scholarly journals Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

2016 ◽  
Vol 83 (3) ◽  
Author(s):  
Jonas Durand ◽  
Coralie Herrmann ◽  
Dolores Genné ◽  
Anouk Sarr ◽  
Lise Gern ◽  
...  
Keyword(s):  
Lyme Borreliosis ◽  
Vertebrate Host ◽  
Competitive Interactions ◽  
Life History Trait ◽  
Content Type ◽  
Tick Vector ◽  
Nymphal Tick ◽  
Vector Borne ◽  
Spirochete Load ◽  
Important Life History Trait

ABSTRACT 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.

scholarly journals Species Co-Occurrence Patterns among Lyme Borreliosis Pathogens in the Tick Vector Ixodes ricinus

2013 ◽  
Vol 79 (23) ◽  
pp. 7273-7280 ◽  
Author(s):  
Coralie Herrmann ◽  
Lise Gern ◽  
Maarten J. Voordouw
Keyword(s):  
Lyme Borreliosis ◽  
Ixodes Ricinus ◽  
Vertebrate Host ◽  
Mixed Infections ◽  
Data Set ◽  
Content Type ◽  
Tick Vector ◽  
Pairwise Interactions ◽  
Spirochete Load ◽  
Reservoir Hosts

ABSTRACTMixed infections have important consequences for the ecology and evolution of host-parasite interactions. In vector-borne diseases, interactions between pathogens occur in both the vertebrate host and the arthropod vector. Spirochete bacteria belonging to theBorrelia burgdorferisensu latogenospecies complex are transmitted byIxodesticks and cause Lyme borreliosis in humans. In Europe, there is a high diversity ofBorreliapathogens, and the main tick vector,Ixodes ricinus, is often infected with multipleBorreliagenospecies. In the present study, we characterized the pairwise interactions between fiveB. burgdorferisensu latogenospecies in a large data set ofI. ricinusticks collected from the same field site in Switzerland. We measured two types of pairwise interactions: (i) co-occurrence, whether double infections occurred more or less often than expected, and (ii) spirochete load additivity, whether the total spirochete load in double infections was greater or less than the sum of the single infections. Mixed infections ofBorreliagenospecies specialized on different vertebrate reservoir hosts occurred less frequently than expected (negative co-occurrence) and had joint spirochete loads that were lower than the additive expectation (inhibition). In contrast, mixed infections of genospecies that share the same reservoir hosts were more common than expected (positive co-occurrence) and had joint spirochete loads that were similar to or greater than the additive expectation (facilitation). Our study suggests that the vertebrate host plays an important role in structuring the community ofB. burgdorferisensu latogenospecies inside the tick vector.

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

2015 ◽  
Vol 81 (22) ◽  
pp. 7740-7752 ◽  
Author(s):  
Jonas Durand ◽  
Maxime Jacquet ◽  
Lye Paillard ◽  
Olivier Rais ◽  
Lise Gern ◽  
...  
Keyword(s):  
Deep Sequencing ◽  
Content Type ◽  
Arthropod Vector ◽  
Tick Vector ◽  
Vector Borne ◽  
Vertebrate Hosts ◽  
Cross Immunity ◽  
Multiple Strains ◽  
Pathogen Strains

ABSTRACTMany 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 afzeliiandB. gariniiare 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. BothBorreliaspecies consist of multiple strains that are classified using the highly polymorphicospCgene. Vertebrate cross-immunity against the OspC antigen is predicted to structure the community of multiple-strainBorreliapathogens.Borreliaisolates were cultured from field-collectedI. ricinusticks over a period spanning 11 years. TheBorreliaspecies of each isolate was identified using a reverse line blot (RLB) assay. Deep sequencing was used to characterize theospCcommunities of 190B. afzeliiisolates and 193B. gariniiisolates. Infections with multipleospCstrains were common in ticks, but vertebrate cross-immunity did not influence the strain structure in the tick vector. The pattern of genetic variation at theospClocus suggested that vertebrate cross-immunity exerts strong selection against intermediately divergentospCalleles. Deep sequencing found that more than 50% of our isolates contained exoticospCalleles derived from otherBorreliaspecies. Two alternative explanations for these exoticospCalleles are cryptic coinfections that were not detected by the RLB assay or horizontal transfer of theospCgene betweenBorreliaspecies.

