Tick-Borne bacterial and protozoan animal pathogens shape the native microbiome within Hyalomma anatolicum anatolicum and Rhipicephalus microplus tick vectors

Abstract

BackgroundTicks vector a variety of bacterial, viral, and protozoan pathogens of public and animal health significance. Ticks also harbor a diverse community of microbes linked with their biological processes like hematophagy and hence vector competence. The interactions between bacterial and/or protozoan pathogens and their tick vector microbiome are yet to be investigated. In lieu of this, this study was designed to define the microbial composition of uninfected and infected Hyalomma (H.) anatolicum anatolicum and Rhipicephalus (R.) microplus tick species. Methodology/Principal findingsA total of 320 H. anatolicum and R. microplus were screened for the presence of the protozoan (Theileria sp.), and bacterial (Anaplasma marginale) pathogens by PCR. Subsequently, the microbiome of uninfected and infected individual H. anatolicum and R. microplus were analyzed. The highly conserved V1-V3 region of the 16S rRNA gene was sequenced using the MiSeq Illumina platform. The microbiome of female H. anatolicum anatolicum ticks was dominated by the endosymbiont Candidatus Midichloria mitochondrii (CMM) and Francisella-like endosymbiont (FLE) which were not affected by pathogen infection. Ehrlichia species was detected in A. marginale-infected male H. anatolicum anatolicum (6.2%) as opposed to the Theileria sp.-infected female H. anatolicum anatolicum. Coxiella sp. was also detected in uninfected (2.96%) and A. marginale-infected (4.25%), but not in Theileria sp.-infected R. microplus ticks. Analysis of the eukaryote composition in the respectively ticks also revealed the presence of operational taxonomic units (OTUs) belonging to Plasmodium (P.) falciparum in Theileria sp.-infected H. a. anatolicum and R. microplus ticks, while Hepatozoon americanum detected from Theileria sp.-infected and uninfected H. a. anatolicum. Conclusion and SignificanceThis study establishes the extent of the diversity of microbial community of two important tick species from Pakistan and also revealed the presence of Theileria and A. marginale and additional pathogenic bacteria that could be of public health significance. We hypothesized that infection with either a protozoan or bacterial pathogen will alter the microbial composition within these tick species. Interestingly, we reported the detection of the malarial parasite (P. falciparum) from ticks infected with the protozoan pathogen (Theileria sp.). Further validation experiments are required on endosymbionts and pathogens of ticks to investigate how they could be important in the epidemiology of human and animal pathogens.