Yi Sun

Ticks, which are globally distributed, transmit a wide range of human and animal pathogens. Soft and hard ticks are two major tick families exhibiting distinct vector capacities and blood-feeding abilities. However, understanding the genetic basis of these differences is hindered by the scarcity of high-quality tick genomes, particularly for soft ticks. Here, we present high-quality genomes of two soft and two hard tick species of both evolutionary and medical importance, and compare the genomic characteristics of the two tick families. Compared with soft ticks, hard ticks exhibited faster genome evolution, characterized by larger genome sizes, higher rates of gene gain and loss, and a greater number of positively selected genes. Both tick families exhibited frequent positive selection across metabolism and organismal systems, sharing a core set of adaptive genes but undergoing refinement at different sites. Gene families underpinning various vector capacities, including those involved in cuticle structure, heme biosynthesis, egg waxing, and immune pathways, were identified. Additionally, we assembled the genomes of two novel Rickettsia endosymbionts from soft ticks, revealing high genomic divergence and lineage-specific adaptations to their hosts. These genomic resources provide fundamental insights into the genetic basis of tick biology and vector capacity, highlighting the divergent evolutionary strategies of blood-feeding arthropods shaped by their ecological niches.

We report genomic characterization and molecular detection of a previously unrecognized Anaplasma species, provisionally named Candidatus Anaplasma cheelooensis, in goats and ticks in Shandong Province, China. During 2021–2022, metagenomic sequencing of blood from a sick goat kid yielded a 1.13-Mb Anaplasma genome with 45.3% G+C content and only 77.0%–77.6% nucleotide identity to recognized Anaplasma species. Whole-genome and gltA-based phylogenies placed the organism in a distinct lineage related to A. phagocytophilum, A. platys, and A. bovis. Specific PCR detected the organism in 37/53 goat blood samples and 7/145 Haemaphysalis longicornis ticks from the same region; gltA sequences shared 97.9%–100% identity. These findings provide genome-level evidence for a candidate novel Anaplasma species circulating in small ruminants and ticks. Its pathogenicity, vector competence, host range, and zoonotic potential require further investigation.

Ticks, recognized as the second most significant vector of pathogens after mosquitoes, are of considerable interest in medical research. Although mitochondrial genomes are commonly employed in the phylogenetic studies of insects and arthropods, investigations into tick mitochondrial genomes are relatively scarce. The evolutionary and phylogenetic relationships at the family and genus levels remain unresolved. In this study, the mitochondrial genomes of Haemaphysalis warburtoni, Ixodes crenulatus, Rhipicephalus bursa , and Rhipicephalus pumilio were first sequenced and annotated based on the Illumina NovaSeq 6,000 platform, and compared with the mitochondrial genes of 150 other hard ticks. All examined tick mitochondrial genomes exhibit a notable AT bias, with A+T content ranging significantly from 72.28% to 81.06%. They also exhibit distinct codon usage patterns, with most codons ending in either A or U. A phylogenetic analysis, based on 13 protein-coding genes (PCGs), confirms that the Ixodidae family forms a monophyletic group. Based on the phylogenetic analysis of 13 protein-coding genes, the relationships of Ixodidae family as follows: Ixodes + ( Robertsicus + (( Bothriocroton + Archaeocroton + Cryptocroton + Haemaphysalis ) + ( Amblyomma + ( Dermacentor + ( Rhipicentor + ( Hyalomma + Rhipicephalus )))))). This study provides in-depth insights into tick mitochondrial genomes, offering important references for research on their systematics, evolution, and species identification, while also laying the groundwork for tick-borne disease control and public health risk assessment.

SARS-CoV, MERS-CoV, and SARS-CoV-2 have posed tremendous threats to human health, highlighting the necessity of monitoring cross-species transmission of animal coronaviruses to humans. Hedgehogs infected with coronaviruses have been reported in several countries across Europe and Asia, raising concerns about the potential transmission of coronaviruses from hedgehogs to humans. In this study, we investigated coronavirus infections in hedgehogs inhabiting greenspaces in metropolitan Beijing and identified a Merbecovirus subgenus coronavirus with a prevalence rate of 30% (95% CI: 25–35%) among 317 hedgehogs. Phylogenetic analysis of 23 complete viral genome sequences revealed a monophyletic origin, showing close relatedness to Erinaceus hedgehog coronavirus HKU31 (Ea-HedCoV HKU31) with genome-wide nucleotide identities of 93.24–96.42%, and evidence of recombination with Tylonycteris bat coronavirus HKU4. These findings suggest that the increase in wildlife populations associated with urban greenspace development may pose a potential threat to human health that should not be overlooked.

