Maternal Antibodies Provide Bank Voles with Strain-Specific Protection against Infection by the Lyme Disease Pathogen

Abstract

Multistrain microbial pathogens often induce strain-specific antibody responses in their vertebrate hosts. Mothers can transmit antibodies to their offspring, which can provide short-term, strain-specific protection against infection. Few experimental studies have investigated this phenomenon for multiple strains of zoonotic pathogens occurring in wildlife reservoir hosts. 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 female bank voles infected with B. afzelii via tick bite transmit protective antibodies to their offspring. To test the specificity of protection, the offspring were challenged using a natural tick bite challenge with either the maternal strain to which the mothers had been exposed or a different strain. The maternal antibodies protected the offspring against a homologous infectious challenge but not against a heterologous infectious challenge. The offspring from the uninfected control mothers were equally susceptible to both strains. Borrelia outer surface protein C (OspC) is an antigen that is known to induce strain-specific immunity. Maternal antibodies in the offspring reacted more strongly with homologous than with heterologous recombinant OspC, but other antigens may also mediate strain-specific immunity. Our study shows that maternal antibodies provide strain-specific protection against B. afzelii in an ecologically important rodent reservoir host. The transmission of maternal antibodies may have important consequences for the epidemiology of multistrain pathogens in nature. IMPORTANCE Many microbial pathogen populations consist of multiple strains that induce strain-specific antibody responses in their vertebrate hosts. Females can transmit these antibodies to their offspring, thereby providing them with short-term strain-specific protection against microbial pathogens. We investigated this phenomenon using multiple strains of the tick-borne microbial pathogen Borrelia afzelii and its natural rodent reservoir host, the bank vole, as a model system. We found that female bank voles infected with B. afzelii transmitted to their offspring maternal antibodies that provided highly efficient but strain-specific protection against a natural tick bite challenge. The transgenerational transfer of antibodies could be a mechanism that maintains the high strain diversity of this tick-borne pathogen in nature.

Tick-Borne Encephalitis Virus: Seasonal and Annual Variation of Epidemiological Parameters Related to Nymph-to-Larva Transmission and Exposure of Small Mammals

“…Therefore, TBEV seroprevalence in small mammals is a good proxy for the occurrence of new infections in a month, although it is impossible to distinguish antibodies due to maternal transfer from those developed after a recent infection. In small mammals, maternal antibodies generally last from six to 10 weeks [ 46 , 47 , 48 ], but this duration is unknown for TBEV. We captured two juveniles aged 3–4 weeks according to their weight that were seropositive.…”

Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal

“…Further support for this is provided by the positive association between neonatal antibody levels and the mother's own anti-strongyle antibody levels in the summer prior to giving birth. Previous experimental studies in captive rodents have demonstrated that maternal antibodies provide strain-specific protection which depends on the infection history of the mother [ 46 , 47 ]. Given that exposure to worms starts early, we would expect that all females would be sufficiently exposed to have developed an acquired immune response to strongyles by sexual maturity, despite exposure varying in time and space [ 19 ].…”

Competition between strains of Borrelia afzelii in the host tissues and consequences for transmission to ticks

“…For the subset of infected tissues, we found that the spirochete load was highest in the ears and the dorsal skin, and lower in internal organs like the heart, bladder, and ankle joints. Other studies on B. afzelii and B. burgdorferi sensu stricto (ss) in rodent hosts, have also found that the spirochete load is higher in the skin compared to internal organs like the bladder and heart [33,[36][37][38][39]. One explanation for this result is that the skin is important for the host-to-tick transmission of B. burgdorferi sl [21][22][23], whereas the internal organs (e.g., bladder, heart, and joints) are a deadend for spirochete transmission to ticks (39).…”

“…The I. ricinus ticks came from the laboratory colony that has been maintained at the University of Neuchâtel since 1978. We used B. afzelii strains NE4049 and Fin-Jyv-A3 in this study because we have a history of successful experimental infections with these two strains [33,34,36,37]. Strain NE4049 was isolated from an I. ricinus tick in Switzerland, has multi-locus sequence type (MLST) 679, strain ID number 1887 in the Borrelia MLST database, and ospC major group (oMG) A10.…”