Tissue tropism and vertical transmission ofCoxiellainRhipicephalus sanguineusandRhipicephalus turanicusticks

Abstract

Arthropod symbionts present tissue tropism that corresponds to the nature of the association and the mode of transmission between host generations. In ticks, however, our knowledge of symbiont tissue tropism and function is limited. Here, we quantified and localized previously described Coxiella-like symbionts in several organs of the tick Rhipicephalus turanicus. Quantitative polymerase chain reaction revealed high densities of Coxiella in the female gonads, and both male and female Malpighian tubules. Using fluorescence in situ hybridization and transmission electron microscopy, we further showed that in the gonads of both Rh. turanicus and Rh. sanguineus, Coxiella does not colonize the primary oocytes but is found later in young and mature oocytes in a specific distribution, suggesting controlled vertical transmission. This method revealed the presence Coxiella in the distal part of the Malpighian tubules, suggesting a possible role in nitrogen metabolism. While testing Rickettsia symbionts, no specific tissue tropism was found, but a slightly higher densities in the tick gut. The low density of Rickettsia in the female ovaries suggests competition between Rickettsia and Coxiella for vertical transmission. The described tissue distribution supports an obligatory role for Coxiella in ticks.

Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks

“…Nevertheless, FLE and other bacterial endosymbionts have been known to colonize salivary glands, and their presence in this organ does not ensure transmission to vertebrate hosts (41). Similar observations have been made for other hard ticks and their obligatory symbionts (36,40), suggesting a potential nutritional role of the symbionts in supplying B vitamins missing in the tick blood meal (11,42).…”

“…In addition, we demonstrated FLE in the tick ovaries, suggesting a specific mechanism to ensure transmission. High densities of FLE were found in the Malpighian tubules, organs which have been shown to harbor main endosymbionts in ticks (8,40). Interestingly, ubiquitous sporadic clusters of FLE were found in the salivary glands, which raises questions regarding the pathogenic potential of FLE (8).…”

“…Pools of organs were transferred into cell strainers (Corning, USA) and placed in 6-well plates filled with FAA (5% acetic acid, 5% formaldehyde, 90% ethanol) in a vacuum chamber for 1 h. After 24 h at room temperature, the organs were dehydrated in increasing ethanol concentrations of 50% for 10 min, and then 50%, 80%, and 100% for 15 min each step, and finally the organs were left to dry at room temperature for 10 min. Staining was performed on separate pools of salivary glands, ovaries, and Malpighian tubules, as described before (40), with a few modifications, in that cell strainers were used to transfer the organs from buffer to buffer. The probes /Cy3/FLE and /Cy5/Eub338 were diluted in the hybridization buffer (20 to a concentration of 6.25 ng/l.…”

Analysis of the Caenorhabditis elegans innate immune response to Coxiella burnetii

“…C. burnetii is an obligate intracellular parasite that has been shown to invade and replicate in a wide variety of host cells, including wax moth haemocytes, 28 tick tissues, 60 alveolar macrophages, 61,62 human cardiac valves 63 and goat placental trophoblasts. 64 Following an 8-d exposure, C. burnetii accumulation in C. elegans occasionally resulted in structures resembling extra-luminal blebs (Elbs; Figure 3d), which were not evident in nematodes that fed on live CEC (Figure 3a, b; Figure 4) or dead CCB (not shown), suggesting that C. burnetii activity or an autoclave-labile metabolite(s) played a role in their formation.…”

Symbiont dynamics of the Tibetan tick Haemaphysalis tibetensis (Acari: Ixodidae)

“…Some microbes have been shown to provide the necessary nutrition needed for tick development whereas others have been shown to interfere with survival and transmission of tick-borne pathogens [15]. Among the tick-associated symbionts, Coxiella -like symbionts have been detected in several genera of ticks [16, 17], and were found mainly infecting ovaries and vertically transmitted by transovarial transmission [18, 19]. Eliminating of Coxiella -like symbionts with antibiotics could cause severe reduction in fecundity and fitness of Amblyomma americanum [20], and recent genome studies on Coxiella -like symbionts in A. americanum and Rhipicephalus turanicus suggested their specific functions in providing required nutrients lacking in a blood meal [21, 22].…”