Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen, Borrelia afzelii

Jacquet, Maxime; Durand, Jonas; Rais, Olivier; Voordouw, Maarten J.

doi:10.1016/j.meegid.2015.09.012

Cited by 32 publications

(96 citation statements)

References 84 publications

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“…Previous work on B. afzelii has shown that host-to-tick transmission success increases with the spirochete density in the skin of the rodent reservoir host (69,75). Strains of B. afzelii that establish higher spirochete loads in the rodent tissues (ospC strain A10) have higher host-to-tick transmission than strains with lower spirochete loads (ospC strain A3) (69). Conversely, strain-specific differences in spirochete load inside the nymphal tick might influence the probability of tick-to-host transmission.…”

Section: Discussionmentioning

confidence: 99%

“…To date, no studies have tested whether the relative abundances of the strains in the tissues of the rodent host are transmitted to and maintained in the tick vector. Two independent studies on B. afzelii found that there was no relationship between rodent spirochete load and nymphal spirochete load (69,75). This result suggests that processes operating in the nymphal tick may also influence the strain-specific spirochete abundance in the tick vector.…”

Section: Discussionmentioning

confidence: 99%

“…We have recently shown that antibodies developed against one OspC antigen can sometimes protect mice against infection with strains carrying a different oMG allele (69). Such apparent competition in the vertebrate host might produce negative associations between ospC strains in the tick vector.…”

Section: Discussionmentioning

confidence: 99%

“…Conversely, strain-specific differences in spirochete load inside the nymphal tick might influence the probability of tick-to-host transmission. Infection experiments with different ospC strains of B. afzelii have shown that some strains (e.g., A10) establish much higher spirochete loads inside the nymphal ticks than other strains (e.g., A3) (69,73). A recent experimental infection study using genetically tagged strains of B. burgdorferi sensu stricto (that were otherwise identical in fitness) showed that strains that were more abundant in the nymphal tick had a higher probability of transmission to the rodent host (21).…”

Section: Discussionmentioning

confidence: 99%

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Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Durand

Herrmann

Genné

et al. 2017

Appl Environ Microbiol

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Mixed or multiple-strain infections are common in vector-borne diseases and have important implications for the epidemiology of these pathogens. Previous studies have mainly focused on interactions between pathogen strains in the vertebrate host, but little is known about what happens in the arthropod vector. Borrelia afzelii and Borrelia garinii are two species of spirochete bacteria that cause Lyme borreliosis in Europe and that share a tick vector, Ixodes ricinus. Each of these two tick-borne pathogens consists of multiple strains that are often differentiated using the highly polymorphic ospC gene. For each Borrelia species, we studied the frequencies and abundances of the ospC strains in a wild population of I. ricinus ticks that had been sampled from the same field site over a period of 3 years. We used quantitative PCR (qPCR) and 454 sequencing to estimate the spirochete load and the strain diversity within each tick. For B. afzelii, there was a negative relationship between the two most common ospC strains, suggesting the presence of competitive interactions in the vertebrate host and possibly the tick vector. The flat relationship between total spirochete abundance and strain richness in the nymphal tick indicates that the mean abundance per strain decreases as the number of strains in the tick increases. Strains with the highest spirochete load in the nymphal tick were the most common strains in the tick population. The spirochete abundance in the nymphal tick appears to be an important life history trait that explains why some strains are more common than others in nature.IMPORTANCE Lyme borreliosis is the most common vector-borne disease in the Northern Hemisphere and is caused by spirochete bacteria that belong to the Borrelia burgdorferi sensu lato species complex. These tick-borne pathogens are transmitted among vertebrate hosts by hard ticks of the genus Ixodes. Each Borrelia species can be further subdivided into genetically distinct strains. Multiple-strain infections are common in both the vertebrate host and the tick vector and can result in competitive interactions. To date, few studies on multiple-strain vector-borne pathogens have investigated patterns of cooccurrence and abundance in the arthropod vector. We demonstrate that the abundance of a given strain in the tick vector is negatively affected by the presence of coinfecting strains. In addition, our study suggests that the spirochete abundance in the tick is an important life history trait that can explain why some strains are more common in nature than others.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 2 more Smart Citations

Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Durand

Herrmann

Genné

et al. 2017

Appl Environ Microbiol

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“…The OspC protein is critical for establishing infection inside the vertebrate host (37,38). This antigen induces a protective antibody response in the vertebrate host (39)(40)(41) that is highly specific for strains carrying that particular ospC allele (42)(43)(44). The ospC gene has a large amount of sequence variation that allows ospC alleles to be classified into discrete major ospC groups (45).…”

mentioning

confidence: 99%

Cross-Immunity and Community Structure of a Multiple-Strain Pathogen in the Tick Vector

Durand

Jacquet

Paillard

et al. 2015

Appl Environ Microbiol

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bMany vector-borne pathogens consist of multiple strains that circulate in both the vertebrate host and the arthropod vector. Characterization of the community of pathogen strains in the arthropod vector is therefore important for understanding the epidemiology of mixed vector-borne infections. Borrelia afzelii and B. garinii are two species of tick-borne bacteria that cause Lyme disease in humans. These two sympatric pathogens use the same tick, Ixodes ricinus, but are adapted to different classes of vertebrate hosts. Both Borrelia species consist of multiple strains that are classified using the highly polymorphic ospC gene. Vertebrate cross-immunity against the OspC antigen is predicted to structure the community of multiple-strain Borrelia pathogens. Borrelia isolates were cultured from field-collected I. ricinus ticks over a period spanning 11 years. The Borrelia species of each isolate was identified using a reverse line blot (RLB) assay. Deep sequencing was used to characterize the ospC communities of 190 B. afzelii isolates and 193 B. garinii isolates. Infections with multiple ospC strains were common in ticks, but vertebrate cross-immunity did not influence the strain structure in the tick vector. The pattern of genetic variation at the ospC locus suggested that vertebrate cross-immunity exerts strong selection against intermediately divergent ospC alleles. Deep sequencing found that more than 50% of our isolates contained exotic ospC alleles derived from other Borrelia species. Two alternative explanations for these exotic ospC alleles are cryptic coinfections that were not detected by the RLB assay or horizontal transfer of the ospC gene between Borrelia species. Many vector-borne pathogens consist of multiple genetically distinct strains (1-4). The adaptive arm of the vertebrate immune system plays a key role in generating and maintaining this diversity of pathogen strains (5-7). Genetic diversity is often the highest at loci coding for surface-exposed pathogen molecules that function during the invasion and infection of host tissues (8, 9). The study of these highly polymorphic pathogen molecules is important for understanding how cross-reactive acquired immunity can mediate indirect competition and superinfection in the vertebrate host (10, 11). In addition, these pathogen outer surface proteins are often used to characterize pathogen strains because they provide an upper estimate of pathogen strain richness.In vector-borne diseases, the community of pathogen strains can be studied in both the vertebrate host and the arthropod vector. The vertebrate immune system creates nonrandom associations between pathogen strains (1, 12) that are subsequently transmitted to the arthropod vector. Conversely, the study of mixed infections in the arthropod vector can provide information on the processes that structure the community of multiple pathogen strains in the vertebrate host (13,14). In addition, estimates of strain richness in the arthropod vector are important for understanding the frequency with which ...

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