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

ABSTRACTBackgroundOribatid 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.ResultsWe 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.ConclusionsWith 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.

De novo biosynthesis of simple aromatic compounds by an arthropod ( Archegozetes longisetosus )

The ability to synthesize simple aromatic compounds is well known from bacteria, fungi and plants, which all share an exclusive biosynthetic route—the shikimic acid pathway. Some of these organisms further evolved the polyketide pathway to form core benzenoids via a head-to-tail condensation of polyketide precursors. Arthropods supposedly lack the ability to synthesize aromatics and instead rely on aromatic amino acids acquired from food, or from symbiotic microorganisms. The few studies purportedly showing de novo biosynthesis via the polyketide synthase (PKS) pathway failed to exclude endosymbiotic bacteria, so their results are inconclusive. We investigated the biosynthesis of aromatic compounds in defence secretions of the oribatid mite Archegozetes longisetosus . Exposing the mites to a diet containing high concentrations of antibiotics removed potential microbial partners but did not affect the production of defensive benzenoids. To gain insights into benzenoid biosynthesis, we fed mites with stable-isotope labelled precursors and monitored incorporation with mass spectrometry. Glucose, malonic acid and acetate, but not phenylalanine, were incorporated into the benzenoids, further evidencing autogenous biosynthesis. Whole-transcriptome sequencing with hidden Markov model profile search of protein domain families and subsequent phylogenetic analysis revealed a putative PKS domain similar to an actinobacterial PKS, possibly indicating a horizontal gene transfer.

Cytological evidence for automictic thelytoky in parthenogenetic oribatid mites (Acari, Oribatida): Synaptonemal complexes confirm meiosis in Archegozetes longisetosus

Diplo-diploid parthenogenesis (thelytoky) is a widespread phenomenon in the mite taxon Sarcoptiformes, and is unusually frequent in the suborder Oribatida, where it characterizes almost 10% of extant species, including whole genera and families. Based on molecular and cytological data, terminal fusion automixis with an inverted meiotic sequence based on holokinetic chromosomes has been suggested as the reproductive mode in these mites. However, unequivocal structural evidence for meiosis is missing. The model organism Archegozetes longisetosus, a thelytokous member of the parthenogenetic family Trhypochthoniidae, was studied to gain ultrastructural insight in oocyte progression and meiotic processes. In this study, ovarian nuclear organization of its tritonymphal instar was examined by transmission electron microscopy (TEM). Numerous synaptonemal complexes were observed in the ovary, unequivocally confirming automixis (meiotic thelytoky) in oribatid mites for the first time. No recombination nodules were found. The nuclei are transcriptionally active in late prophase. Inverted meiosis is discussed as a result of the spatial arrangement of chromatid segregation.

Effects of green algae and napa cabbage on life-history parameters and gut microflora of Archegozetes longisetosus (Acari: Oribatida) under laboratory conditions

We compared the effect of green algae (dominated byProtococcussp.) and the earlier studied napa cabbage on the life-history parameters and gut microflora of the oribatid miteArchegozetes longisetosus(a chelicerate model organism). Napa cabbage contained more crude ash, protein, and crude fibre than green algae, butA.longisetosusdeveloped better on the latter food, displaying higher fertility, lower mortality of offspring and shorter development than on napa cabbage. The gut microflora ofA.longisetosusdepended on the kind of food and developmental stage of this mite. The adults fed with napa cabbage had more abundant and more active microflora than those fed with green algae, whereas in the tritonymphs the microflora was more abundant when they were fed with green algae, and was more active in the group fed with napa cabbage. Irrespective of the treatment, the highest percentage of the isolated bacteria were gram-positive bacilli or gram-negative bacteria, but the mites feeding onProtococcussp. contained no cocci, whereas those fed with cabbage had no gram-positive bacteria.