Within-host competition between Borrelia afzelii ospC strains in wild hosts as revealed by massively parallel amplicon sequencing

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1675, 2015, Pages

  Strandh, Maria ^a   Råberg, Lars ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Borrelia afzelii; Mixed infections; OspC; Virulence; Within host competition

Indexed keywords

BACTERIUM; EPIDEMIOLOGY; EVOLUTIONARY BIOLOGY; HETEROGENEITY; INFECTIOUS DISEASE; INFECTIVITY; INOCULATION; INTRASPECIFIC COMPETITION; INTRASPECIFIC INTERACTION; VIRULENCE;

BORRELIA AFZELII;

BACTERIAL ANTIGEN; BACTERIAL DNA; OSPC PROTEIN; OUTER MEMBRANE PROTEIN;

ANIMAL; ARVICOLINAE; BACTERIAL GENE; BORRELIA BURGDORFERI; DNA SEQUENCE; GENETICS; GENOTYPE; HIGH THROUGHPUT SEQUENCING; HOST PATHOGEN INTERACTION; HOST RANGE; LYME DISEASE; MICROBIOLOGY; MURINE; PATHOGENICITY; SHREW; VETERINARY; VIROLOGY;

ANIMALS; ANTIGENS, BACTERIAL; ARVICOLINAE; BACTERIAL OUTER MEMBRANE PROTEINS; BORRELIA BURGDORFERI GROUP; DNA, BACTERIAL; GENES, BACTERIAL; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; LYME DISEASE; MURINAE; SEQUENCE ANALYSIS, DNA; SHREWS;

EID: 84936970610     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0293     Document Type: Article

References (40)

