Tick Ecdysteroid Hormone, Global Microbiota/Rickettsia Signaling in the Ovary versus Carcass during Vitellogenesis in Part-Fed (Virgin) American Dog Ticks, Dermacentor variabilis

Abstract

The transovarial transmission of tick-borne bacterial pathogens is an important mechanism for their maintenance in natural populations and transmission, causing disease in humans and animals. The mechanism for this transmission and the possible role of tick hormones facilitating this process have never been studied. Injections of physiological levels of the tick hormone, 20-hydroxyecdysone (20E), into part-fed (virgin) adult females of the American dog tick, Dermacentor variabilis, attached to the host caused a reduction in density of Rickettsia montanensis in the carcass and an increase in the ovaries compared to buffer-injected controls. This injection initiates yolk protein synthesis and uptake by the eggs but has no effect on blood feeding. Francisella sp. and R. montanensis were the predominant bacteria based on the proportionality in the carcass and ovary. The total bacteria load increased in the carcass and ovaries, and bacteria in the genus Pseudomonas increased in the carcass after the 20E injection. The mechanism of how the Rickettsia species respond to changes in tick hormonal regulation needs further investigation. Multiple possible mechanisms for the proliferation of R. montanensis in the ovaries are proposed.

Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

“…In this comparison, the sand fly shares 24 genera with the tick, but only 11 genera with both the mosquito and the tick, namely, Acinetobacter, Bacillus, Delftia, Enterobacter, Luteibacter, Methylobacterium, Pseudomonas, Rickettsia, Sphingomonas, Stenotrophomonas and Wolbachia. The highest amount of symbiont sharing was between the mosquito and the sandfly (33). However, there also was considerable sharing between the tick and the mosquito (18) and the sandfly (24), as well as 11 symbionts shared between all three vectors-a remarkable finding given the long evolutionary separation between ticks and insects.…”

“…In some arthropod vectors, endosymbionts invade specific body organs only during female reproductive activity. In the American dog tick, D. variabilis, Rickettsia montanensis invade the developing oocytes in response to rapidly increasing levels of the so-called molting hormone, 20-hydroxyecdysone (20-E) [33]. The adaptations used by these bacteria to invade the ovary and the significance of these processes for pathogen transmission to the tick's progeny are discussed below (Section 6 Does the vector microbiome affect the survival and/or development of pathogenic microbes?).…”

“…In ticks, transovarial transmission of tick-borne pathogens and non-pathogenic endosymbionts is a common phenomenon [87,91], although the factors that regulate this process are largely unknown. A surprising finding was the discovery of elevated densities of R. montanensis in the ovaries of female D. variabilis following treatment with 20-hydroxyecdsysone (20-E) [33], increasing 6.8-fold in density in the ovaries while decreasing 3.5-fold in the carcasses. Injection of 20-E into tick females during blood feeding was shown to trigger vitellogenesis and vitellogenin uptake by receptors on the developing oocytes [92].…”

A Novel Rhipicephalus microplus Estrogen Related Receptor (RmERR), a Molecular and In Silico Characterization of a Potential Protein Binding Estrogen

“…Currently, tick endocrinology research assumes that ticks regulate their larval, nymphal, and adult development by the same hormones and mechanisms that insects use; however, this does not necessarily occur [ 7 ]. Interestingly, the juvenile hormone (JH), which participates in insect molting and development, has not been identified in ticks [ 9 ].…”

“…For example, during the life cycle and after engorgement, ecdysteroid hormones trigger the salivary glands degeneration in Rhipicephalus haemaphysaloides [ 12 ]. There even exist reports proposing that the tick microbiome is responsive to the hormone 20-hydroxyecdysone, which regulates vitellogenesis and the egg development in Dermacentor variabilis [ 9 ]. Finally, the recent advances in tick genomics, transcriptomics, and proteomics have allowed researches to explore other possibilities to understand the endocrine and molecular host-vector-pathogen relationships [ 15 , 16 , 17 , 18 , 19 ].…”