Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia

Alkathiry, Hadil A, Alghamdi, Samia Q, Sinha, Amit, Margos, Gabriele, Stekolnikov, Alexandr A, Alagaili, Abdulaziz N, Darby, Alistair C, Makepeace, Benjamin L and Khoo, Jing Jing ORCID: 0000-0003-1285-6052 (2024) Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia. BMC Genomics, 25 (1). 380-.

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Abstract

<jats:title>Abstract</jats:title><jats:sec> <jats:title>Background</jats:title> <jats:p>Trombiculid mites are globally distributed, highly diverse arachnids that largely lack molecular resources such as whole mitogenomes for the elucidation of taxonomic relationships. Trombiculid larvae (chiggers) parasitise vertebrates and can transmit bacteria (<jats:italic>Orientia</jats:italic> spp.) responsible for scrub typhus, a zoonotic febrile illness. <jats:italic>Orientia tsutsugamushi</jats:italic> causes most cases of scrub typhus and is endemic to the Asia-Pacific Region, where it is transmitted by <jats:italic>Leptotrombidium</jats:italic> spp. chiggers. However, in Dubai, <jats:italic>Candidatus</jats:italic> Orientia chuto was isolated from a case of scrub typhus and is also known to circulate among rodents in Saudi Arabia and Kenya, although its vectors remain poorly defined. In addition to <jats:italic>Orientia</jats:italic>, chiggers are often infected with other potential pathogens or arthropod-specific endosymbionts, but their significance for trombiculid biology and public health is unclear.</jats:p> </jats:sec><jats:sec> <jats:title>Results</jats:title> <jats:p>Ten chigger species were collected from rodents in southwestern Saudi Arabia. Chiggers were pooled according to species and screened for <jats:italic>Orientia</jats:italic> DNA by PCR. Two species (<jats:italic>Microtrombicula muhaylensis</jats:italic> and <jats:italic>Pentidionis agamae</jats:italic>) produced positive results for the <jats:italic>htrA</jats:italic> gene, although <jats:italic>Ca</jats:italic>. Orientia chuto DNA was confirmed by Sanger sequencing only in <jats:italic>P. agamae</jats:italic>. Metagenomic sequencing of three pools of <jats:italic>P. agamae</jats:italic> provided evidence for two other bacterial associates: a spirochaete and a <jats:italic>Wolbachia</jats:italic> symbiont. Phylogenetic analysis of 16S rRNA and multi-locus sequence typing genes placed the spirochaete in a clade of micromammal-associated <jats:italic>Borrelia</jats:italic> spp. that are widely-distributed globally with no known vector. For the <jats:italic>Wolbachia</jats:italic> symbiont, a genome assembly was obtained that allowed phylogenetic localisation in a novel, divergent clade. Cytochrome c oxidase I (<jats:italic>COI</jats:italic>) barcodes for Saudi Arabian chiggers enabled comparisons with global chigger diversity, revealing several cases of discordance with classical taxonomy. Complete mitogenome assemblies were obtained for the three <jats:italic>P. agamae</jats:italic> pools and almost 50 SNPs were identified, despite a common geographic origin.</jats:p> </jats:sec><jats:sec> <jats:title>Conclusions</jats:title> <jats:p><jats:italic>P. agamae</jats:italic> was identified as a potential vector of <jats:italic>Ca.</jats:italic> Orientia chuto on the Arabian Peninsula. The detection of an unusual <jats:italic>Borrelia</jats:italic> sp. and a divergent <jats:italic>Wolbachia</jats:italic> symbiont in <jats:italic>P. agamae</jats:italic> indicated links with chigger microbiomes in other parts of the world, while <jats:italic>COI</jats:italic> barcoding and mitogenomic analyses greatly extended our understanding of inter- and intraspecific relationships in trombiculid mites.</jats:p> </jats:sec>

Item Type:	Article
Uncontrolled Keywords:	Animals, Rodentia, Trombiculidae, Borrelia, Orientia tsutsugamushi, Wolbachia, Scrub Typhus, DNA, RNA, Ribosomal, 16S, Phylogeny, Saudi Arabia, Multilocus Sequence Typing, Microbiota, Orientia
Divisions:	Faculty of Health and Life Sciences Faculty of Health and Life Sciences > Institute of Infection, Veterinary and Ecological Sciences
Depositing User:	Symplectic Admin
Date Deposited:	19 Apr 2024 08:31
Last Modified:	26 Apr 2024 22:17
DOI:	10.1186/s12864-024-10301-6
Open Access URL:	https://doi.org/10.1186/s12864-024-10301-6
Related URLs:	Author Publisher
URI:	https://livrepository.liverpool.ac.uk/id/eprint/3180450