Transcriptomic analysis of Rhipicephalus microplus hemocytes from female ticks infected with Babesia bovis or Babesia bigemina

Authors: VIMONISH, RUBIKAH - Washington State University; CAPELLI-PEIXOTO, JANAINA - Washington State University; JOHNSON, WENDELL - Retired ARS Employee; Kappmeyer, Lowell; Saelao, Perot; Taus, Naomi; Chung, Chungwon; Ueti, Massaro

Submitted to: Parasites & Vectors
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/7/2025
Publication Date: 2/3/2025
Citation: Vimonish, R., Capelli-Peixoto, J., Johnson, W., Kappmeyer, L.S., Saelao, P., Taus, N.S., Chung, C.J., Ueti, M.W. 2025. Transcriptomic analysis of Rhipicephalus microplus hemocytes from female ticks infected with Babesia bovis or Babesia bigemina. Parasites & Vectors. (18):37. https://doi.org/10.1186/s13071-025-06662-w.
DOI: https://doi.org/10.1186/s13071-025-06662-w

Interpretive Summary: Ticks transmit microorganisms to animals, causing severe diseases and economic loss. Ticks have a rudimentary immune system, that if enhanced, could suppress pathogens transmission. The tick defense mechanism against microorganisms consists of cell-based and fluid based natural responses. Tick cells called hemocytes, which reside in the hemolymph fluid, are known to participate in immune responses against microorganisms, yet our understanding of their anti-protozoan potential is still limited. In this study, we performed gene expression analysis using the RNA-Seq technique, targeting of hemocytes from female Rhipicephalus microplus ticks infected with Babesia parasites. We identified potential natural cellular and humoral immune response genes activated by parasites infection of the tick. The hemocyte response to Babesia included both up-and down-regulated genes. Genes such as defensin, microplusins, and acanthoscurrins were up-regulated in tick hemocytes during infection, indicating the activation of humoral and cellular immune responses. Unexpected findings were that one of the major cellular immune responses, apoptosis, was not active upon Babesia infection, and some genes were even down-regulated. Insights into the tick immune responses against Babesia parasites may lead to hypotheses about their enhancement to diminish transmission of tick-borne diseases.

Technical Abstract: Ticks have a rudimentary immune system as compared to vertebrates. The tick defense mechanism against microorganisms consists of innate cellular and humoral responses. Despite the critical involvement of tick hemocytes in immune responses against bacteria, fungi, and parasites, our understanding of their anti-protozoan potential is still limited. In this study, we performed transcriptomic analysis using high throughput RNA-Seq of Rhipicephalus microplus hemocytes from female ticks infected with protozoa parasites, Babesia bovis or Babesia bigemina. We identified potential innate cellular and humoral immune response markers against Babesia parasites. The hemocyte response to individual Babesia spp. included both up and downregulated genes, however, the magnitude of fold increase was higher in infection with B. bigemina than B. bovis. The upregulation of effector component genes such as defensin, microplusins, acanthoscurrins, leucine-rich repeat containing proteins, thioester containing proteins, trichohyalin, and Von Willebrand factor by tick hemocytes during infection indicated the activation of humoral and cellular immune responses. Unexpected findings were that one of the major cellular immune responses, apoptosis, was not active upon Babesia infection, and genes for homeodomain-interacting protein kinase 2, apoptosis-stimulating of p53 protein 2-like, and endosome/lysosome-associated apoptosis and autophagy regulator family member 2-like were downregulated. The data presented herein provides insights into the tick hemocyte-mediated immune responses against protozoan parasites.