Genetic variation in transmission success of the Lyme borreliosis pathogen Borrelia afzelii

Ticks and Tick-borne Diseases

Volumn 6, Issue 3, 2015, Pages 334-343

  Tonetti, Nicolas ^a   Voordouw, Maarten J ^a   Durand, Jonas ^a   Monnier, Séverine ^a   Gern, Lise ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Borrelia afzelii; Co feeding transmission; Ixodes ricinus; Lyme borreliosis; Reproductive number; Vector borne pathogen

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; BACTERIUM DETECTION; BACTERIUM ISOLATE; BORRELIA AFZELII; CONTROLLED STUDY; GENETIC CORRELATION; GENETIC VARIABILITY; IXODES RICINUS; LYME DISEASE; MALE; MOUSE; NONHUMAN; OSPC GENE; PHENOTYPE; PRIORITY JOURNAL; STRAIN DIFFERENCE; ANIMAL; BAGG ALBINO MOUSE; BORRELIA BURGDORFERI; DNA SEQUENCE; GENETIC VARIATION; GENETICS; GERMFREE ANIMAL; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; IXODES; MICROBIOLOGY; PARASITE VECTOR; PHYSIOLOGY; TRANSMISSION;

BACTERIA (MICROORGANISMS); BORRELIA AFZELII; IXODES RICINUS; IXODIDA; RODENTIA; VERTEBRATA;

ANIMALS; ARACHNID VECTORS; BORRELIA BURGDORFERI GROUP; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; IXODES; LYME DISEASE; MALE; MICE; MICE, INBRED BALB C; SEQUENCE ANALYSIS, DNA; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 84928213485     PISSN: 1877959X     EISSN: 18779603     Source Type: Journal    
DOI: 10.1016/j.ttbdis.2015.02.007     Document Type: Article

References (74)

