Comparative proteomics of the vector Dermacentor reticulatus revealed differentially regulated proteins associated with pathogen transmission in response to laboratory infection with Rickettsia slovaca

Abstract

Background Tick-borne rickettsial diseases are caused by pathogens acquired from hard ticks. In particular, Rickettsia slovaca , a zoonotic infectious bacterium causing tick-borne lymphadenopathy (TIBOLA), is transmitted by the vectors Dermacentor spp. that can be found all over Europe. Although recent studies point out the extreme complexity of bacteria-induced effects in these blood-feeding vectors, the knowledge of individual molecules involved in the preservation and transmission of the pathogen is still limited. System biology tools, including proteomics, may contribute greatly to the understanding of pathogen-tick-host interactions. Methods Herein, we performed a comparative proteomics study of the tick vector Dermacentor reticulatus that was experimentally infected with the endosymbiotic bacterium R. slovaca . Rickettsia -free ticks, collected in the southern region of Slovakia, were infected with the bacterium by a capillary tube-feeding system, and the dynamics of infection was assessed by quantitative PCR method after 5, 10, 15 and 27 days. Results At the stage of controlled proliferation (at 27 dpi), 33 (from 481 profiled) differentially abundant protein spots were detected on a two-dimensional gel. From the aforementioned protein spots, 21 were successfully identified by tandem mass spectrometry. Conclusions Although a few discovered proteins were described as having structural or housekeeping functions, the vast majority of the affected proteins were suggested to be essential for tick attachment and feeding on the host, host immune system evasion and defensive response modulation to ensure successful pathogen transmission. Electronic supplementary material The online version of this article (10.1186/s13071-019-3564-y) contains supplementary material, which is available to authorized users.

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“…This response has been observed in response to the bacterium R. rickettsi in Amblyomma sculptum, which experiences and increase in catabolism, signal transduction, protein and extracellular matrix management, and immunity; this was implied to be responsible for its relative resistance as compared to A. aureolatum, a species that shows downregulation of the same pathways and is more easily infected with R. rickettsi. 100 Transcriptional changes have also been observed in D. reticulatus when infected with R. slovaca, 101 with the targets thought to be related to feeding behaviour and salivary factors; a similar response has also been observed with D. variabilis infected with R. montanensis, where tissue-specific responses being observed in a number of functions associated with metabolism, cellular transport, and salivary factors. 102 The response of R. annulatus to Babesia bigemnia, a eukaryotic parasite, has also been observed, with a stress response and increase in apoptosis observed with increased expression of the apoptosis-associated proteins GP80, death-associated protein kinase 1 (DAPK-1), bax inhibitor-1 related protein (BI-1), several heat-shock related proteins and tRNA-ribosyltransferase; GP80, DAPK-1 and BI-1 were found to be required to regulate the replicate B. bigemina replication.…”

“…This response has been observed in response to the bacterium R. rickettsi in Amblyomma sculptum , which experiences and increase in catabolism, signal transduction, protein and extracellular matrix management, and immunity; this was implied to be responsible for its relative resistance as compared to A. aureolatum , a species that shows downregulation of the same pathways and is more easily infected with R. rickettsi 100 . Transcriptional changes have also been observed in D. reticulatus when infected with R. slovaca , 101 with the targets thought to be related to feeding behaviour and salivary factors; a similar response has also been observed with D. variabilis infected with R . montanensis , where tissue‐specific responses being observed in a number of functions associated with metabolism, cellular transport, and salivary factors 102 .…”

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“…In Glossina morsitans , Attacins play a role in Trypanosoma resistance , and can maintain homeostasis in infected individuals ( Wang et al., 2008 ). Also, in the study of Flores-Ramirez et al. (2019) three glycine-rich proteins have been identified as a response to infection of D. reticulatus ticks that was experimentally infected with Rickettsia slovaca .…”