Endosymbionts Alter Larva-to-Nymph Transstadial Transmission of Babesia microti in Rhipicephalus haemaphysaloides Ticks

Abstract

Maternally inherited endosymbionts inhabit a variety of arthropods. Some of them can protect the arthropod host against a wide range of pathogens. However, very little is known about the association between endosymbionts and pathogen susceptibility in ticks. The present study investigated the effect of endosymbionts on larva-to-nymph transstadial transmission of Babesia microti by Rhipicephalus haemaphysaloides ticks. Engorged female ticks were injected with PBS, ciprofloxacin or kanamycin. The offspring larvae were used to infest B. microti-positive mice. Prevalence of B. microti among the nymphs in different treatment groups and its association with endosymbiont density in the larvae were analyzed. The results showed that the prevalence of B. microti in the kanamycin-treated group (63.9%, 95% confidence interval (CI): 52.8–75.0%) was higher than that in the PBS (23.6%, 95% CI: 13.8–33.4%) or ciprofloxacin-treated (25.0%, 95% CI: 15.0–35.0%) groups. This increased prevalence was associated with reduced density of Coxiella-like endosymbiont but was not related to the density of Rickettsia-like endosymbiont. No direct evidence has previously been reported about the impact of Coxiella-like endosymbiont on pathogen susceptibility in ticks. This study reveals that endosymbionts are potentially important defensive symbionts of R. haemaphysaloides which may influence the colonization or susceptibility of B. microti in the tick host.

The Prevalence of Coxiella burnetii in Hard Ticks in Europe and Their Role in Q Fever Transmission Revisited—A Systematic Review

“…A reduced infection rate of R. haemaphysaloides with CLE correlated with a lower rate of transstadial transmission of Babesia microti. Candidatus Midichloria mitochondrii , another tick endosymbiont, is known to influence the occurrence and ability to detect tick-borne pathogens in I. ricinus ( 159 , 160 ).…”

The Tick Microbiota Dysbiosis Promote Tick-Borne Pathogen Transstadial Transmission in a Babesia microti–Infected Mouse Model

“…The genus Coxiella in ticks includes both symbiotic and pathogenic bacteria (Nardi et al, 2021), and non-pathogenic symbionts may be important in the transmission of TBPs (Bonnet et al, 2017). Li et al (2018) suggested that Coxiella was likely an important defensive endosymbiont, and TBPs prevalence was decreased, with this being dependent on reduced Coxiella endosymbiont in ticks. We showed that the Coxiella abundance was decreased and B. microti infection increased in AT adults compared to the CT adults, which is consistent with the results of Li et al However, TBPs transmission needs further study and may lead to a potential biological strategy for TBPs control.…”

“…The genus Coxiella in ticks includes both symbiotic and pathogenic bacteria ( Nardi et al., 2021 ), and non-pathogenic symbionts may be important in the transmission of TBPs ( Bonnet et al., 2017 ). Li et al. (2018) suggested that Coxiella was likely an important defensive endosymbiont, and TBPs prevalence was decreased, with this being dependent on reduced Coxiella endosymbiont in ticks.…”

Borreliainfection in rodent host has dramatic effects on the microbiome of ticks

“…A growing number of studies have investigated whether dysbiosing ticks influences their susceptibility to acquiring tick-borne pathogens [8, 11-13]. In some systems, microbiome disruption makes tick species more susceptible to infection with tick-borne pathogens [8, 13], whereas other systems found the opposite effect [11, 12]. In the present study, we found no evidence that microbiome disruption influenced B. afzelii infection rates or the B. afzelii spirochete load in infected ticks.…”

“…For successful transmission, however, vector-borne pathogens must contend with both the immunological defenses of the arthropod vector, and the community of other microbiota that inhabit it [4-7], and it is now clear that endogenous microbes can shape the competence of diverse arthropod vectors in acquiring and transmitting pathogens [8-12]. Experimental perturbations of the microbiome (‘dysbiosis’) via the use of antibiotics or other methods have, in various contexts, been shown to either increase or decrease the susceptibility of arthropods to colonization by vector-borne pathogens [8, 10, 12, 13]. In particular, the introduction of the intracellular bacterium Wolbachia into mosquito vectors [14] can dramatically reduce mosquito competence to vector arboviruses, malaria parasites, and filarial nematodes (Kambris et al 2009, Moreira et al 2009, Bian et al 2010).…”