scholarly journals Superinfection Exclusion of the Ruminant Pathogen Anaplasma marginale in Its Tick Vector Is Dependent on the Time between Exposures to the Strains

2016 ◽  
Vol 82 (11) ◽  
pp. 3217-3224 ◽  
Author(s):  
Susan M. Noh ◽  
Michael J. Dark ◽  
Kathryn E. Reif ◽  
Massaro W. Ueti ◽  
Lowell S. Kappmeyer ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Anaplasma Marginale ◽  
Host Population ◽  
Mammalian Host ◽  
Content Type ◽  
Tropical Regions ◽  
Superinfection Exclusion ◽  
Tick Vector ◽  
Exposure Interval ◽  
Vector Borne

ABSTRACTThe remarkable genetic diversity of vector-borne pathogens allows for the establishment of superinfection in the mammalian host. To have a long-term impact on population strain structure, the introduced strains must also be transmitted by a vector population that has been exposed to the existing primary strain. The sequential exposure of the vector to multiple strains frequently prevents establishment of the second strain, a phenomenon termed superinfection exclusion. As a consequence, superinfection exclusion may greatly limit genetic diversity in the host population, which is difficult to reconcile with the high degree of genetic diversity maintained among vector-borne pathogens. UsingAnaplasma marginale, a tick-borne bacterial pathogen of ruminants, we hypothesized that superinfection exclusion is temporally dependent and that longer intervals between strain exposures allow successful acquisition and transmission of a superinfecting strain. To test this hypothesis, we sequentially exposedDermacentor andersoniticks to two readily tick-transmissible strains ofA. marginale. The tick feedings were either immediately sequential or 28 days apart. Ticks were allowed to transmission feed and were individually assessed to determine if they were infected with one or both strains. The second strain was excluded from the tick when the exposure interval was brief but not when it was prolonged. Midguts and salivary glands of individual ticks were superinfected and transmission of both strains occurred only when the exposure interval was prolonged. These findings indicate that superinfection exclusion is temporally dependent, which helps to account for the differences in pathogen strain structure in tropical compared to temperate regions.IMPORTANCEMany vector-borne pathogens have marked genetic diversity, which influences pathogen traits such as transmissibility and virulence. The most successful strains are those that are preferentially transmitted by the vector. However, the factors that determine successful transmission of a particular strain are unknown. In the case of intracellular, bacterial, tick-borne pathogens, one potential factor is superinfection exclusion, in which colonization of ticks by the first strain of a pathogen it encounters prevents the transmission of a second strain. UsingA. marginale, the most prevalent tick-borne pathogen of cattle worldwide, and its natural tick vector, we determined that superinfection exclusion occurs when the time between exposures to two strains is brief but not when it is prolonged. These findings suggest that superinfection exclusion may influence strain transmission in temperate regions, where tick activity is limited by season, but not in tropical regions, where ticks are active for long periods.

scholarly journals Competition between strains of Borrelia afzelii inside the rodent host and the tick vector

2018 ◽  
Vol 285 (1890) ◽  
pp. 20181804 ◽  
Author(s):  
Dolores Genné ◽  
Anouk Sarr ◽  
Andrea Gomez-Chamorro ◽  
Jonas Durand ◽  
Claire Cayol ◽  
...  
Keyword(s):  
Competitive Ability ◽  
Vertebrate Host ◽  
Mixed Infections ◽  
Rodent Host ◽  
Borrelia Afzelii ◽  
Arthropod Vector ◽  
Tick Vector ◽  
Trade Offs ◽  
Tick Transmission ◽  
Vector Borne

Multiple-strain pathogens often establish mixed infections inside the host that result in competition between strains. In vector-borne pathogens, the competitive ability of strains must be measured in both the vertebrate host and the arthropod vector to understand the outcome of competition. Such studies could reveal the existence of trade-offs in competitive ability between different host types. We used the tick-borne bacterium Borrelia afzelii to test for competition between strains in the rodent host and the tick vector, and to test for a trade-off in competitive ability between these two host types. Mice were infected via tick bite with either one or two strains, and these mice were subsequently used to create ticks with single or mixed infections. Competition in the rodent host reduced strain-specific host-to-tick transmission and competition in the tick vector reduced the abundance of both strains. The strain that was competitively superior in host-to-tick transmission was competitively inferior with respect to bacterial abundance in the tick. This study suggests that in multiple-strain vector-borne pathogens there are trade-offs in competitive ability between the vertebrate host and the arthropod vector. Such trade-offs could play an important role in the coexistence of pathogen strains.

