Gomez-Chamorro, A. | Search bioRxiv

bioRxiv2020

Borrelia afzelii does not suppress the development of anti-tick immunity in bank voles

Vector-borne pathogens manipulate their vertebrate hosts to enhance their transmission to arthropod vectors. The ability of vertebrate hosts to develop acquired immunity against arthropod vectors represents an existential threat for both the vector and the pathogen. The purpose of the study was to test whether the tick-borne spirochete bacterium Borrelia afzelii could suppress the development of acquired immunity to its tick vector Ixodes ricinus in the bank vole Myodes glareolus, which is an important host for both the tick and the pathogen. We created a group of B. afzelii-infected bank voles and an uninfected control group by exposing lab-reared animals to infected or uninfected ticks. At 1, 2, and 3 months post-infection, all bank voles were infested with larval I. ricinus ticks. The bank voles developed a strong antibody response against tick salivary gland extract proteins. This anti-tick immunity had negative effects on tick fitness traits including engorged larval weight, unfed nymphal weight, larva-to-nymph molting time and larva-to-nymph molting success. Infection with B. afzelii did not suppress the development of acquired immunity against I. ricinus ticks. The development of anti-tick immunity was strongly correlated with a dramatic temporal decline in both the bacterial abundance in the host ear tissues and the host-tick transmission success of B. afzelii. Our study suggests that the development of anti-tick immunity in bank voles has important consequences for the density of infected ticks and the risk of Lyme borreliosis. ImportanceMany pathogens enhance their persistence and transmission by suppressing the immune system of their host. We used an experimental infection approach to test whether the Lyme disease pathogen, Borrelia afzelii, could suppress the development of acquired immunity against its tick vector (Ixodes ricinus) in the bank vole (Myodes glareolus), but found no evidence for this phenomenon. Uninfected and B. afzelii-infected bank voles both developed a strong IgG antibody response against tick salivary gland extract following repeated infestations with I. ricinus ticks. The development of anti-tick immunity was negatively correlated with the abundance of B. afzelii in ear tissue biopsies and with host-to-tick transmission to I. ricinus ticks. Our study suggests that anti-tick immunity in the bank vole reduces the prevalence of this important tick-borne pathogen.

microbiology↗

bioRxiv2019

Maternal antibodies provide strain-specific protection against infection with the Lyme disease pathogen in a wild rodent

The vertebrate immune system can produce antibodies that protect the host against pathogens. Females can transmit antibodies to their offspring, which provide short-term protection against infection. The tick-borne bacterium Borrelia afzelii causes Lyme disease in Europe and consists of multiple strains that cycle between the tick vector (Ixodes ricinus) and vertebrate hosts such as the bank vole (Myodes glareolus). We used a controlled experiment to show that infected female bank voles transmit protective antibodies to their offspring that are specific for the strain of B. afzelii. To test the specificity of protection, the offspring were challenged with either the same strain to which the mothers had been exposed or a different strain. The maternal antibodies protected the offspring against the same strain, but not against the different strain. The offspring from the uninfected control mothers were equally susceptible to both strains. Our study shows that maternal antibodies provide strong but highly strain-specific protection against B. afzelii in an important rodent reservoir host. The transmission of maternal antibodies may have important consequences for the epidemiology of multiple-strain pathogens in nature.\n\nAuthor SummaryMany pathogens that cause infectious disease consist of multiple strains. In vertebrate hosts, the immune system can generate antibodies that are highly specific for different pathogen strains. Mothers can transmit these antibodies to their offspring and thereby protect them from infectious disease. To date, few studies have investigated whether this transgenerational transfer of protective antibodies is important for pathogens that cycle in wild animal populations. The tick-borne spirochete bacterium Borrelia afzelii causes Lyme disease in Europe and cycles between Ixodes ticks and wild rodent hosts, such as the bank vole (Myodes glareolus). The purpose of our study was to test whether female bank voles infected with B. afzelii transmit antibodies to their offspring that protect them from an infected tick bite. Our study found that infected mothers do transmit antibodies, but the offspring were only protected against the strain of B. afzelii to which their mothers had been exposed and not to a different strain (i.e. protection was highly strain-specific). The broader implications of our study is that the transfer of protective antibodies between generations in the vertebrate host population could be important for organizing the community of pathogen strains that circulate in nature.

immunology↗