Molecular evolutionary trends and biosynthesis pathways in the Oribatida revealed by the genome of Archegozetes longisetosus

Background Oribatid mites are a specious order of microarthropods within the subphylum Chelicerata, compromising about 11,000 described species. They are ubiquitously distributed across different microhabitats in all terrestrial ecosystems around the world and were among the first animals colonizing terrestrial habitats as decomposers and scavengers. Noted for their biosynthesis capacities and biochemical diversity, the majority of oribatid mites possess a pair of exocrine opisthonotal oil-glands used for chemical defense and communication. Genomic resources are lacking for oribatids despite their species richness and ecological importance.

Results We used a comparative genomic approach to investigate the developmental, sensory and glandular biosynthetic gene repertoire of the clonal, all-female oribatid mite species Archegozetes longisetosus Aoki, a model species used by numerous laboratories for the past 30 years. Here, we present a 190-Mb genome assembly constructed from Nanopore MinION and Illumina sequencing platforms with 23,825 predicted protein-coding genes. Genomic and transcriptional analyses revealed patterns of reduced body segmentation and loss of segmental identity gene abd-A within Acariformes, and unexpected expression of key eye development genes in these eyeless mites across developmental stages.

Consistent with the soil dwelling lifestyle, investigation of the sensory genes revealed a species-specific expansion of gustatory receptors, the largest chemoreceptor family in the genome used in olfaction, and evidence of horizontally transferred enzymes used in cell wall degradation of plant and fungal matter, both components of the Archegozetes longisetosus diet. Using biochemical and genomic data, we were able to delineate the backbone biosynthesis of monoterpenes, an important class of compounds found in the major exocrine gland system of Oribatida – the oil glands.

Conclusions With the Archegozetes longisetosus genome, we now have the first high-quality, annotated genome of an oribatid mite genome. Given the mite’s strength as an experimental model, the new sequence resources provided here will serve as the foundation for molecular research in Oribatida and will enable a broader understanding of chelicerate evolution.