scholarly journals Drug Resistance in Filarial Parasites Does Not Affect Mosquito Vectorial Capacity

Pathogens ◽  
2020 ◽  
Vol 10 (1) ◽  
pp. 2
Author(s):  
Erik Neff ◽  
Christopher C. Evans ◽  
Pablo D. Jimenez Castro ◽  
Ray M. Kaplan ◽  
Guha Dharmarajan
Keyword(s):  
Drug Resistance ◽  
Transmission Efficiency ◽  
Vectorial Capacity ◽  
Vertebrate Host ◽  
Mosquito Vector ◽  
Drug Resistant ◽  
Vector Borne Diseases ◽  
Asian Tiger ◽  
Significant Difference ◽  
Vector Borne

Parasite drug resistance presents a major obstacle to controlling and eliminating vector-borne diseases affecting humans and animals. While vector-borne disease dynamics are affected by factors related to parasite, vertebrate host and vector, research on drug resistance in filarial parasites has primarily focused on the parasite and vertebrate host, rather than the mosquito. However, we expect that the physiological costs associated with drug resistance would reduce the fitness of drug-resistant vs. drug-susceptible parasites in the mosquito wherein parasites are not exposed to drugs. Here we test this hypothesis using four isolates of the dog heartworm (Dirofilaria immitis)—two drug susceptible and two drug resistant—and two vectors—the yellow fever mosquito (Aedes aegypti) and the Asian tiger mosquito (Ae. albopictus)—as our model system. Our data indicated that while vector species had a significant effect on vectorial capacity, there was no significant difference in the vectorial capacity of mosquitoes infected with drug-resistant vs. drug-susceptible parasites. Consequently, contrary to expectations, our data indicate that drug resistance in D. immitis does not appear to reduce the transmission efficiency of these parasites, and thus the spread of drug-resistant parasites in the vertebrate population is unlikely to be mitigated by reduced fitness in the mosquito vector.

scholarly journals Contributions of Environmental Signals and Conserved Residues to the Functions of Carbon Storage Regulator A of Borrelia burgdorferi

2013 ◽  
Vol 81 (8) ◽  
pp. 2972-2985 ◽  
Author(s):  
S. L. Rajasekhar Karna ◽  
Rajesh G. Prabhu ◽  
Ying-Han Lin ◽  
Christine L. Miller ◽  
J. Seshu
Keyword(s):  
Borrelia Burgdorferi ◽  
Carbon Storage ◽  
Vertebrate Host ◽  
Acetyl Phosphate ◽  
Mobility Shift ◽  
Acetyl Coa ◽  
Site Specific ◽  
Content Type ◽  
Environmental Signals ◽  
Carbon Storage Regulator

ABSTRACTCarbon storage regulator A ofBorrelia burgdorferi(CsrABb) contributes to vertebrate host-specific adaptation by modulating activation of the Rrp2-RpoN-RpoS pathway and is critical for infectivity. We hypothesized that the functions of CsrABbare dependent on environmental signals and on select residues. We analyzed the phenotype ofcsrABbdeletion and site-specific mutants to determine the conserved and pathogen-specific attributes of CsrABb. Levels of phosphate acetyltransferase (Pta) involved in conversion of acetyl phosphate to acetyl-coenzyme A (acetyl-CoA) and posttranscriptionally regulated by CsrABbin thecsrABbmutant were reduced from or similar to those in the control strains under unfed- or fed-tick conditions, respectively. Increased levels of supplemental acetate restored vertebrate host-responsive determinants in thecsrABbmutant to parental levels, indicating that both the levels of CsrABband the acetyl phosphate and acetyl-CoA balance contribute to the activation of the Rrp2-RpoN-RpoS pathway. Site-specific replacement of 8 key residues of CsrABb(8S) with alanines resulted in increased levels of CsrABband reduced levels of Pta and acetyl-CoA, while levels of RpoS, BosR, and other members ofrpoSregulon were elevated. Truncation of 7 amino acids at the C terminus of CsrABb(7D) resulted in reducedcsrABbtranscripts and posttranscriptionally reduced levels of FliW located upstream of CsrABb. Electrophoretic mobility shift assays revealed increased binding of 8S mutant protein to the CsrA binding box upstream ofptacompared to the parental and 7D truncated protein. Two CsrABbbinding sites were also identified upstream offliWwithin theflgKcoding sequence. These observations reveal conserved and unique functions of CsrABbthat regulate adaptive gene expression inB. burgdorferi.

