the early evolution and host associations of Wolbachia. Further discoveries of Wolbachia diversity in acariform mites are anticipated.