Characterization of the life cycle of Dermacentor nuttalli in the Qinghai-Tibetan Plateau under laboratory conditions and identification of spotted fever group Rickettsia

Abstract

Abstract Background Dermacentor nuttalli has been a focus of study because tick-borne pathogens have been widely identified in D. nuttalli in the northern and southwestern China. The salivary glands and midgut of ticks are specific and major barriers to efficient pathogen transmission. The spotted fever group Rickettsia causes tick-borne rickettsiosis, which poses serious threats to the health of humans and animals. Identification of the species of Rickettsia in the midgut and salivary glands of D. nuttalli is essential for understanding the colonization of the pathogens in ticks and for developing effective control strategies for Rickettsia. Methods This study collected D. nuttalli in the field on the Qinghai-Tibetan Plateau from March to April 2021 to characterize the D. nuttalli life-cycle under laboratory conditions, and identified SFG Rickettsia in the D. nuttalli midgut and salivary glands of males and females in both original and next-generational adults. Results D. nuttalli ticks collected in this area were molecularly confirmed, and exhibited one life cycle of an average of 67.4 days under laboratory conditions. The average weight of engorged females was 656.0 mg, which was 74.5 times the weight of unfed females. Moreover, high colonization rates of Rickettsia spp. were found in both the midgut and salivary glands of both male (92.0%) and female (93.0%) D. nuttalli ticks, anf no positivity being found in single tissue colonization. However, low rates of 4.0–6.0% of Rickettsia spp. colonization in the D. nuttalli midgut and salivary glands were detected. Furthermore, the sequencing analysis showed that the Rickettsia sequences obtained in this study shared 98.6 to 100% nucleotide identity to R. slovaca and R. raoultii isolated from Dermacentor spp. in China. The phylogenetic analysis of Rickettsia spp. based on the gltA, ompA, ompB and sca4 genes revealed that the Rickettsia sequences obtained could be classified into these two groups, R. slovaca and R. raoultii. Conclusions This study is the first to identify the life-cycle of collected D. nuttalli in the field in the Qinghai-Tibetan Plateau under laboratory conditions, and to detect the two species of SFG Rickettsia in the midgut and salivary glands of males and females in both original and next-generational D. nuttalli adults. Our study provides new insights into the pathogen colonization in ticks in the Qinghai-Tibet Plateau, and the relationship among hosts, ticks and pathogens.