scholarly journals Spatial genetic analysis and long-term mark–recapture data demonstrate male-biased dispersal in a snake

2006 ◽  
Vol 3 (1) ◽  
pp. 33-35 ◽  
Author(s):  
J. Scott Keogh ◽  
Jonathan K Webb ◽  
Richard Shine
Keyword(s):  
Demographic Data ◽  
Molecular Data ◽  
Life History Trait ◽  
Eastern Australia ◽  
Powerful Approach ◽  
Adult Dispersal ◽  
Spatial Genetic Analysis ◽  
Polygynous Mating System ◽  
Important Life History Trait

Dispersal is an important life-history trait, but it is notoriously difficult to study. The most powerful approach is to attack the problem with multiple independent sources of data. We integrated information from a 14-year demographic study with molecular data from five polymorphic microsatellite loci to test the prediction of male-biased dispersal in a common elapid species from eastern Australia, the small-eyed snake Rhinoplocephalus nigrescens . These snakes have a polygynous mating system in which males fight for access to females. Our demographic data demonstrate that males move farther than females (about twice as far on average, and about three times for maximum distances). This sex bias in adult dispersal was evident also in the genetic data, which showed a strong and significant genetic signature of male-biased dispersal. Together, the genetic and demographic data suggest that gene flow is largely mediated by males in this species.

scholarly journals Induction of Interleukin 10 byBorrelia burgdorferiIs Regulated by the Action of CD14-Dependent p38 Mitogen-Activated Protein Kinase and cAMP-Mediated Chromatin Remodeling

2018 ◽  
Vol 86 (4) ◽  
Author(s):  
Bikash Sahay ◽  
Kathleen Bashant ◽  
Nicole L. J. Nelson ◽  
Rebeca L. Patsey ◽  
Shiva Kumar Gadila ◽  
...  
Keyword(s):  
Protein Kinase ◽  
Lyme Borreliosis ◽  
Human Peripheral Blood ◽  
Interleukin 10 ◽  
Mapk Signaling ◽  
Lyme Arthritis ◽  
Mitogen Activated Protein Kinase ◽  
Content Type ◽  
C3h Mice ◽  
Mitogen Activated Protein

ABSTRACTHost genotype influences the severity of murine Lyme borreliosis, caused by the spirochetal bacteriumBorrelia burgdorferi. C57BL/6 (B6) mice develop mild Lyme arthritis, whereas C3H/HeN (C3H) mice develop severe Lyme arthritis. Differential expression of interleukin 10 (IL-10) has long been associated with mouse strain differences in Lyme pathogenesis; however, the underlying mechanism(s) of this genotype-specific IL-10 regulation remained elusive. Herein we reveal a cAMP-mediated mechanism of IL-10 regulation in B6 macrophages that is substantially diminished in C3H macrophages. Under cAMP and CD14-p38 mitogen-activated protein kinase (MAPK) signaling, B6 macrophages stimulated withB. burgdorferiproduce increased amounts of IL-10 and decreased levels of arthritogenic cytokines, including tumor necrosis factor (TNF). cAMP relaxes chromatin, while p38 increases binding of the transcription factors signal transducer and activator of transcription 3 (STAT3) and specific protein 1 (SP1) to the IL-10 promoter, leading to increased IL-10 production in B6 bone marrow-derived monocytes (BMDMs). Conversely, macrophages derived from arthritis-susceptible C3H mice possess significantly less endogenous cAMP, produce less IL-10, and thus are ill equipped to mitigate the damaging consequences ofB. burgdorferi-induced TNF. Intriguingly, an altered balance between anti-inflammatory and proinflammatory cytokines and CD14-dependent regulatory mechanisms also is operative in primary human peripheral blood-derived monocytes, providing potential insight into the clinical spectrum of human Lyme disease. In line with this notion, we have demonstrated that cAMP-enhancing drugs increase IL-10 production in myeloid cells, thus curtailing inflammation associated with murine Lyme borreliosis. Discovery of novel treatments or repurposing of FDA-approved cAMP-modulating medications may be a promising avenue for treatment of patients with adverse clinical outcomes, including certain post-Lyme complications, in whom dysregulated immune responses may play a role.

