Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan

The diversity and prevalence of canine vector-borne pathogens (VBPs) in Bhutan have to date remained unexplored, whilst recent epidemiological surveys in other South Asian nations have found diseases caused by VBPs to be rife in local dog populations. Importantly, many of such VBPs can infect people...

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Main Authors: Lucas G. Huggins, Ugyen Namgyel, Pelden Wangchuk, Ushani Atapattu, Rebecca Traub, Vito Colella
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:One Health
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352771424001654
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author Lucas G. Huggins
Ugyen Namgyel
Pelden Wangchuk
Ushani Atapattu
Rebecca Traub
Vito Colella
author_facet Lucas G. Huggins
Ugyen Namgyel
Pelden Wangchuk
Ushani Atapattu
Rebecca Traub
Vito Colella
author_sort Lucas G. Huggins
collection DOAJ
description The diversity and prevalence of canine vector-borne pathogens (VBPs) in Bhutan have to date remained unexplored, whilst recent epidemiological surveys in other South Asian nations have found diseases caused by VBPs to be rife in local dog populations. Importantly, many of such VBPs can infect people as well, with a building body of evidence identifying potentially zoonotic rickettsial organisms infecting humans in Bhutan. Given the lack of data on canine pathogens in Bhutan we employed a suite of deep-sequencing metabarcoding methods using Oxford Nanopore Technologies' MinION™ device to holistically characterise the bacterial, apicomplexan and filarial worm blood-borne pathogens of dogs in the country's south. Of the 95 stray, owned and community dogs sampled 78% (95% CI = 69%–85%) were infected with at least one VBP. Pathogen species detected were highly diverse including the bacteria Mycoplasma haemocanis in 16% (95% CI: 10–24%), Ehrlichia canis in 4% (95% CI: 2–10%), Anaplasma platys in 2% (95% CI: 0.5–7%) of dogs as well as the zoonotic species Bartonella clarridgeiae in 1% (95% CI: 0.1–6%), a potentially novel Bartonella spp. and an Ehrlichia chaffeensis-like bacterium, both in 1% (95% CI: 0.1–6%) of dogs. The apicomplexan haemoparasites Hepatozoon canis in 62% (95% CI: 52–71%), Babesia gibsoni in 45% (95% CI: 36–55%) and Babesia vogeli in 3% (95% CI: 1–9%) of dogs were also detected. Finally, 5% (95% CI: 2–12%) of dogs were found to be infected with the filarioid Acanthocheilonema reconditum and 1% (95% CI: 0.1–6%) with zoonotic Dirofilaria sp. hongkongensis. One canine was found positive to the filarioid Setaria tundra, a species normally found infecting cervids. The elucidated diversity of VBP communities highlights the strength of assumption-free diagnostics, such as metabarcoding, in detecting rare, novel, and unexpected pathogens. This approach to identifying pathogen diversity is of critical importance when investigating regions and populations that have thus far been neglected, with the findings aiding the development of future One Health informed strategies for disease control.
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spelling doaj-art-3b03b7c0069b413683a2e02f0cc5b0ac2025-08-20T02:37:05ZengElsevierOne Health2352-77142024-12-011910083910.1016/j.onehlt.2024.100839Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from BhutanLucas G. Huggins0Ugyen Namgyel1Pelden Wangchuk2Ushani Atapattu3Rebecca Traub4Vito Colella5Melbourne Veterinary School, Faculty of Science, University of Melbourne, Parkville, Victoria 3050, Australia; Corresponding author.National Centre for Animal Health, Serbithang, Thimphu 11001, BhutanNational Centre for Animal Health, Serbithang, Thimphu 11001, BhutanMelbourne Veterinary School, Faculty of Science, University of Melbourne, Parkville, Victoria 3050, AustraliaMelbourne Veterinary School, Faculty of Science, University of Melbourne, Parkville, Victoria 3050, Australia; CityU Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong KongMelbourne Veterinary School, Faculty of Science, University of Melbourne, Parkville, Victoria 3050, AustraliaThe diversity and prevalence of canine vector-borne pathogens (VBPs) in Bhutan have to date remained unexplored, whilst recent epidemiological surveys in other South Asian nations have found diseases caused by VBPs to be rife in local dog populations. Importantly, many of such VBPs can infect people as well, with a building body of evidence identifying potentially zoonotic rickettsial organisms infecting humans in Bhutan. Given the lack of data on canine pathogens in Bhutan we employed a suite of deep-sequencing metabarcoding methods using Oxford Nanopore Technologies' MinION™ device to holistically characterise the bacterial, apicomplexan and filarial worm blood-borne pathogens of dogs in the country's south. Of the 95 stray, owned and community dogs sampled 78% (95% CI = 69%–85%) were infected with at least one VBP. Pathogen species detected were highly diverse including the bacteria Mycoplasma haemocanis in 16% (95% CI: 10–24%), Ehrlichia canis in 4% (95% CI: 2–10%), Anaplasma platys in 2% (95% CI: 0.5–7%) of dogs as well as the zoonotic species Bartonella clarridgeiae in 1% (95% CI: 0.1–6%), a potentially novel Bartonella spp. and an Ehrlichia chaffeensis-like bacterium, both in 1% (95% CI: 0.1–6%) of dogs. The apicomplexan haemoparasites Hepatozoon canis in 62% (95% CI: 52–71%), Babesia gibsoni in 45% (95% CI: 36–55%) and Babesia vogeli in 3% (95% CI: 1–9%) of dogs were also detected. Finally, 5% (95% CI: 2–12%) of dogs were found to be infected with the filarioid Acanthocheilonema reconditum and 1% (95% CI: 0.1–6%) with zoonotic Dirofilaria sp. hongkongensis. One canine was found positive to the filarioid Setaria tundra, a species normally found infecting cervids. The elucidated diversity of VBP communities highlights the strength of assumption-free diagnostics, such as metabarcoding, in detecting rare, novel, and unexpected pathogens. This approach to identifying pathogen diversity is of critical importance when investigating regions and populations that have thus far been neglected, with the findings aiding the development of future One Health informed strategies for disease control.http://www.sciencedirect.com/science/article/pii/S2352771424001654ZoonosisNext-generation sequencingMinIONEhrlichiaDirofilaria sp. hongkongensisBartonella
spellingShingle Lucas G. Huggins
Ugyen Namgyel
Pelden Wangchuk
Ushani Atapattu
Rebecca Traub
Vito Colella
Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan
One Health
Zoonosis
Next-generation sequencing
MinION
Ehrlichia
Dirofilaria sp. hongkongensis
Bartonella
title Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan
title_full Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan
title_fullStr Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan
title_full_unstemmed Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan
title_short Metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector-borne pathogens from neglected regions: A case study investigating dogs from Bhutan
title_sort metabarcoding using nanopore sequencing enables identification of diverse and zoonotic vector borne pathogens from neglected regions a case study investigating dogs from bhutan
topic Zoonosis
Next-generation sequencing
MinION
Ehrlichia
Dirofilaria sp. hongkongensis
Bartonella
url http://www.sciencedirect.com/science/article/pii/S2352771424001654
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