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Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records

Focusing on the utility of ticks as xenosurveillance sentinels to expose circulating pathogens in Kenyan drylands, host-feeding ticks collected from wild ungulates [buffaloes, elephants, giraffes, hartebeest, impala, rhinoceros (black and white), zebras (Grévy’s and plains)], carnivores (leopards, l...

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Autores principales: Ergunay, Koray, Mutinda, Mathew, Bourke, Brian, Justi, Silvia A., Caicedo-Quiroga, Laura, Kamau, Joseph, Mutura, Samson, Akunda, Irene Karagi, Cook, Elizabeth, Gakuya, Francis, Omondi, Patrick, Murray, Suzan, Zimmerman, Dawn, Linton, Yvonne-Marie
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9283121/
https://www.ncbi.nlm.nih.gov/pubmed/35847110
http://dx.doi.org/10.3389/fmicb.2022.932224
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author Ergunay, Koray
Mutinda, Mathew
Bourke, Brian
Justi, Silvia A.
Caicedo-Quiroga, Laura
Kamau, Joseph
Mutura, Samson
Akunda, Irene Karagi
Cook, Elizabeth
Gakuya, Francis
Omondi, Patrick
Murray, Suzan
Zimmerman, Dawn
Linton, Yvonne-Marie
author_facet Ergunay, Koray
Mutinda, Mathew
Bourke, Brian
Justi, Silvia A.
Caicedo-Quiroga, Laura
Kamau, Joseph
Mutura, Samson
Akunda, Irene Karagi
Cook, Elizabeth
Gakuya, Francis
Omondi, Patrick
Murray, Suzan
Zimmerman, Dawn
Linton, Yvonne-Marie
author_sort Ergunay, Koray
collection PubMed
description Focusing on the utility of ticks as xenosurveillance sentinels to expose circulating pathogens in Kenyan drylands, host-feeding ticks collected from wild ungulates [buffaloes, elephants, giraffes, hartebeest, impala, rhinoceros (black and white), zebras (Grévy’s and plains)], carnivores (leopards, lions, spotted hyenas, wild dogs), as well as regular domestic and Boran cattle were screened for pathogens using metagenomics. A total of 75 host-feeding ticks [Rhipicephalus (97.3%) and Amblyomma (2.7%)] collected from 15 vertebrate taxa were sequenced in 46 pools. Fifty-six pathogenic bacterial species were detected in 35 pools analyzed for pathogens and relative abundances of major phyla. The most frequently observed species was Escherichia coli (62.8%), followed by Proteus mirabilis (48.5%) and Coxiella burnetii (45.7%). Francisella tularemia and Jingmen tick virus (JMTV) were detected in 14.2 and 13% of the pools, respectively, in ticks collected from wild animals and cattle. This is one of the first reports of JMTV in Kenya, and phylogenetic reconstruction revealed significant divergence from previously known isolates and related viruses. Eight fungal species with human pathogenicity were detected in 5 pools (10.8%). The vector-borne filarial pathogens (Brugia malayi, Dirofilaria immitis, Loa loa), protozoa (Plasmodium spp., Trypanosoma cruzi), and environmental and water-/food-borne pathogens (Entamoeba histolytica, Encephalitozoon intestinalis, Naegleria fowleri, Schistosoma spp., Toxoplasma gondii, and Trichinella spiralis) were detected. Documented viruses included human mastadenovirus C, Epstein-Barr virus and bovine herpesvirus 5, Trinbago virus, and Guarapuava tymovirus-like virus 1. Our findings confirmed that host-feeding ticks are an efficient sentinel for xenosurveillance and demonstrate clear potential for wildlife-livestock-human pathogen transfer in the Kenyan landscape.
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spelling pubmed-92831212022-07-16 Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records Ergunay, Koray Mutinda, Mathew Bourke, Brian Justi, Silvia A. Caicedo-Quiroga, Laura Kamau, Joseph Mutura, Samson Akunda, Irene Karagi Cook, Elizabeth Gakuya, Francis Omondi, Patrick Murray, Suzan Zimmerman, Dawn Linton, Yvonne-Marie Front Microbiol Microbiology Focusing on the utility of ticks as xenosurveillance sentinels to expose circulating pathogens in Kenyan drylands, host-feeding ticks collected from wild ungulates [buffaloes, elephants, giraffes, hartebeest, impala, rhinoceros (black and white), zebras (Grévy’s and plains)], carnivores (leopards, lions, spotted hyenas, wild dogs), as well as regular domestic and Boran cattle were screened for pathogens using metagenomics. A total of 75 host-feeding ticks [Rhipicephalus (97.3%) and Amblyomma (2.7%)] collected from 15 vertebrate taxa were sequenced in 46 pools. Fifty-six pathogenic bacterial species were detected in 35 pools analyzed for pathogens and relative abundances of major phyla. The most frequently observed species was Escherichia coli (62.8%), followed by Proteus mirabilis (48.5%) and Coxiella burnetii (45.7%). Francisella tularemia and Jingmen tick virus (JMTV) were detected in 14.2 and 13% of the pools, respectively, in ticks collected from wild animals and cattle. This is one of the first reports of JMTV in Kenya, and phylogenetic reconstruction revealed significant divergence from previously known isolates and related viruses. Eight fungal species with human pathogenicity were detected in 5 pools (10.8%). The vector-borne filarial pathogens (Brugia malayi, Dirofilaria immitis, Loa loa), protozoa (Plasmodium spp., Trypanosoma cruzi), and environmental and water-/food-borne pathogens (Entamoeba histolytica, Encephalitozoon intestinalis, Naegleria fowleri, Schistosoma spp., Toxoplasma gondii, and Trichinella spiralis) were detected. Documented viruses included human mastadenovirus C, Epstein-Barr virus and bovine herpesvirus 5, Trinbago virus, and Guarapuava tymovirus-like virus 1. Our findings confirmed that host-feeding ticks are an efficient sentinel for xenosurveillance and demonstrate clear potential for wildlife-livestock-human pathogen transfer in the Kenyan landscape. Frontiers Media S.A. 2022-07-01 /pmc/articles/PMC9283121/ /pubmed/35847110 http://dx.doi.org/10.3389/fmicb.2022.932224 Text en Copyright © 2022 Ergunay, Mutinda, Bourke, Justi, Caicedo-Quiroga, Kamau, Mutura, Akunda, Cook, Gakuya, Omondi, Murray, Zimmerman and Linton. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ergunay, Koray
Mutinda, Mathew
Bourke, Brian
Justi, Silvia A.
Caicedo-Quiroga, Laura
Kamau, Joseph
Mutura, Samson
Akunda, Irene Karagi
Cook, Elizabeth
Gakuya, Francis
Omondi, Patrick
Murray, Suzan
Zimmerman, Dawn
Linton, Yvonne-Marie
Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records
title Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records
title_full Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records
title_fullStr Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records
title_full_unstemmed Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records
title_short Metagenomic Investigation of Ticks From Kenyan Wildlife Reveals Diverse Microbial Pathogens and New Country Pathogen Records
title_sort metagenomic investigation of ticks from kenyan wildlife reveals diverse microbial pathogens and new country pathogen records
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9283121/
https://www.ncbi.nlm.nih.gov/pubmed/35847110
http://dx.doi.org/10.3389/fmicb.2022.932224
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