scholarly journals An Ixodes scapularis Protein Disulfide Isomerase Contributes to Borrelia burgdorferi Colonization of the Vector

2020 ◽  
Vol 88 (12) ◽  
Author(s):  
Yongguo Cao ◽  
Connor Rosen ◽  
Gunjan Arora ◽  
Akash Gupta ◽  
Carmen J. Booth ◽  
...  
Keyword(s):  
Life Cycle ◽  
Borrelia Burgdorferi ◽  
Protein Disulfide Isomerase ◽  
Inflammatory Responses ◽  
Ixodes Scapularis ◽  
Vertebrate Host ◽  
Content Type ◽  
Disulfide Isomerase ◽  
Complex Interactions ◽  
Protein Disulfide

ABSTRACT Borrelia burgdorferi causes Lyme disease, the most common tick-transmitted illness in North America. When Ixodes scapularis feed on an infected vertebrate host, spirochetes enter the tick gut along with the bloodmeal and colonize the vector. Here, we show that a secreted tick protein, I. scapularis protein disulfide isomerase A3 (IsPDIA3), enhances B. burgdorferi colonization of the tick gut. I. scapularis ticks in which ispdiA3 has been knocked down using RNA interference have decreased spirochete colonization of the tick gut after engorging on B. burgdorferi-infected mice. Moreover, administration of IsPDIA3 antiserum to B. burgdorferi-infected mice reduced the ability of spirochetes to colonize the tick when feeding on these animals. We show that IsPDIA3 modulates inflammatory responses at the tick bite site, potentially facilitating spirochete survival at the vector-host interface as it exits the vertebrate host to enter the tick gut. These data provide functional insights into the complex interactions between B. burgdorferi and its arthropod vector and suggest additional targets to interfere with the spirochete life cycle.

scholarly journals Effect of Complement Component C3 Deficiency on Experimental Lyme Borreliosis in Mice

2003 ◽  
Vol 71 (8) ◽  
pp. 4432-4440 ◽  
Author(s):  
Matthew B. Lawrenz ◽  
R. Mark Wooten ◽  
James F. Zachary ◽  
Scott M. Drouin ◽  
Janis J. Weis ◽  
...  
Keyword(s):  
Lyme Borreliosis ◽  
Early Time ◽  
Heart Tissue ◽  
Complement Component ◽  
Joint Tissue ◽  
Complement Component C3 ◽  
In The Wild ◽  
Spirochete Load ◽  
The Complement System

ABSTRACT Mice deficient in complement component C3 (C3−/−) and syngeneic C57BL/6 control mice were challenged with Borrelia burgdorferi to determine the role of complement in immune clearance and joint histopathology during experimental Lyme borreliosis. Tibiotarsal joint, ear, and heart tissues were monitored for spirochete numbers at 2, 4, 8, and 12 weeks postinoculation with 105 B. burgdorferi B31 clone 5A4 by using quantitative real-time PCR. The spirochete load in joint and ear tissue remained higher in the C3−/− mice than in the wild-type counterparts throughout the 12-week study, whereas the numbers in heart tissue of both groups of mice decreased substantially at 8 to 12 weeks postinfection. Histopathology scores for joint tissue were generally higher in the C3−/− mice compared to C57BL/6 controls at 2 and 4 weeks postinfection, which may reflect the presence of higher numbers of bacteria in the joints at these early time points. Levels of anti-B. burgdorferi immunoglobulin G tended to be reduced in the C3−/− mice compared to control mice. Furthermore, a 5.5-fold-lower number of the complement-sensitive Borrelia garinii was needed to infect C3−/− mice compared to C57BL/6 mice, indicating that its sensitivity to complement is one barrier to infection of the mouse model by B. garinii. These results indicate that the complement system may be important in controlling the early dissemination and progression of B. burgdorferi infection.

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