Evidence for Host-Genotype Associations of Borrelia burgdorferi Sensu Stricto

Mechai, Samir; Margos, Gabriele; Feil, Edward J.; Barairo, Nicole; Lindsay, L. Robbin; Michel, Pascal; Ogden, Nicholas H.

doi:10.1371/journal.pone.0149345

Cited by 53 publications

(66 citation statements)

References 81 publications

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“…Monitoring changes in the prevalences of different B. burgdorferi sensu lato genospecies in ticks might produce an important indicator of host adaptation, which, in turn, has been suggested to contribute to differences in pathogenicity in humans (45). Nevertheless, although we have reported statistically significant changes in the overall prevalence of B. burgdorferi sensu lato and relatively high geographical variability, these differences have only a limited effect on the total infection risk compared with differences in total tick abundance.…”

Section: Discussionmentioning

confidence: 52%

Europe-Wide Meta-Analysis of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks

Strnad

Hönig

Růžek

et al. 2017

Appl Environ Microbiol

165

131

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Lyme borreliosis is the most common zoonotic disease transmitted by ticks in Europe and North America. Despite having multiple tick vectors, the causative agent, Borrelia burgdorferi sensu lato, is vectored mainly by Ixodes ricinus in Europe. In the present study, we aimed to review and summarize the existing data published from 2010 to 2016 concerning the prevalence of B. burgdorferi sensu lato spirochetes in questing I. ricinus ticks. The primary focus was to evaluate the infection rate of these bacteria in ticks, accounting for tick stage, adult tick gender, region, and detection method, as well as to investigate any changes in prevalence over time. The data obtained were compared to the findings of a previous metastudy. The literature search identified data from 23 countries, with 115,028 ticks, in total, inspected for infection with B. burgdorferi sensu lato. We showed that the infection rate was significantly higher in adults than in nymphs and in females than in males. We found significant differences between European regions, with the highest infection rates in Central Europe. The most common genospecies were B. afzelii and B. garinii, despite a negative correlation of their prevalence rates. No statistically significant differences were found among the prevalence rates determined by conventional PCR, nested PCR, and real-time PCR.IMPORTANCE Borrelia burgdorferi sensu lato is a pathogenic bacterium whose clinical manifestations are associated with Lyme borreliosis. This vector-borne disease is a major public health concern in Europe and North America and may lead to severe arthritic, cardiovascular, and neurological complications if left untreated. Although pathogen prevalence is considered an important predictor of infection risk, solitary isolated data have only limited value. Here we provide summarized information about the prevalence of B. burgdorferi sensu lato spirochetes among host-seeking Ixodes ricinus ticks, the principal tick vector of borreliae in Europe. We compare the new results with previously published data in order to evaluate any changing trends in tick infection.KEYWORDS Borrelia burgdorferi sensu lato, tick, Ixodes ricinus, genospecies, metaanalysis, Lyme borreliosis, Lyme disease T he Borrelia burgdorferi sensu lato group includes the causative agents of Lyme borreliosis (LB), the most prevalent human tick-borne disease in the Northern Hemisphere (1). The bacterium is maintained in a horizontal transmission cycle between its vector, ticks of the genus Ixodes, and vertebrate reservoir host species. In Europe, there are a number of different B. burgdorferi sensu lato genospecies, many of them directly associated with human LB. The disease is caused predominantly by Borrelia burgdorferi sensu stricto, B. afzelii, B. garinii, and B. bavariensis (previously known as B. garinii OspA serotype 4) (2). In addition, four other genospecies are occasionally

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Section: Discussionmentioning

confidence: 52%

Europe-Wide Meta-Analysis of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks

Strnad

Hönig

Růžek

et al. 2017

Appl Environ Microbiol

165

131

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“…Two alternative explanations include the multiple niche polymorphism (MNP) hypothesis and apparent competition mediated by the host immune system. The MNP hypothesis suggests that the different ospC strains cycle in different vertebrate host species (23,64), and there is conflicting evidence for this hypothesis for B. burgdorferi sensu stricto in North America (23,(65)(66)(67). In Europe, studies on host specialization of ospC strains have been restricted to B. afzelii and its rodent hosts (30,40,68).…”

Section: Discussionmentioning

confidence: 99%

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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“…Also, within the species Anaplasma phagocytophilum, the pathogen responsible for tick-borne fever, sequence clusters are associated with different mammalian hosts (70). Within Borrelia burgdorferisensu stricto, the North American Lyme disease spirochete, some sequence clusters are associated with different rodent species (101,162), although it is not yet clear whether the adaptations to specific hosts are genome-wide adaptations or are due primarily to a single outer-surface protein (163). In some cases, host specificity is determined by plasmids, and the bacteria can adapt from one host species to another with acquisition of plasmids, as seen in legume-infecting Rhizobium ecotypes (133) or mammal-versus insect-infecting ecotypes in B. cereus sensu lato (143).…”

Section: Resource Differences Among Pathogensmentioning

confidence: 99%

Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

Cohan

2017

Microbiol Spectr

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Any two lineages, no matter how distant they are now, began their divergence as one population splitting into two lineages that could coexist indefinitely. The rate of origin of higher-level taxa is therefore the product of the rate of speciation times the probability that two new species coexist long enough to reach a particular level of divergence. Here I have explored these two parameters of disparification in bacteria. Owing to low recombination rates, sexual isolation is not a necessary milestone of bacterial speciation. Rather, irreversible and indefinite divergence begins with ecological diversification, that is, transmission of a bacterial lineage to a new ecological niche, possibly to a new microhabitat but at least to new resources. Several algorithms use sequence data from a taxon of focus to identify phylogenetic groups likely to bear the dynamic properties of species. Identifying these newly divergent lineages allows us to characterize the genetic bases of speciation, as well as the ecological dimensions upon which new species diverge. Speciation appears to be least frequent when a given lineage has few new resources it can adopt, as exemplified by photoautotrophs, C1 heterotrophs, and obligately intracellular pathogens; speciation is likely most rapid for generalist heterotrophs. The genetic basis of ecological divergence may determine whether ecological divergence is irreversible and whether lineages will diverge indefinitely into the future. Long-term coexistence is most likely when newly divergent lineages utilize at least some resources not shared with the other and when the resources themselves will coexist into the remote future.

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Evidence for Host-Genotype Associations of Borrelia burgdorferi Sensu Stricto

Cited by 53 publications

References 81 publications

Europe-Wide Meta-Analysis of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks

Europe-Wide Meta-Analysis of Borrelia burgdorferi Sensu Lato Prevalence in Questing Ixodes ricinus Ticks

Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

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