Comparative genomics of juvenile hormone biosynthesis in the ticks, Dermacentor variabilis, Ixodes scapularis, and Ornithodoros turicata

Ticks are obligatory hematophagous arthropods and important vectors of human and animal diseases, like Lyme disease and Rocky Mountain spotted fever.  They rank second only to mosquitoes as vectors of life-threatening or debilitating diseases and transmit a wider variety of pathogen-borne diseases than any other arthropod.  Juvenile hormone (JH) controls the growth, development, metamorphosis, and reproduction of insects, and each enzyme in the JH pathway is a potential target for chemical control.  For many years, the general assumption has been that the role of JH in the regulation of development in ticks and other acarines is similar to insects. Although researchers in one study were not able to find the common insect JHs in a hard and soft tick species, it is difficult to prove the negative.  Next-gen sequencing of the tick synganglion transcriptome provides another approach for examining each step in JH III biosynthesis and was conducted in adults of the American dog tick, Dermacentor variabilis, the deer tick, Ixodes scapularis, and the relapsing fever tick, Ornithodoros turicata.  The enzymes involved in the beginning of the JH pathway from acetyl-CoA to farnesyl diphosphate (the mevalonate branch) were found in all of the ticks studied.  However, the JH branch from farnesyl diphosphate to JH III was not found.  Methyltransferases (MTs) were present that showed similarity as high as 36% at the amino acid level to insect JH acid methyltransferase (JHAMT) . However, when the tick MTs were compared to the known insect JHAMTs from several insect species at the amino acid level, the former lacked the farnesoic acid binding motif. Also the P450 shown in insects to add the C10,11 epoxide to methyl farnesoate, CYP15, was not present in the ticks studied.  This is the first report identifying the putative enzymes involved in the mevalonate branch of the JH pathway from acetyl-CoA to farnesyl diphosphate in any tick species, while providing evidence that the insect JH branch is absent in both the hard and soft ticks examined.  The functional significance of the mevalonate pathway in ticks is unknown but based on its role in insects is likely also important in the developmental biology of chelicerates.