Differential expression of putative Ornithodoros turicata defensins mediated by tick feeding

Authors: ARMSTRONG, BRITTANY - Baylor College Of Medicine; KNEUBEHL, ALEXANDER - Baylor College Of Medicine; Mitchell Iii, Robert; KRISHNAVAJHALA, APARNA - Baylor College Of Medicine; TEEL, PETE - Texas Agrilife Research; Perez De Leon, Adalberto - Beto; LOPEZ, JOB - Baylor College Of Medicine

Submitted to: Frontiers in Cellular and Infection Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/23/2020
Publication Date: 5/5/2020
Citation: Armstrong, B.A., Kneubehl, A.R., Mitchell III, R.D., Krishnavajhala, A., Teel, P.D., Perez De Leon, A.A., Lopez, J.E. 2020. Differential expression of putative Ornithodoros turicata defensins mediated by tick feeding. Frontiers in Cellular and Infection Microbiology. https://doi.org/10.3389/fcimb.2020.00152.
DOI: https://doi.org/10.3389/fcimb.2020.00152

Interpretive Summary: There is a gap in our knowledge between soft and hard ticks because the latter have been studied more extensively. However, soft ticks are also of veterinary and public health importance. Among the soft ticks in the family Argasidae, the molecular mechanisms of soft tick species in the genus Ornithodoros remain to be fully understood. Specifically, Ornithodoros turicata is known to transmit a bacterium causing relapsing fever in humans, and in the laboratory this soft tick was shown to be a competent vector of African swine fever virus that threatens the pork industry globally. In this regard, it is important to study soft tick vector-pathogen interactions involving components of the tick immune response. Ticks utilize a basic innate immune system consisting of recognition factors and molecular responses to produce antimicrobial peptides, like defensins. In this study we identified and characterized the first putative defensins of O. turicata, which is found primarily in the southwestern United States and parts of Latin America. Molecular assays and computer tools were applied to identify 4 genes containing sequences characteristic of defensins in other invertebrate animals with jointed legs like ticks. Other experiments looked at the expression patterns of these putative defensin genes in organs of O. turicata. Different patterns of expression in soft tick midgut and salivary glands were observed between the 4 putative defensins. This information sets the stage for additional studies in efforts to determine the molecular mechanisms by which O. turicata can become infected with, and transmit disease-causing agents.

Technical Abstract: Additional research on soft ticks in the family Argasidae is needed to bridge the knowledge gap relative to hard ticks of the family Ixodidae; especially, the molecular mechanisms of Ornithodoros biology. Ornithodoros species are vectors of human and animal pathogens that include tick-borne relapsing fever spirochetes and African swine fever virus. Soft tick vector-pathogen interactions involving components of the tick immune response are not understood. Ticks utilize a basic innate immune system consisting of recognition factors and cellular and humoral responses to produce antimicrobial peptides, like defensins. In the present study, we identified and characterized the first putative defensins of Ornithodoros turicata, an argasid tick found primarily in the southwestern United States and regions of Latin America. Four genes (otdA, otdB, otdC, and otdD) were identified through sequencing and their predicted amino acid sequences contained motifs characteristic of arthropod defensins. A phylogenetic analysis grouped these four genes with arthropod defensins, and computational structural analyses further supported the identification. Since pathogens transmitted by O. turicata colonize both the midgut and salivary glands, expression patterns of the putative defensins were determined in these tissues 1 week post engorgement and after molting. Defensin genes up-regulated in the tick midgut 1 week post blood feeding were otdA and otdC, while otdD was up-regulated in the midgut of post-molt ticks. Moreover, otdB and otdD were also up-regulated in the salivary glands of flat post-molt ticks, while otdC was up-regulated within 1 week post blood-feeding.This work is foundational toward additional studies to determine mechanisms of vector competence and pathogen transmission from O. turicata.