title: Diversity and vector biology of ectoparasites of small mammals in Saudi Arabia: implications for bacterial zoonoses
Creators: name: Alkathiry, Hadil
Publisher: name: University of Liverpool Repository
Year: 2024

description: Globally, rodents are a major reservoir for many vector-borne bacterial diseases that are important for public and veterinary health. Due to their widespread distribution across ecological niches and their capacity to host a vast array of ectoparasites, including ticks, mites,
and fleas, rodents are considered important hosts that aid in the persistence and spread of zoonotic illnesses such as scrub typhus (caused by Orientia spp.), Lyme disease and
rickettsioses. The objectives of the current study were to (i) investigate the chigger mite fauna and other ectoparasites on rodents in two regions: Asir and Al-Bahah provinces (Saudi Arabia); (ii) determine the identity and prevalence of bacterial pathogens and symbionts in ectoparasites and hosts in these regions, with a special focus of on Orientia; and (iii) analyse the metagenome of the chigger Pentidionis agamae, identified here as a potential vector of
Orientia in Saudi Arabia. Small mammals were trapped in southwest Saudi Arabia and in total, 7,392 chiggers, 368 ticks of various stages, 146 mesostigmatid mites, and 53 fleas (Parapulex chephrensis) were collected from 82 hosts. Internal rodent organs were also harvested and
stored in 70% ethanol. Chiggers comprised 20 species belonging to nine genera, including a newly described species (Odontacarus thesigeri) and five species that constituted new records for the Arabian Peninsula. The most prevalent chigger species in Asir were Ericotrombidium kazeruni and Ericotrombidium caucasicum, while Schoutedenichia zarudnyi
and P. agamae were dominant in Al-Bahah. Phylogenetic analysis of COI fragments of eight chigger species revealed a monophyletic grouping for each chigger genus. Phylogenetic analysis and ASAP (“assemble species by automatic partitioning”) analysis of COI sequences
of mesostigmatid mites showed a distinct operational taxonomic unit that may represent a new Dermanyssus spp. The morphology of immature ticks assigned the specimens to Rhipicephalus spp. and Haemaphysalis spp., while phylogenetic trees were constructed based
on COI, 12S rRNA, and 16S rRNA sequences, revealing novel clades of Rhipicephalus and Haemaphysalis ticks in Asir. Thirty-two per cent of tested Rhipicephalus spp. and
Haemaphysalis spp. were found to be infected with Ehrlichia spp., forming two distinct clades separated by geographical regions. Wolbachia symbiont detection using the wsp gene was conducted on 53 flea samples and 17 chigger pools from Asir and sequences matched supergroups A, B, and V, while two clusters were distinct from known supergroups. The amplification of traD and htrA for Orientia screening was conducted for rodent organs and 165 chigger pools. Seven rodents and two chigger pools of Microtrombicula muhaylensis and
P. agamae (sample R9P) were found to be Orientia positive. Phylogenetic analysis of the R9P htrA sequence revealed a single clade shared with Candidatus (Ca.) O. chuto htrA sequences from A. dimidiatus tissues collected in Asir. This is the first time that DNA from Ca. O. chuto
has been found in potential vector species from this region, where it is geographically distant from a reported human case in Dubai. Metagenomic assembly and phylogenetic analysis of Wolbachia detected in P. agamae positioned a novel strain, designated as wPaga, within its
own distinct clade, namely supergroup X, which segregated with other divergent supergroups. Moreover, the analysis of contigs from all three P. agamae pools identified sequences assigned to Spirochaetes. Based on 16S rRNA and sequence typing genes, these were found to represent a Borrelia clade associated with rodents that has not been detected in arthropods previously. Finally, the metagenomic analysis allowed for the assembly of three mitochondrial genomes from different P. agamae pools, enabling intraspecific comparisons. In summary, these findings highlight the hidden biology of rodent ectoparasites, zoonotic agents, and arthropod symbionts in a highly neglected biogeographical region.