Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia
Abstract Background 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 (Orientia spp.) resp...
| Glavni autori: | , , , , , , , , |
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| Format: | Članak |
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BMC
2024-04-01
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| Serija: | BMC Genomics |
| Teme: | |
| Online pristup: | https://doi.org/10.1186/s12864-024-10301-6 |
| _version_ | 1827277281302675456 |
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| author | Hadil A. Alkathiry Samia Q. Alghamdi Amit Sinha Gabriele Margos Alexandr A. Stekolnikov Abdulaziz N. Alagaili Alistair C. Darby Benjamin L. Makepeace Jing Jing Khoo |
| author_facet | Hadil A. Alkathiry Samia Q. Alghamdi Amit Sinha Gabriele Margos Alexandr A. Stekolnikov Abdulaziz N. Alagaili Alistair C. Darby Benjamin L. Makepeace Jing Jing Khoo |
| author_sort | Hadil A. Alkathiry |
| collection | DOAJ |
| description | Abstract Background 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 (Orientia spp.) responsible for scrub typhus, a zoonotic febrile illness. Orientia tsutsugamushi causes most cases of scrub typhus and is endemic to the Asia-Pacific Region, where it is transmitted by Leptotrombidium spp. chiggers. However, in Dubai, Candidatus 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 Orientia, chiggers are often infected with other potential pathogens or arthropod-specific endosymbionts, but their significance for trombiculid biology and public health is unclear. Results Ten chigger species were collected from rodents in southwestern Saudi Arabia. Chiggers were pooled according to species and screened for Orientia DNA by PCR. Two species (Microtrombicula muhaylensis and Pentidionis agamae) produced positive results for the htrA gene, although Ca. Orientia chuto DNA was confirmed by Sanger sequencing only in P. agamae. Metagenomic sequencing of three pools of P. agamae provided evidence for two other bacterial associates: a spirochaete and a Wolbachia symbiont. Phylogenetic analysis of 16S rRNA and multi-locus sequence typing genes placed the spirochaete in a clade of micromammal-associated Borrelia spp. that are widely-distributed globally with no known vector. For the Wolbachia symbiont, a genome assembly was obtained that allowed phylogenetic localisation in a novel, divergent clade. Cytochrome c oxidase I (COI) 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 P. agamae pools and almost 50 SNPs were identified, despite a common geographic origin. Conclusions P. agamae was identified as a potential vector of Ca. Orientia chuto on the Arabian Peninsula. The detection of an unusual Borrelia sp. and a divergent Wolbachia symbiont in P. agamae indicated links with chigger microbiomes in other parts of the world, while COI barcoding and mitogenomic analyses greatly extended our understanding of inter- and intraspecific relationships in trombiculid mites. |
| first_indexed | 2024-04-24T07:18:17Z |
| format | Article |
| id | doaj.art-3ac4a8e4baf44ea6af8ac4e63ade6761 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-24T07:18:17Z |
| publishDate | 2024-04-01 |
| publisher | BMC |
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| series | BMC Genomics |
| spelling | doaj.art-3ac4a8e4baf44ea6af8ac4e63ade67612024-04-21T11:10:03ZengBMCBMC Genomics1471-21642024-04-0125111810.1186/s12864-024-10301-6Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and BorreliaHadil A. Alkathiry0Samia Q. Alghamdi1Amit Sinha2Gabriele Margos3Alexandr A. Stekolnikov4Abdulaziz N. Alagaili5Alistair C. Darby6Benjamin L. Makepeace7Jing Jing Khoo8Imam Mohammad Ibn Saud Islamic UniversityDepartment of Biology, Faculty of Science, Al-Baha UniversityNew England BiolabsNational Reference Centre for Borrelia, Bavarian Health and Food Safety AuthorityLaboratory of Parasitic Arthropods, Zoological Institute of the Russian Academy of Sciences, Universitetskaya embankment 1Department of Zoology, King Saud UniversityInstitute of Infection, Veterinary & Ecological Sciences, University of LiverpoolInstitute of Infection, Veterinary & Ecological Sciences, University of LiverpoolInstitute of Infection, Veterinary & Ecological Sciences, University of LiverpoolAbstract Background 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 (Orientia spp.) responsible for scrub typhus, a zoonotic febrile illness. Orientia tsutsugamushi causes most cases of scrub typhus and is endemic to the Asia-Pacific Region, where it is transmitted by Leptotrombidium spp. chiggers. However, in Dubai, Candidatus 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 Orientia, chiggers are often infected with other potential pathogens or arthropod-specific endosymbionts, but their significance for trombiculid biology and public health is unclear. Results Ten chigger species were collected from rodents in southwestern Saudi Arabia. Chiggers were pooled according to species and screened for Orientia DNA by PCR. Two species (Microtrombicula muhaylensis and Pentidionis agamae) produced positive results for the htrA gene, although Ca. Orientia chuto DNA was confirmed by Sanger sequencing only in P. agamae. Metagenomic sequencing of three pools of P. agamae provided evidence for two other bacterial associates: a spirochaete and a Wolbachia symbiont. Phylogenetic analysis of 16S rRNA and multi-locus sequence typing genes placed the spirochaete in a clade of micromammal-associated Borrelia spp. that are widely-distributed globally with no known vector. For the Wolbachia symbiont, a genome assembly was obtained that allowed phylogenetic localisation in a novel, divergent clade. Cytochrome c oxidase I (COI) 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 P. agamae pools and almost 50 SNPs were identified, despite a common geographic origin. Conclusions P. agamae was identified as a potential vector of Ca. Orientia chuto on the Arabian Peninsula. The detection of an unusual Borrelia sp. and a divergent Wolbachia symbiont in P. agamae indicated links with chigger microbiomes in other parts of the world, while COI barcoding and mitogenomic analyses greatly extended our understanding of inter- and intraspecific relationships in trombiculid mites.https://doi.org/10.1186/s12864-024-10301-6Scrub typhusChiggersMetagenomicsOrientiaWolbachiaBorrelia |
| spellingShingle | Hadil A. Alkathiry Samia Q. Alghamdi Amit Sinha Gabriele Margos Alexandr A. Stekolnikov Abdulaziz N. Alagaili Alistair C. Darby Benjamin L. Makepeace Jing Jing Khoo 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 Scrub typhus Chiggers Metagenomics Orientia Wolbachia Borrelia |
| title | Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia |
| title_full | Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia |
| title_fullStr | Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia |
| title_full_unstemmed | Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia |
| title_short | Microbiome and mitogenomics of the chigger mite Pentidionis agamae: potential role as an Orientia vector and associations with divergent clades of Wolbachia and Borrelia |
| title_sort | microbiome and mitogenomics of the chigger mite pentidionis agamae potential role as an orientia vector and associations with divergent clades of wolbachia and borrelia |
| topic | Scrub typhus Chiggers Metagenomics Orientia Wolbachia Borrelia |
| url | https://doi.org/10.1186/s12864-024-10301-6 |
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