1. Balmer O, Tanner M. 2011 Prevalence and implications of multiple-strain infections. Lancet Infect. Dis. 11, 868-878. (doi:10. 1016/S1473-3099(11)70241-9)
2. Read AF, Taylor LH. 2001 The ecology of genetically diverse infections. Science 292, 1099-1102. (doi:10. 1126/science. 1059410)
3. De Roode JC et al. 2005 Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl Acad. Sci. USA 102, 7624-7628. (doi:10. 1073/ pnas. 0500078102)
4. Bell AS, De Roode JC, Sim D, Read AF. 2006 Withinhost competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60, 1358-1371. (doi:10. 1111/j. 0014-3820. 2006. tb01215. x)
5. Alizon S, De Roode JC, Michalakis Y. 2013 Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556-567. (doi:10. 1111/ele. 12076)
6. Taylor LH, Walliker D, Read AF. 1997 Mixedgenotype infections of malaria parasites: withinhost dynamics and transmission success of competing clones. Proc. R. Soc. Lond. B 264, 927-935. (doi:10. 1098/rspb. 1997. 0128)
7. De Roode JC, Culleton R, Cheesman SJ, Carter R, Read AF. 2004 Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proc. R. Soc. Lond. B 271, 1073-1080. (doi:10. 1098/rspb. 2004. 2695)
8. De Roode JC, Helinski MEH, Anwar MA, Read AF. 2005 Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 166, 531-542. (doi:10. 1086/491659)
9. Hodgson DJ, Hitchman RB, Vanbergen AJ, Hails RS, Possee RD, Cory JS. 2004 Host ecology determines the relative fitness of virus genotypes in mixedgenotype nucleopolyhedrovirus infections. J. Evol. Biol. 17, 1018-1025. (doi:10. 1111/j. 1420-9101. 2004. 00750. x)
10. Brisson D, Drecktrah D, Eggers CH, Samuels DS. 2012 Genetics of Borrelia burgdorferi. Annu. Rev. Genet. 46, 515-536. (doi:10. 1146/annurev-genet-011112-112140)
11. Kurtenbach K, Hanincová K, Tsao JI, Margos G, Fish D, Ogden NH. 2006 Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat. Rev. Microbiol. 4, 660-669. (doi:10. 1038/ nrmicro1475)
12. Hanincová K, Schäfer SM, Etti S, Sewell H-S, Taragelová V, Ziak D, Labuda M, Kurtenbach K. 2003 Association of Borrelia afzelii with rodents in Europe. Parasitology 126, 11-20. (doi:10. 1017/ S0031182002002548)
13. Hellgren O, Andersson M, Råberg L. 2011 The genetic structure of Borrelia afzelii varies with geographic but not ecological sampling scale. J. Evol. Biol. 24, 159-167. (doi:10. 1111/j. 1420-9101. 2010. 02148. x)
14. Wang IN, Dykhuizen DE, Qiu W, Dunn JJ, Bosler EM, Luft BJ. 1999 Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 151, 15-30.
15. Pérez D, Kneubühler Y, Rais O, Jouda F, Gern L. 2011 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. 2, 137-142. (doi:10. 1016/j. ttbdis. 2011. 06. 003)
16. Derdáková M, Dudiòák V, Brei B, Brownstein S, Schwartz I, Fish D. 2004 Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system. Appl. Environ. Microbiol. 70, 6783-6788. (doi:10. 1128/AEM. 70. 11. 6783)
17. Andersson M, Scherman K, Råberg L. 2013 Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity? Am. Nat. 181, 545-554. (doi:10. 1086/669905)
18. Laird P, Zijderveld A, Linders K, Rudnicki M. 1991 Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293. (doi:10. 1093/nar/ 19. 15. 4293)
19. Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG. 2004 Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiology 150, 1741-1755. (doi:10. 1099/mic. 0. 26944-0)
20. Råberg L. 2012 Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii. J. Evol. Biol. 25, 1448-1453. (doi:10. 1111/j. 1420-9101. 2012. 02515. x)
21. Andrews S. 2012 FastQC: A quality control tool for high throughput sequence data. See http://www. bioinformatics. babraham. ac. uk/projects/fastqc/.
22. Stuglik MT, Radwan J, Babik W. 2011 jMHC: software assistant for multilocus genotyping of gene families using next-generation amplicon sequencing. Mol. Ecol. Resour. 11, 739-742. (doi:10. 1111/j. 1755-0998. 2011. 02997. x)
23. Dykhuizen DE, Baranton G. 2001 The implications of a low rate of horizontal transfer in Borrelia. Trends Microbiol. 9, 344-350. (doi:10. 1016/S0966-842X(01)02066-2)
24. Travinsky B, Bunikis J, Barbour AG. 2010 Geographic differences in genetic locus linkages for Borrelia burgdorferi. Emerg. Infect. Dis. 16, 1147-1150. (doi:10. 3201/eid1607. 091452)
25. Juliano JJ, Porter K, Mwapasa V, Sem R, Rogers WO, Ariey F, Wongsrichanalai C, Read A, Meshnick SR. 2010 Exposing malaria in-host diversity and estimating population diversity by capture-recapture using massively parallel pyrosequencing. Proc. Natl Acad. Sci. USA 107, 20 138-20 143. (doi:10. 1073/ pnas. 1007068107)
26. Mcelroy K, Thomas T, Luciani F. 2014 Deep sequencing of evolving pathogen populations: applications, errors, and bioinformatic solutions. Microb. Inform. Exp. 4, 1. (doi:10. 1186/2042-5783-4-1)
27. Amend A, Seifert K, Bruns T. 2010 Quantifying microbial communities with 454 pyrosequencing: does read abundance count? Mol. Ecol. 19, 5555-5565. (doi:10. 1111/j. 1365-294X. 2010. 04898. x)
28. Zhou J et al. 2011 Reproducibility and quantitation of amplicon sequencing-based detection. ISME J. 5, 1303-1313. (doi:10. 1038/ ismej. 2011. 11)
29. Pilloni G, Granitsiotis MS, Engel M, Lueders T. 2012 Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to T-RFLP fingerprinting of aquifer microbes. PLoS ONE 7, e40467. (doi:10. 1371/journal. pone. 0040467)
30. Zhan A, He S, Brown EA, Chain FJJ, Therriault TW, Abbott CL, Heath DD, Cristescu ME, MacIsaac HJ. 2014 Reproducibility of pyrosequencing data for biodiversity assessment in complex communities. Methods Ecol. Evol. 5, 881-890. (doi:10. 1111/2041-210X. 12230)
31. Soininen J, Passy S, Hillebrand H. 2012 The relationship between species richness and evenness: a meta-analysis of studies across aquatic ecosystems. Oecologia 169, 803-809. (doi:10. 1007/ s00442-011-2236-1)
32. Laird RA, Schamp BS. 2006 Competitive intransitivity promotes species coexistence. Am. Nat. 168, 182-193. (doi:10. 1086/506259)
33. Bruce MC. 2000 Cross-species interactions between malaria parasites in humans. Science 287, 845-848. (doi:10. 1126/science. 287. 5454. 845)
34. Råberg L, De Roode JC, Bell AS, Stamou P, Gray D, Read AF. 2006 The role of immune-mediated apparent competition in genetically diverse malaria infections. Am. Nat. 168, 41-53. (doi:10. 1086/ 505160)
35. Santhanam J, Råberg L, Read AF, Savill NJ. 2014 Immune-mediated competition in rodent malaria is most likely caused by induced changes in innate immune clearance of merozoites. PLoS Comput. Biol. 10, e1003416. (doi:10. 1371/journal. pcbi. 1003416)
36. Probert WS, Crawford M, Cadiz RB, Lefebvre RB. 1997 Immunization with outer surface protein (Osp) A, but not OspC, provides cross-protection of mice challenged with North American isolates of Borrelia burgdorferi. J. Infect. Dis. 175, 400-405. (doi:10. 1093/infdis/175. 2. 400)
37. Alban PS, Johnson PW, Nelson DR. 2000 Serumstarvation-induced changes in protein synthesis and morphology of Borrelia burgdorferi. Microbiology 146, 119-127.
38. Kurtenbach K, Dizij A, Seitz HM, Margos G, Moter SE, Kramer MD, Wallich R, Schaible UE, Simon MM. 1994 Differential immune responses to Borrelia burgdorferi in European wild rodent species influence spirochete transmission to Ixodes ricinus L. (Acari: Ixodidae). Infect. Immun. 62, 5344-5352.
39. Voordouw MJ, Lachish S, Dolan MC. 2015 The Lyme disease pathogen has no effect on the survival of its rodent reservoir host. PLoS ONE 10, e0118265. (doi:10. 1371/journal. pone. 0118265)
40. Lord CC, Barnard B, Day K, Hargrove JW, McNamara JJ, Paul RE, Trenholme K, Woolhouse ME. 1999 Aggregation and distribution of strains in microparasites. Phil. Trans. R. Soc. Lond. B 354, 799-807. (doi:10. 1098/rstb. 1999. 0432)