Introduction
Mites (belonging to the Chelicerata, Arachnida, Acari) represent the
most abundant group of species in the subphylum Chelicerata, with
approximately 48,200 described species and an estimated total diversity
up to 1 million species (Halliday et
al. , 2000; Krantz, 2009). Their
ecological niches and lifestyles are varied, such as the free-living
house dust mites, plant-feeding spider mites, predatory mites, and
parasitic mites. Among them, Sarcoptes scabiei represents a very
rare species that has a unique permanent parasitic life in the epidermis
of humans and mammals, including pets (dogs, cats), domestic animals
(e.g., cattle, sheep, pig, horse, and rabbits, etc.), and more than 100
species of wild animals. S. scabiei causes scabies in humans or
sarcoptic mange in animals, which is characterized by irritation,
inflammation, hyperkeratosis, alopecia, pruritis, dermatitis, and
lesions, and is generally accompanied by secondary infections
(Arlian & Morgan, 2017;
Escobar et al. , 2021;
Pence & Ueckermann, 2002). Scabies has
afflicted human societies for at least 2500 years
(Orion et al. , 2006), and was also
the first disease in the history of medicine with a definite known cause
(Friedman, 1934). Not only has scabies
been listed among the top 50 most prevalent diseases and the top 15 most
burdensome dermatological conditions worldwide, but also was officially
designated as a neglected tropical diseases in 2017
(Hay et al. , 2014;
Karimkhani et al. , 2017;
WHO, 2017). A recent study showed that
the human scabies disease burden was estimated as 204 million, with a
prevalence ranging from 0.2% to 71.4%
(Romani et al. , 2015). For
animals, sarcoptic mange provokes distress, causing economic loss in the
livestock industry, disease and death in wildlife
(Fraser et al. , 2016). Therefore,S. scabiei is globally important for public health, pet health,
animal husbandry production, and wildlife conservation.
As a permanent ectoparasitic mite, scabies mites have evolved from
various levels. They have short and stubby legs to facilitate burrowing
and crawling, legs III and IV of both sexes do not extend beyond the
lateral-posterior margin of the idiosoma
(Arlian & Morgan, 2017), while their
relatives, such as surface-feeding mites P. ovis and T.
mercedesae , as well as plant surface resident T. urticae , they
use longer legs to secure themselves on the surface of their hosts.
Moreover, using unique chewing mouthparts instead of piercing-sucking
mouthparts make scabies mites more efficient in burrowing the skin,
contributing to their highly contagious nature, and their activity in
the epidermis induces extreme itching in the mammalian hosts. Compared
with those mites whose niches and lifestyles are diverse, the potential
parasitic mechanisms of S. scabiei in mammal skin are still
poorly understood.
The S. scabiei species that parasitize various hosts are
morphologically indistinguishable and have a ‘high degree of host
specificity and low degree of
cross-infestivity’(Arlian et al. ,
1984; Currier et al. , 2011;
Fain, 1978); therefore, there is an
ongoing debate regarding the taxonomy and origin of S .scabiei from different hosts
(Alasaad et al. , 2011;
Engelman et al. , 2013;
Gakuya et al. , 2011;
Matsuyama et al. , 2015;
Pence & Ueckermann, 2002;
Rasero et al. , 2010;
Walton et al. , 1999). Although
the taxonomy of S. scabiei from different hosts is uncertain, it
is believed that a single, but variable, species that has evolved
adaptations to infect a variety of mammals with limited
cross-infestations between different hosts
(Heukelbach & Feldmeier, 2006;
Kraabl et al. , 2015), e.g.,S. scabiei var. hominis , var. chimp , var.canis , var. suis and so on
(Matsuyama et al. , 2015;
Walton et al. , 1999). However,
the inconsistent use of gene loci across studies and conflicting results
provided by limited gene markers cannot lead to the exact nature of the
host specific adaptations, origin, and species differentiation
(V Andriantsoanirina, Ariey, Izri,
Bernigaud, Fang, Charrel, et al. , 2015;
V Andriantsoanirina, Ariey, Izri,
Bernigaud, Fang, Guillot, et al. , 2015;
V. Andriantsoanirina et al. , 2016;
Gakuya et al. , 2011;
Mofiz et al. , 2016). To explain
these questions, the high-quality genome assembly is essential. At
present, although several versions of S. scabiei genome has been
published, including var. suis , var. canis and var.hominis (Korhonen et al. ,
2020; Mofiz et al. , 2016;
Rider et al. , 2015), among which,
Korhonen et al.(Korhonen et al. ,
2020) reported a scaffold-level genome assembly of S. scabiei,the chromosome-level genome is still absent for the study of this highly
contagious pathogen.
