Identification of Zoonotic Tick-Borne Pathogens from Korean Water Deer ( <i>Hydropotes inermis argyropus</i> )

Abstract

Korean water deer (<i>Hydropotes inermis argyropus</i>) are widespread in the Republic of Korea (ROK). Mostly, Korean water deer are essential hosts for maintaining ticks and tick-borne diseases (TBDs). Here, we investigated the prevalence of tick-borne pathogens (TBPs) among rescued Korean water deer. <i>Anaplasma phagocytophilum</i> (21.4%, 6/28), <i>Anaplasma capra</i> (14.3%, 4/28), <i>Babesia capreoli</i> (3.6%, 1/28), and <i>Coxiella burnetii</i> (3.6%, 1/28) were detected, but <i>Borrelia burgdorferi</i>, <i>Ehrlichia</i>, <i>Rickettsia</i>, and <i>Theileria</i> infections were not found. <i>A. phagocytophilum</i> was the most commonly detected pathogen, and co-infection with <i>A</i>. <i>capra</i> and <i>B</i>. <i>capreoli</i> was also noted in one Korean water deer. To our knowledge, this is the first article of <i>B</i>. <i>capreoli</i> infection in Korean water deer in the ROK. The infecting isolate of <i>A. phagocytophilum</i> was genetically characterized by 16S ribosomal RNA (rRNA) gene and ankyrin-related protein (<i>ankA</i>) gene. Although the 16S rRNA gene alone may not be informative enough to delineate distinct host species, <i>ankA</i>-based phylogeny revealed a high identity of Korean water deer sequences with those of the causative agent of human granulocytic anaplasmosis. <i>A. capra</i> was detected by using citrate synthase gene (<i>gltA</i>), heat-shock protein (<i>groEL</i>), and major surface protein 4 (<i>msp4</i>) genes. Phylogenetic tree based on these gene markers revealed that there were at least two distinct variants within <i>A. capra</i> circulating in the ROK. One variant originated from different hosts including humans, ticks, goats, and sheep, whereas the other variant was reported recently in Korean water deer in the ROK. Consequently, these sequences were identified to belong to a zoonotic species. Sequencing analysis of the 18S rRNA gene revealed that our isolate belonged to <i>B. capreoli</i> and was distinct from <i>Babesia divergens</i> and <i>Babesia venatorum</i>. Moreover, our isolate showed 92.2% homology with <i>B. capreoli</i> sequences, indicating that these differences may be attributed to the different tick species that transmit <i>B. capreoli</i> or to different host species. Genotyping and phylogenetic analysis of <i>C. burnetii</i> based on 16S rRNA and IS1111 genes revealed that our isolate was grouped with several strains of <i>C. burnetii</i> and was genetically distant from <i>Coxiella</i>-like bacteria isolates. The present results highlight that Korean water deer act as potential reservoir hosts for zoonotic TBPs, and thus play an important role in the transmission of TBDs in humans, animals, and livestock.