Competition between strains of Borrelia afzelii in the host tissues and consequences for transmission to ticks

Read AF, Taylor LH. The ecology of genetically diverse infections. Science. 2001;292:1099–102.

CAS  PubMed  Article  Google Scholar 

Balmer O, Tanner M. Prevalence and implications of multiple-strain infections. Lancet Infect Dis. 2011;11:868–78.

PubMed  Article  Google Scholar 

de Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, Wargo AR, et al. Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA. 2005;102:7624–8.

PubMed  Article  CAS  Google Scholar 

de Roode JC, Yates AJ, Altizer S. Virulence-transmission trade-offs and population divergence in virulence in a naturally occuring butterfly parasite. Proc Natl Acad Sci USA. 2008;105:7489–94.

PubMed  Article  Google Scholar 

Alizon S, de Roode JC, Michalakis Y. Multiple infections and the evolution of virulence. Ecol Lett. 2013;16:556–67.

PubMed  Article  Google Scholar 

Mideo N. Parasite adaptations to within-host competition. Trends Parasitol. 2009;25:261–8.

PubMed  Article  Google Scholar 

Bashey F. Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philos T R Soc B. 2015;370:1–8.

Article  Google Scholar 

Alizon S, Lion S. Within-host parasite cooperation and the evolution of virulence. P R Soc B-Biol Sci. 2011;278:3738–47.

Google Scholar 

Andersson M, Scherman K, Raberg L. Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity? Am Nat. 2013;181:545–54.

PubMed  Article  Google Scholar 

Balmer O, Stearns SC, Schotzau A, Brun R. Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes. Ecology. 2009;90:3367–78.

PubMed  Article  Google Scholar 

Strandh M, Raberg L. Within-host competition between Borrelia afzelii ospC strains in wild hosts as revealed by massively parallel amplicon sequencing. Philos T Roy Soc B. 2015;370:1–8.

Article  CAS  Google Scholar 

Bell AS, De Roode JC, Sim D, Read AF. Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution. 2006;60:1358–71.

PubMed  Article  Google Scholar 

de Roode JC, Culleton R, Cheesman SJ, Carter R, Read AF. Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. P R Soc B-Biol Sci. 2004;271:1073–80.

Article  Google Scholar 

Genné D, Sarr A, Gomez-Chamorro A, Durand J, Cayol C, Rais O et al. Competition between strains of Borrelia afzelii inside the rodent host and the tick vector. P Roy Soc B-Biol Sci. 2018;285:1–10.

Google Scholar 

Genné D, Sarr A, Rais O, Voordouw MJ. Competition between strains of Borrelia afzelii in immature Ixodes ricinus ticks is not affected by season. Front Cell Infect Microbiol. 2019;9:1–14.

Article  CAS  Google Scholar 

Pollitt LC, Bram JT, Blanford S, Jones MJ, Read AF. Existing infection facilitates establishment and density of malaria parasites in their mosquito vector. PLOS Pathog. 2015;11:1–18.

Reif KE, Palmer GH, Crowder DW, Ueti MW, Noh SM. Restriction of Francisella novicida genetic diversity during infection of the vector midgut. PLOS Pathog. 2014;10:1–11.

Schneider P, Bell AS, Sim DG, O’Donnell AJ, Blanford S, Paaijmans KP, et al. Virulence, drug sensitivity and transmission success in the rodent malaria, Plasmodium chabaudi. P R Soc B-Biol Sci. 2012;279:4677–85.

CAS  Google Scholar 

van Duijvendijk G, Sprong H, Takken W. Multi-trophic interactions driving the transmission cycle of Borrelia afzelii between Ixodes ricinus and rodents: a review. Parasit Vectors. 2015;8:1–11.

Article  CAS  Google Scholar 

Rollend L, Fish D, Childs JE. Transovarial transmission of Borrelia spirochetes by Ixodes scapularis: A summary of the literature and recent observations. Ticks Tick Borne Dis. 2013;4:46–51.

PubMed  Article  Google Scholar 

Jacquet M, Durand J, Rais O, Voordouw MJ. Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen, Borrelia afzelii. Infect Genet Evolution. 2015;36:131–40.

CAS  Article  Google Scholar 

Raberg L. Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii. J Evol Biol. 2012;25:1448–53.

CAS  PubMed  Article  Google Scholar 

Grillon A, Westermann B, Cantero P, Jaulhac B, Voordouw MJ, Kapps D, et al. Identification of Borrelia protein candidates in mouse skin for potential diagnosis of disseminated Lyme borreliosis. Sci Rep. 2017;7:1–13.

CAS  Article  Google Scholar 

Bunikis J, Garpmo U, Tsao J, Berglund J, Fish D, Barbour AG. Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe. Microbiol-Sgm. 2004;150:1741–55.

CAS  Article  Google Scholar 

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;41:5059–65.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Durand J, Jacquet M, Paillard L, Rais O, Gern L, Voordouw MJ. Cross-immunity and community structure of a multiple-strain pathogen in the tick vector. Appl Environ Microbiol. 2015;81:7740–52.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Durand J, Herrmann C, Genné D, Sarr A, Gern L, Voordouw MJ. Multistrain infections with Lyme borreliosis pathogens in the tick vector. Appl Environ Microbiol. 2017;83:1–14.

Article  Google Scholar 

Durand J, Jacquet M, Rais O, Gern L, Voordouw MJ. Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field. Sci Rep. 2017;7: 1–9.

Article  CAS  Google Scholar 

Hellgren O, Andersson M, Raberg L. The genetic structure of Borrelia afzelii varies with geographic but not ecological sampling scale. J Evol Biol. 2011;24:159–67.