In this study, we employed a combination of sequencing methods,
including Illumina pair-end sequencing, Pacific Biosciences (PacBio)
single-molecule real-time (SMRT) sequencing, and chromosome interaction
mapping (Hi-C) sequencing to get a chromosome-level genome of S.
scabiei that isolated from rabbits. We also carried out whole-genome
resequencing of 13 sarcoptic mite populations and downloaded 7 Illumina
short read datasets from scabies mites distributed in four host species
and three geographical locations to clarify the controversial taxonomic
status and origin of S. scabiei. Comparative genomics study
revealed the potential mechanism of the S. scabiei adaption to
the parasitic life. These results will increase the awareness,
education, and research into taxonomy, pathogenic biology, diagnosis,
treatment, and prevention of scabies or sarcoptic mange.
Materials and Methods
Source of samples
The S. scabiei var. cuniculi was originated from a
farm-collected New Zealand rabbit (Ya’an, China), and maintained in New
Zealand rabbit, the strain has undergone sibmating to maximize
homozygosity.
Twelve scabies mite colonies from three different mammal hosts (one from
dog, three from pigs and eight from rabbits) were collected to perform
re-sequencing (Table S1) . In addition, we also downloaded the 7
publicly available datasets from other representative S. scabieipopulations to do further analysis (Table S1) , including one
isolated from dogs, 2 isolated from humans and 4 isolated from pigs
(Mofiz et al. , 2016;
Rider et al. , 2015).
DNA preparation and genome sequencing
Adult mites, nymphs, larvae and eggs were collected in a 1.5 mL
Eppendorf tube, treated with bleach solution to remove rabbit tissue and
possible microbial contaminants and prepared for DNA extraction.
Pool-staged mites were ground in a glass tissue grinder and DNA
extraction was performed using Qiagen DNA purification kit (Qiagen,
Valencia, CA, USA) according to manufacturer’s protocol and the
extracted DNA was qualified with Qubit 3.0 Fluorometer (Thermo Fisher
Scientific, USA).
To obtain a high-quality scabies mite genome assembly, a combination of
sequencing methods was used, including Illumina paired-end sequencing,
Pacific Biosciences (PacBio) single-molecule real-time (SMRT) sequencing
and chromosome interaction mapping (Hi-C) sequencing. In details, one
short-insert (230 bp, paired-end) DNA library was constructed according
to standard Illumina library prep protocols and sequenced on the
Illumina HiSeq platform as 2 × 150 bp reads, which generated 4.7 Gb raw
data. And then, a 20 kb PacBio long-reads library was constructed using
the BluePippinTM Size-Selection System recommended by Pacific
Biosciences and sequenced on the Pacbio sequel platform. A total of 16
Gb sequencing data was generated, including 1.4 million clean subreads
with an average length of 12.065 kb and N50 value of 19.706 kb. Finally,
to scaffold the genome, one Hi-C library was constructed from the
purified DNA using the Illumina Mate Pair Sample Preparation Kit and
sequenced using the Illumina HiSeq X platform, and 12.7 Gb was
generated.