Ticks transmit diverse pathogens, posing significant public health threats in northeastern China; clarifying human-biting tick species and their carried pathogens is crucial for risk assessment and prevention. This study was designed as a pathogen detection and molecular epidemiological investigation. During the May-August period of each of 2023 and 2024, 232 ticks that had bitten humans were collected from a local sentinel hospital. Ticks were morphologically identified, followed by DNA extraction, semi-nested/nested PCR targeting specific genetic markers, and Sanger sequencing to detect bacterial pathogens. Four tick species were found, with Ixodes persulcatus dominant (87.9%), followed by Dermacentor silvarum (6.9%), Haemaphysalis concinna (3.5%), and Haemaphysalis japonica (1.7%). Seven bacterial pathogens were detected, including Candidatus Rickettsia tarasevichiae (35.3%) and Borreliella garinii (17.2%); 49.6% of ticks were pathogen-positive. The coinfection rate was 13.8%, most commonly Candidatus R. tarasevichiae plus B. garinii, and I. persulcatus carried all pathogens. These findings provide basic data on human-biting tick species and their bacterial pathogen spectrum in the region, serving as a reference for subsequent tick-borne disease research and targeted prevention.

Ticks are arthropod vectors capable of transmitting a wide spectrum of pathogens affecting humans and animals. However, we have relatively limited information of their genomic characteristics and the diversity of associated microbiomes. Here we used long- and short-read sequencing on 1,479 samples from 48 tick species across eight genera from China to determine their genome and associated pathogens and microbiome. Through de novo assembly, we reconstructed 7,783 bacterial genomes representing 1,373 bacterial species, of which, 712 genomes represented 32 potentially pathogenic species. Computational analysis found nutritional endosymbionts to be prevalent and highly specific to tick genera. The microbiome genome-wide association study revealed host genetic variants linked to pathogen diversity, abundance and key biological pathways essential to tick biology, including blood-feeding and pathogen invasion. These findings provide a resource for studying the host–microbe interactions within ticks, paving the way for strategies to control tick populations and tick-borne diseases.

Theileria luwenshuni and Babesia spp. Infections

Objects: Vector ticks’ perception of characteristic odors emitted by infected hosts is key to understand tick’s foraging behavior for infected host and design odor-based control strategies for tick-borne diseases. Methods: Laboratory mice knocked out for type I interferon (IFN) receptors (Ifnar^-/-) were used to develop a simulated host by intraperitoneal infection with Bandavirus dabieense (SFTSV). Urine and fecal samples were collected 4 days post-infection and analyzed to detect differential volatile metabolites (DVMs) during infection. Next, the two salient odor cues among the SFTSV-induced host DVMs, indole and 3-methylindole, were used to test the olfactory response of Haemaphysalis. longicornis by electroantennographic detection (EAD) and Y-tube olfactometry, respectively. To gain insight into the potential olfactory mechanism, two olfactory-associated proteins, Niemann-Pick type C2 (NPC2) and Odor Binding Protein-like (OBPL) proteins were annotated from the transcriptomic data derived from H. longicornis forelegs. Online tools were used to predict the ligand binding properties of the two proteins to the two indole candidates. Simultaneously, quantitative RT-PCR using β-actin as an internal reference gene was used to monitor the relative transcript levels of NPC2 and OBPL proteins under the stimulation of two indole candidates. The significantly regulated proteins were cloned and expressed with the vector plasmid pET-28b in vitro. The purified proteins were tested for the binding properties to the two indole candidates. Results: SFTSV-infected Ifnar^-/- mice upregulated 11 DVMs in fecal samples, mostly indoles and phenols, along with indole biosynthesis and related metabolic processes. In the urine samples, 29 DVMs were downregulated in the infected host, with eucalyptol and phenylalanine acid being the most altered. We test the olfactory responses of H. longicornis to indole and 3-methylindole, which influence tick foraging behavior. The olfactometers showed that the tick preferred both indole and 3-methylindole. EAD tests showed that stimulation of the olfactory receptor neuron in Haller’s organ produced significant active potential in response to indoles. Two olfactory proteins, NPC2 and OBPL, were successfully annotated from H. longicornis foreleg transcriptomic data. NPC2 has a β-barrel structure that binds signal chemicals, while OBPL is a classical OBP with a hydrophobic binding cavity. When monitoring the transcript levels of NPC2 and OBPL in the tick forelegs, the increased transcript level (1.2-1.4 folds change) of OBPL was observed following indoles stimulation, compared to the downregulated level (0.6-0.8 folds change) of NPC2 under the same circumstances. The OBPL and NPC2 gene from H. longicornis were successfully cloned and expressed as inclusion proteins respectively. The purified OBPL (20.28 kDa) showed higher affinity for both indole (Ki 2.256μM) and 3-methylindole (Ki 4.191μM) than NPC2 in the competitive fluorescence binding assays with 1-NPN as a competitor. Conclusions: Facilitated by the olfactory OBPL protein in Haller’s organ, H. longicornis smells and is attracted to the characteristic indolic scents of hosts induced by SFTSV infection. Olfactory associations between infected hosts and vector arthropods could provide a new perspective to understand host foraging behavior and design novel control strategies for tick-borne diseases based on pathogen-induced scent according to chemical ecology theory.

