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Environmental Microbiology

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

Andrea Gomez-Chamorro, Vanina Heinrich, Anouk Sarr, Owen Roethlisberger, Dolores Genné, Cindy Bregnard, Maxime Jacquet, Maarten J. Voordouw
Harold L. Drake, Editor
Andrea Gomez-Chamorro
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland
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Vanina Heinrich
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland
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Anouk Sarr
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland
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Owen Roethlisberger
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland
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Dolores Genné
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland
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Cindy Bregnard
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, Switzerland
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Maxime Jacquet
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, SwitzerlandDepartment of Pathobiology, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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Maarten J. Voordouw
Laboratoire d’Ecologie et Evolution des Parasites, Institut de Biologie, Université de Neuchâtel, Neuchâtel, SwitzerlandDepartment of Veterinary Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada
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Harold L. Drake
University of Bayreuth
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DOI: 10.1128/AEM.01887-19
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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.

FOOTNOTES

    • Received 16 August 2019.
    • Accepted 13 September 2019.
    • Accepted manuscript posted online 20 September 2019.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.01887-19.

  • Copyright © 2019 American Society for Microbiology.

All Rights Reserved.

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Maternal Antibodies Provide Bank Voles with Strain-Specific Protection against Infection by the Lyme Disease Pathogen
Andrea Gomez-Chamorro, Vanina Heinrich, Anouk Sarr, Owen Roethlisberger, Dolores Genné, Cindy Bregnard, Maxime Jacquet, Maarten J. Voordouw
Applied and Environmental Microbiology Nov 2019, 85 (23) e01887-19; DOI: 10.1128/AEM.01887-19

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Maternal Antibodies Provide Bank Voles with Strain-Specific Protection against Infection by the Lyme Disease Pathogen
Andrea Gomez-Chamorro, Vanina Heinrich, Anouk Sarr, Owen Roethlisberger, Dolores Genné, Cindy Bregnard, Maxime Jacquet, Maarten J. Voordouw
Applied and Environmental Microbiology Nov 2019, 85 (23) e01887-19; DOI: 10.1128/AEM.01887-19
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KEYWORDS

Borrelia afzelii
Lyme disease
ecology of infectious disease
maternal antibodies
maternal effects
outer surface protein C
strain-specific immunity
tick-borne disease
Borrelia burgdorferi
vector-borne pathogen

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