Comparative genomics of Sarcoptes scabiei provide new insights into adaptation to permanent parasitism and within‐host species divergence

Abstract

Sarcoptes scabiei is the causative agent of a highly contagious skin disease in humans and more than 100 mammals. Here, we reported the first chromosome‐level reference genome of S. scabiei isolated from rabbits, with a contig N50 size of 5.92 Mb, a total assembled length of 57.30 Mb, ∼12.65% repetitive sequences and 9333 predicted protein‐coding genes. The phylogenetic tree based on 1338 shared high‐confidence single‐copy orthologous genes estimated that the mammalian ectoparasite S. scabiei and the plant‐feeding mite Tetranychus urticae separated ∼340 million years ago. Both neighbour‐joining tree and principal component analysis of 20 mite populations isolated from four hosts (humans, pigs, dogs and rabbits) distributed in three countries (China, Australia and the USA) consistently supported genetic subdivisions according to host species rather than geographical location. The demographic history of S. scabiei reconstructed by multiple sequentially Markovian coalescent analysis suggested that S. scabiei isolated from rabbits, humans, dogs and pigs diverged ∼5000 years ago. Investigation of the homeobox (Hox) genes revealed that S. scabiei contains 8 of 10 canonical Hox genes that are present in the arthropod ancestor, and the absence of the Abd‐A gene may correlate with the long gap between their front and back legs. Comparative genomics demonstrated that genes specific to scabies mites were mainly enriched in nutrition digestive systems, whereas genes in the families that involved detoxification (cytochrome P450, carboxyl/cholinesterases and the ATP‐binding cassette transporter C group) were extremely contracted compared with that of other mites analysed in this study. Selective sweep analysis of mite populations from various pairs of two out of the four host species revealed that the strongest selective sweep signals were mainly enriched in cysteine‐type peptidase activity and apoptosis. The results provided clues for the mechanisms of S. scabiei adaptation to a permanent parasitic lifestyle and knowledge that would enable further control of this highly contagious skin disease.

Role of the Hox Genes, Sex combs reduced, Fushi tarazu and Antennapedia, in Leg Development of the Spider Mite Tetranychus urticae

“…Therefore, we speculate that different or altered cofactors in T. urticae led to changes in Hox gene function, as previous studies have shown that mite genomes are much smaller than those of other arthropods [ 35 ] and that Hox genes deletion varies among different mites [ 36 , 37 , 38 ]. In this regard, it has been suggested that Abdominal-A ( Abd-A ) was responsible for the morphological diversity of mites [ 39 ]. In addition, the relationship between Hox genes and the target gene ( DlI ) differed significantly in different arthropods.…”

Sarcoptic mange in Felidae: does Sarcoptes scabiei var. felis exist? A first molecular study

“…felis of S. scabiei may not exist. This conclusion needs confirmation by further molecular analyses based, in parallel, on microsatellite markers and innovative genomic techniques [ 9 , 18 , 22 , 46 ]. A larger dataset of mites from diversified geographical areas and carnivore communities is similarly recommended.…”

“…Thus, the continued use of the term “var” in the past scientific literature referring to Sarcoptes host-specific subspecies or “strains” may be outdated or even misleading, appearing of little relevance. Accordingly, we believe that the contemporary understanding of the broad and sometimes unexpected host associations of S. scabiei should cautiously lead to the dismission of the historic nomenclature based on questionable mite morphological differences and the exclusive view of strict host association [ 46 ].…”