Emerging tick-borne infections pose growing public health threats, causing global disease burdens and economic losses. In this study, tick-borne pathogens were detected in ticks collected from ruminants in 19 sites of Khyber Pakhtunkhwa Province, Pakistan, between 2023 and 2024. A total of 989 ticks, belonging to five species, i.e., Hyalomma marginatum, Rhipicephalus microplus, Rhipicephalus sanguineus, Rhipicephalus haemaphysaloides, and Haemaphysalis bispinosa, were tested by specific PCR followed by Sanger sequencing. In total, fourteen pathogens including two Anaplasma species, three Ehrlichia species, three Rickettsia species, one Babesia species, and five Theileria species were identified, with an overall infection rate of 20.2% (95% CI: 17.7–22.7%). Phylogenetic analyses revealed two undefined Ehrlichia species: Candidatus Ehrlichia hyalommae was exclusively detected in Hy. marginatum ticks, while Candidatus Ehrlichia rhipicephalis was only found in R. microplus. Additionally, an undefined Rickettsia, provisionally named Candidatus Rickettsia pakistanensis, was identified, which is phylogenetically close to R. sibirica in North Asia and R. africae in Africa, suggesting its potential pathogenicity to humans. Although coinfections of two pathogens were observed, the coinfection rates were quite low. The findings revealed a significant diversity of tick-borne pathogens in Pakistani ticks, which may pose risks to livestock and humans.

Ticks are important vectors for pathogen transmission, yet studies on the diversity and distribution of viruses carried by ticks in desert regions remain limited. This study investigated the tick virome in desert areas of Xinjiang, China, and identified two tick species, Hyalomma asiaticum and Rhipicephalus turanicus. A total of 30 meta-transcriptome sequencing libraries were constructed from ticks pooled by location, tick species, sex, and host. The proportion of viral reads ranged from 0.004% to 0.165%, and significant differences in viral alpha- and beta-diversity were observed between the two tick species. A total of 125 complete or nearly complete viral genomes were classified into 5 families of positive-sense single-stranded RNA viruses, 6 families of negative-sense single-stranded RNA viruses, and 2 families of double-stranded RNA viruses. Twenty-eight viral species were identified, including 20 known viruses and 8 novel viruses from the genera Orthonairovirus, Quaranjavirus, and Mitovirus, and families Peribunyaviridae and Narnaviridae. Notably, the discovery of Desert orthonairovirus, Desert quaranjavirus, and Desert peribunya-like virus revealed a potential new role for desert ticks as viral vectors. Among the other 25 viruses, 12 were specific to H. asiaticum, and 9 were specific to R. turanicus. This study highlights the diversity of tick-borne viruses in Xinjiang’s desert regions, their distribution across different tick species, and underscores the importance of these tick species in pathogen transmission. These findings provide scientific evidence for further research into viral circulation in desert ecosystems and the potential public health threats posed by tick-borne pathogens.