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.
1819 The vertebrate immune system can produce antibodies that protect the host against 20 pathogens. Females can transmit antibodies to their offspring, which provide short-term 21 protection against infection. The tick-borne bacterium Borrelia afzelii causes Lyme 22 disease in Europe and consists of multiple strains that cycle between the tick vector 23 (Ixodes ricinus) and vertebrate hosts such as the bank vole (Myodes glareolus). We used 24 a controlled experiment to show that infected female bank voles transmit protective 25 antibodies to their offspring that are specific for the strain of B. afzelii. To test the 26 specificity of protection, the offspring were challenged with either the same strain to 27 which the mothers had been exposed or a different strain. The maternal antibodies 28 protected the offspring against the same strain, but not against the different strain. The 29 offspring from the uninfected control mothers were equally susceptible to both strains.30 Our study shows that maternal antibodies provide strong but highly strain-specific 31 protection against B. afzelii in an important rodent reservoir host. The transmission of 32 maternal antibodies may have important consequences for the epidemiology of multiple-33 strain pathogens in nature. 3435 40 41 Many pathogens that cause infectious disease consist of multiple strains. In vertebrate 42 hosts, the immune system can generate antibodies that are highly specific for different 43 pathogen strains. Mothers can transmit these antibodies to their offspring and thereby 44 protect them from infectious disease. To date, few studies have investigated whether this 45 transgenerational transfer of protective antibodies is important for pathogens that cycle in 46 wild animal populations. The tick-borne spirochete bacterium Borrelia afzelii causes 47 Lyme disease in Europe and cycles between Ixodes ticks and wild rodent hosts, such as 48 the bank vole (Myodes glareolus). The purpose of our study was to test whether female 49 bank voles infected with B. afzelii transmit antibodies to their offspring that protect them 50 from an infected tick bite. Our study found that infected mothers do transmit antibodies, 51 but the offspring were only protected against the strain of B. afzelii to which their 52 mothers had been exposed and not to a different strain (i.e. protection was highly strain-53 specific). The broader implications of our study is that the transfer of protective 54 antibodies between generations in the vertebrate host population could be important for 55 organizing the community of pathogen strains that circulate in nature. 56 57 4 58 Introduction 59Parents transmit to their offspring more than just their genes [1]. Mothers transfer 60 their environmental experience and phenotype to their offspring [2] and these maternal 61 effects can influence offspring phenotype and fitness [3]. In vertebrate hosts, an 62 important maternal effect is the transmission of antibodies from mothers to offspring [4]. 63 Young vertebrates are susceptible to infecti...
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