1. Alghaferi M.Y., Anderson J.M., Park J., Auwaerter P.G., Aucot J.N., Norris D.E., Dumler J.S. Borrelia burgdorferi OspC heterogeneity among human and murine isolates from a defined region of northern Maryland and southern Pennsylvania: lack of correlation with invasive and noninvasive genotypes. J. Clin. Microbiol. 2005, 43:1874-1879.
2. Andersson M., Scherman K., Raberg L., Råberg L. Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity?. Am. Nat. 2013, 181:545-554.
3. Baranton G., Seinost G., Theodore G., Postic D., Dykhuizen D. Distinct levels of genetic diversity of Borrelia burgdorferi are associated with different aspects of pathogenicity. Res. Microbiol. 2001, 152:149-156.
4. Baum E., Hue F., Barbour A.G. Experimental infections of the reservoir species Peromyscus leucopus with diverse strains of Borrelia burgdorferi, a Lyme disease agent. mBio 2012, 3. e00434-512.
5. Brisson D., Dykhuizen D.E. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics 2004, 168:713-722.
6. Bunikis J., Garpmo U., Tsao J., Berglund J., Fish D., Barbour A.G. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 2004, 150:1741-1755.
7. Crippa M., Rais O., Gern L. Investigations on the mode and dynamics of transmission and infectivity of Borrelia burgdorferi sensu stricto and Borrelia afzelii in Ixodes ricinus ticks. Vector Borne Zoonot. Dis. 2002, 2:3-9.
8. de Roode J.C., Pansini R., Cheesman S.J., Helinski M.E.H., Huijben S., Wargo A.R., Bell A.S., Chan B.H.K., Walliker D., Read A.F. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:7624-7628.
9. de Roode J.C., Yates A.J., Altizer S. Virulence-transmission trade-offs and population divergence in virulence in a naturally occuring butterfly parasite. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:7489-7494.
10. de Silva A.M., Fikrig E. Growth and migration of Borrelia burgdorferi in Ixodes ticks during blood feeding. Am. J. Trop. Med. Hyg. 1995, 53:397-404.
11. Derdakova M., Dudioak V., Brei B., Brownstein J.S., Schwartz I., Fish D. Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system. Appl. Environ. Microbiol. 2004, 70:6783-6788.
12. Dolan M., Piesman J., Schneider B., Schriefer M., Brandt K., Zeidner N. Comparison of disseminated and nondisseminated strains of Borrelia burgdorferi sensu stricto in mice naturally infected by tick bite. Infect. Immun. 2004, 72:5262-5266.
13. Dykhuizen D.E., Baranton G. The implications of a low rate of horizontal transfer in Borrelia. Trends Microbiol. 2001, 9:344-350.
14. Dykhuizen D.E., Brisson D., Sandigursky S., Wormser G.P., Nowakowski J., Nadelman R.B., Schwartz I. Short report: The propensity of different Borrelia burgdorferi sensu stricto genotypes to cause disseminated infections in humans. Am. J. Trop. Med. Hyg. 2008, 78:806-810.
15. Earnhart C.G., Buckles E.L., Dumler J.S., Marconi R.T. Demonstration of OspC type diversity in invasive human Lyme disease isolates and identification of previously uncharacterized epitopes that define the specificity of the OspC murine antibody response. Infect. Immun. 2005, 73:7869-7877.
16. Ebert D. Evolution - experimental evolution of parasites. Science 1998, 282:1432-1435.
17. Ebert D., Bull J.J. Challenging the trade-off model for the evolution of virulence: is virulence management feasible?. Trends Microbiol. 2003, 11:15-20.
18. Fingerle V., Goettner G., Gern L., Wilske B., Schulte-Spechtel U. Complementation of a Borrelia afzelii OspC mutant highlights the crucial role of OspC for dissemination of Borrelia afzelii in Ixodes ricinus. Int. J. Med. Microbiol. 2007, 297:97-107.
19. Fraser C., Hollingsworth T.D., Chapman R., de Wolf F., Hanage W.P. Variation in HIV-1 set-point viral load: Epidemiological analysis and an evolutionary hypothesis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17441-17446.
20. Gern L., Lebet N., Moret J. Dynamics of Borrelia burgdorferi infection in nymphal Ixodes ricinus ticks during feeding. Exp. Appl. Acarol. 1996, 20:649-658.
21. Gern L., Rais O. Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J. Med. Entomol. 1996, 33:189-192.
22. Gern L., Siegenthaler M., Hu C.M., Leuba-Garcia S., Humair P.F., Moret J. Borrelia burgdorferi in rodents (Apodemus flavicollis and A. sylvaticus): duration and enhancement of infectivity for Ixodes ricinus ticks. Eur. J. Epidemiol. 1994, 10:75-80.
23. Gern L., Zhu Z., Aeschlimann A. Development of Borrelia burgdorferi in Ixodes ricinus females during blood feeding. Ann. Parasitol. Hum. Comp. 1990, 65:89-93.
