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Open AccessArticle

An Assessment of the Molecular Diversity of Ticks and Tick-Borne Microorganisms of Small Ruminants in Pakistan

1
Department of Veterinary Biosciences, Melbourne Veterinary School, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Werribee 3030, Victoria, Australia
2
Department of Zoology, Faculty of Chemical and Life Sciences, The Abdul Wali Khan University, Mardan 23200, Khyber Pakhtunkhwa, Pakistan
3
UMR BIPAR, INRAE, ANSES, Ecole Nationale Vétérinaire d’Alfort, Université Paris-Est, 94700 Maisons-Alfort, France
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Microorganisms 2020, 8(9), 1428; https://doi.org/10.3390/microorganisms8091428
Received: 31 August 2020 / Revised: 9 September 2020 / Accepted: 16 September 2020 / Published: 17 September 2020
(This article belongs to the Special Issue Advance in Tick-Borne Diseases Research)
This study investigated ticks and tick-borne microorganisms of small ruminants from five districts of the Federally Administered Tribal Area (FATA) of Pakistan. Morphological (n = 104) and molecular (n = 54) characterization of the ticks revealed the presence of six ixodid ticks: Rhipicephalus (Rh.) haemaphysaloides, Rh. microplus, Rh. turanicus, Haemaphysalis (Hs.) punctata, Hs. sulcata and Hyalomma anatolicum. Phylogenetic analyses of nucleotide sequence data for two mitochondrial (16S and cytochrome c oxidase 1) and one nuclear (second internal transcribed spacer) DNA regions provided strong support for the grouping of the six tick species identified in this study. Microfluidic real-time PCR, employing multiple pre-validated nuclear and mitochondrial genetic markers, detected 11 potential pathogens and endosymbionts in 72.2% of the ticks (n = 54) tested. Rickettsia (R.) massiliae was the most common pathogen found (42.6% of ticks) followed by Theileria spp. (33.3%), Anaplasma (A.) ovis and R. slovaca (25.9% each). Anaplasma centrale, A. marginale, Ehrlichia spp., R. aeschlimannii, R. conorii and endosymbionts (Francisella- and Coxiella-like) were detected at much lower rates (1.9–22.2%) in ticks. Ticks from goats (83.9%) carried significantly higher microorganisms than those from sheep (56.5%). This study demonstrates that ticks of small ruminants from the FATA are carrying multiple microorganisms of veterinary and medical health significance and provides the basis for future investigations of ticks and tick-borne diseases of animals and humans in this and neighboring regions. View Full-Text
Keywords: tick; Anaplasma; goat; Haemaphysalis; microfluidic real-time PCR; Rhipicephalus; Rickettsia; sheep; Theileria; Pakistan tick; Anaplasma; goat; Haemaphysalis; microfluidic real-time PCR; Rhipicephalus; Rickettsia; sheep; Theileria; Pakistan
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Ghafar, A.; Khan, A.; Cabezas-Cruz, A.; Gauci, C.G.; Niaz, S.; Ayaz, S.; Mateos-Hernández, L.; Galon, C.; Nasreen, N.; Moutailler, S.; Gasser, R.B.; Jabbar, A. An Assessment of the Molecular Diversity of Ticks and Tick-Borne Microorganisms of Small Ruminants in Pakistan. Microorganisms 2020, 8, 1428.

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