24. Graf J.-F. Copulation, nutrition et ponte chez Ixodes ricinus L. (Ixodoidea: Ixodidae) - 1e partie. Bull. Soc. Entomol. Suisse 1978, 51:89-97.
25. Grimm D., Tilly K., Byram R., Steward P.E., Krum J.G., Bueschel D.M., Schwan T.G., Policastro P.F., Elias A.F., Rosa P.A. Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:3142-3147.
26. Gupta S., Ferguson N., Anderson R. Chaos, persistence, and evolution of strain structure in antigenically diverse infectious agents. Science 1998, 280:912-915.
27. Hanincova K., Ogden N.H., Diuk-Wasser M., Pappas C.J., Iyer R., Fish D., Schwartz I., Kurtenbach K. Fitness variation of Borrelia burgdorferi sensu stricto strains in mice. Appl. Environ. Microbiol. 2008, 74:153-157.
28. Harrison A., Bennett N. The importance of the aggregation of ticks on small mammal hosts for the establishment and persistence of tick-borne pathogens: an investigation using the R(0) model. Parasitology 2012, 139:1605-1613.
29. Harrison A., Montgomery W.I., Bown K.J. Investigating the persistence of tick-borne pathogens via the R-0 model. Parasitology 2011, 138:896-905.
30. Hartemink N.A., Randolph S.E., Davis S.A., Heesterbeek J.A.P. The basic reproduction number for complex disease systems: Defining R-0 for tick-borne infections. Am. Nat. 2008, 171:743-754.
31. Hellgren O., Andersson M., Raberg L., Råberg L. The genetic structure of Borrelia afzelii varies with geographic but not ecological sampling scale. J. Evol. Biol. 2011, 24:159-167.
32. Herrmann C., Gern L., Voordouw M. Species co-occurrence patterns among Lyme borreliosis pathogens in the tick vector Ixodes ricinus. Appl. Environ. Microbiol. 2013, 79:7273-7280.
33. Hu C.M., Cheminade Y., Perret J.L., Weynants V., Lobet Y., Gern L. Early detection of Borrelia burgdorferi sensu lato infection in Balb/c mice by co-feeding Ixodes ricinus ticks. Int. J. Med. Microbiol. 2003, 293:421-426.
34. Humair P.F., Gern L. Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Trop. 1998, 69:213-227.
35. Humair P.F., Péter O., Wallich R., Gern L. Strain variation of Lyme disease spirochetes isolated from Ixodes ricinus ticks and rodents collected in two endemic areas in Switzerland. J. Med. Entomol. 1995, 32:433-438.
36. Humair P.F., Rais O., Gern L. Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 1999, 118:33-42.
37. Jouda F., Perret J.L., Gern L. Density of questing Ixodes ricinus nymphs and adults infected by Borrelia burgdorferi sensu lato in Switzerland: spatio-temporal pattern at a regional scale. Vector-Borne Zoonot. Dis. 2004, 4:23-32.
38. Kurtenbach K., Peacey M., Rijpkema S.G.T., Hoodless A.N., Nuttall P.A., Randolph S.E. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl. Environ. Microbiol. 1998, 64:1169-1174.
39. Lagal V., Postic D., Ruzic-Sabljic E., Baranton G. Genetic diversity among Borrelia strains determined by single-strand conformation polymorphism analysis of the ospC gene and its association with invasiveness. J. Clin. Microbiol. 2003, 41:5059-5065.
40. Lindsay L.R., Barker I.K., Surgeoner G.A., McEwen S.A., Campbell G.D. Duration of Borrelia burgdorferi infectivity in white-footed mice for the tick vector Ixodes scapularis under laboratory and field conditions in Ontario. J. Wildl. Dis. 1997, 33:766-775.
41. Mackinnon M.J., Gandon S., Read A.F. Virulence evolution in response to vaccination: The case of malaria. Vaccine 2008, 26:C42-C52.
42. Mackinnon M.J., Read A.F. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 1999, 53:689-703.
43. Mbow M.L., Christe M., Rutti B., Brossard M. Absence of acquired resistance to nymphal Ixodes ricinus ticks in BALB/c mice developing cutaneous reactions. J. Parasitol. 1994, 80:81-87.
44. Morán Cadenas F., Rais O., Jouda F., Douet V., Humair P.-F. Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along a North- and South-facing altitudinal gradient on Chaumont Mountain, Switzerland. J. Med. Entomol. 2007, 44:683-693.
45. Morán Cadenas F.M., Rais O., Humair P.F., Douet V., Moret J., Gern L. Identification of host bloodmeal source and Borrelia burgdorferi sensu lato in field-collected Ixodes ricinus ticks in Chaumont (Switzerland). J. Med. Entomol. 2007, 44:1109-1117.
46. Ohnishi J., Piesman J., de Silva A.M. Antigenic and genetic heterogeneity of Borrelia burgdorferi populations transmitted by ticks. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:670-675.
47. Pal U., Yang X.F., Chen M., Bockenstedt L.K., Anderson J.F., Flavell R.A., Norgard M.V., Fikrig E. OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J. Clin. Investig. 2004, 113:220-230.
48. Pérez D., Kneubühler Y., Rais O., Jouda F., Gern L. Borrelia afzelii ospC genotype diversity in Ixodes ricinus questing ticks and ticks from rodents in two Lyme borreliosis endemic areas: Contribution of co-feeding ticks. Ticks Tick-Borne Dis. 2011, 2:137-142.
49. Piesman J., Gern L. Lyme borreliosis in Europe and North America. Parasitology 2004, 129:S191-S220.
50. Piesman J., Schneider B.S., Zeidner N.S. Use of quantitative PCR to measure density of Borrelia burgdorferi in the midgut and salivary glands of feeding tick vectors. J. Clin. Microbiol. 2001, 39:4145-4148.
51. Qiu W.G., Dykhuizen D.E., Acosta M.S., Luft B.J. Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the northeastern United States. Genetics 2002, 160:833-849.
52. Qiu W.G., Schutzer S.E., Bruno J.F., Attie O., Yun X., Dunn J.J., Fraser C.M., Casjens S.R., Luft B.J. Genetic exchange and plasmid transfers in Borrelia burgdorferi sensu stricto revealed by three-way genome comparisons and multilocus sequence typing. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:14150-14155.
53. Raberg L. Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii. J. Evol. Biol. 2012, 25:1448-1453.
54. Radolf J.D., Caimano M.J. The long strange trip of Borrelia burgdorferi outer-surface protein C. Mol. Microbiol. 2008, 69:1-4.
55. Randolph S.E. Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitol. Today 1998, 14:186-192.
56. Randolph S.E. Transmission of tick-borne pathogens between co-feeding ticks: Milan Labuda's enduring paradigm. Ticks Tick-Borne Dis. 2011, 2:179-182.
57. Randolph S.E., Gern L., Nuttall P.A. Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. Parasitol. Today 1996, 12:472-479.
58. Randolph S.E., Miklisova D., Lysy J., Rogers D.J., Labuda M. Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. Parasitology 1999, 118:177-186.
59. Richter D., Allgower R., Matuschka F.R. Co-feeding transmission and its contribution to the perpetuation of the Lyme disease spirochete Borrelia afzelii. Emerg. Infect. Dis. 2002, 8:1421-1425.
60. Richter D., Postic D., Sertour N., Livey I., Matuschka F.R., Baranton G. Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp nov. Int. J. Syst. Evol. Microbiol. 2006, 56:873-881.
61. Seinost G., Dykhuizen D.E., Dattwyler R.J., Golde W.T., Dunn J.J., Wang I.N., Wormser G.P., Schriefer M.E., Luft B.J. Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect. Immun. 1999, 67:3518-3524.
62. Sinsky R.J., Piesman J. Ear punch biopsy method for detection and isolation of Borrelia burgdorferi from rodents. J. Clin. Microbiol. 1989, 27:1723-1727.
63. Stearns S.C. The evolution of life-histories 1992, Oxford University Press, Oxford.
64. Tilly K., Krum J.G., Bestor A., Jewett M.W., Grimm D., Bueschel D., Byram R., Dorward D., VanRaden M.J., Steward P., Rosa P. Borrelia burgdorferi ospC protein required exclusively in a crucial early stage of mammalian infection. Infect. Immun. 2006, 74:3554-3564.
65. Tilly K., Rosa P.A., Stewart P.E. Biology of infection with Borrelia burgdorferi. Infect. Dis. Clin. North Am. 2008, 22:217-234.
66. Titus R.G., Ribeiro J.M.C. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance leishmania infectivity. Science 1988, 239:1306-1308.
67. Tsao J. Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Vet. Res. (Paris) 2009, 40.
68. Voordouw M.J. Co-feeding transmission in Lyme disease pathogens. Parasitology 2015, 142:290-302.
69. Wang G., Ojaimi C., Iyer R., Saksenberg V., McClain S.A., Wormser G.P., Schwartz I. Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/HeJ mice. Infect. Immun. 2001, 69:4303-4312.
70. Wang G.Q., Ojaimi C., Wu H.Y., Saksenberg V., Iyer R., Liveris D., McClain S.A., Wormser G.P., Schwartz I. Disease severity in a murine model of Lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J. Infect. Dis. 2002, 186:782-791.
71. Wang I.N., Dykhuizen D.E., Qiu W., Dunn J.J., Bosler E.M., Luft B.J. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 1999, 151:15-30.
72. Wikel S.K. Tick modulation of host immunity: an important factor in pathogen transmission. Int. J. Parasitol. 1999, 29:851-859.
73. Wormser G.P., Brisson D., Liveris D., Hanincova K., Sandigursky S., Nowakowski J., Nadelman R.B., Ludin S., Schwartz I. Borrelia burgdorferi genotype predicts the capacity for hematogenous dissemination during early Lyme disease. J. Infect. Dis. 2008, 198:1358-1364.
74. Zeidner N.S., Schneider B.S., Dolan M.C., Piesman J. An analysis of spirochete load, strain, and pathology in a model of tick-transmitted Lyme borreliosis. Vector Borne Zoonot. Dis. 2001, 1:35-44.