CAS  PubMed  Article  PubMed Central  Google Scholar 

Raberg L, Hagstrom A, Andersson M, Bartkova S, Scherman K, Strandh M, et al. Evolution of antigenic diversity in the tick-transmitted bacterium Borrelia afzelii: a role for host specialization? J Evol Biol. 2017;30:1034–41.

CAS  PubMed  Article  Google Scholar 

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;2:137–42.

PubMed  Article  Google Scholar 

Rynkiewicz EC, Brown J, Tufts DM, Huang C-I, Kampen H, Bent SJ, et al. Closely-related Borrelia burgdorferi (sensu stricto) strains exhibit similar fitness in single infections and asymmetric competition in multiple infections. Parasit Vectors. 2017;10:1–9.

Article  CAS  Google Scholar 

Belli A, Sarr A, Rais O, Rego ROM, Voordouw MJ. Ticks infected via co-feeding transmission can transmit Lyme borreliosis to vertebrate hosts. Sci Rep. 2017;7:1–13.

CAS  Article  Google Scholar 

Jacquet M, Margos G, Fingerle V, Voordouw MJ. Comparison of the lifetime host-to-tick transmission between two strains of the Lyme disease pathogen Borrelia afzelii. Parasit Vectors 2016;9:1–8.

Tonetti N, Voordouw MJ, Durand J, Monnier S, Gern L. Genetic variation in transmission success of the Lyme borreliosis pathogen Borrelia afzelii. Ticks Tick Borne Dis. 2015;6:334–43.

PubMed  Article  Google Scholar 

Gomez-Chamorro A, Battilotti F, Cayol C, Mappes T, Koskela E, Boulanger N, et al. Susceptibility to infection with Borrelia afzelii and TLR2 polymorphism in a wild reservoir host. Sci Rep. 2019;9:1–12.

CAS  Article  Google Scholar 

Gomez-Chamorro A, Heinrich V, Sarr A, Roethlisberger O, Genné D, Bregnard C, et al. Maternal antibodies provide bank voles with strain-specific protection against infection by the Lyme disease pathogen. Appl Environ Microbiol. 2019;85:1–12.

Article  Google Scholar 

Baum E, Hue F, Barbour AG. Experimental infections of the reservoir species Peromyscus leucopus with diverse strains of Borrelia burgdorferi, a Lyme disease agent. mBio. 2012;3:1–11.

Article  CAS  Google Scholar 

Zhong X, Nouri M, Råberg L. Colonization and pathology of Borrelia afzelii in its natural hosts. Ticks Tick Borne Dis. 2019;10:822–7.

PubMed  Article  PubMed Central  Google Scholar 

Wang G, Ojaimi C, Iyer R, Saksenberg V, McClain SA, Wormser GP, et al. Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/HeJ mice. Infect Immun. 2001;69:4303–12.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Wang GQ, Ojaimi C, Wu HY, Saksenberg V, Iyer R, Liveris D, et al. 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;186:782–91.

CAS  PubMed  PubMed Central  Article  Google Scholar 

de Roode JC, Helinski MEH, Anwar MA, Read AF. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am Nat. 2005;166:531–42.

PubMed  Article  Google Scholar 

Derdakova M, Dudioak V, Brei B, Brownstein JS, Schwartz I, Fish D. Interaction and transmission of two Borrelia burgdorferi sensu stricto strains in a tick-rodent maintenance system. Appl Environ Microbiol. 2004;70:6783–8.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2009;8:15–25.

Article  CAS  Google Scholar 

Wale N, Sim DG, Read AF. A nutrient mediates intraspecific competition between rodent malaria parasites in vivo. P R Soc B-Biol Sci. 2017;284:1–8.

Google Scholar 

Mideo N, Barclay VC, Chan BHK, Savill NJ, Read AF, Day T. Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. Am Nat. 2008;172:E214–38.

Article  Google Scholar 

Raberg L, de Roode JC, Bell AS, Stamou P, Gray D, Read AF. The role of immune-mediated apparent competition in genetically diverse malaria infections. Am Nat. 2006;168:41–53.

PubMed  Article  Google Scholar 

Fairlie-Clarke KJ, Allen JE, Read AF, Graham AL. Quantifying variation in the potential for antibody-mediated apparent competition among nine genotypes of the rodent malaria parasite Plasmodium chabaudi. Infect Genet Evolution. 2013;20:270–5.

CAS  Article  Google Scholar 

Tilly K, Rosa PA, Stewart PE. Biology of infection with Borrelia burgdorferi. Infect Dis Clin North Am. 2008;22:217–34.

PubMed  PubMed Central  Article  Google Scholar 

Hartemink NA, Randolph SE, Davis SA, Heesterbeek JAP. The basic reproduction number for complex disease systems: Defining R-0 for tick-borne infections. Am Nat. 2008;171:743–54.

CAS  PubMed  Article  PubMed Central  Google Scholar 

Mackinnon MJ, Read AF. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution. 1999;53:689–703.

PubMed  Article  PubMed Central  Google Scholar 

Mackinnon MJ, Read AF. The effects of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology. 2003;126:103–12.

CAS  PubMed  Article  PubMed Central  Google Scholar 

Brisson D, Dykhuizen DE. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics. 2004;168:713–22.

CAS  PubMed  PubMed Central  Article  Google Scholar 

Wang IN, Dykhuizen DE, Qiu W, Dunn JJ, Bosler EM, Luft BJ. Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics. 1999;151:15–30.

CAS  PubMed  PubMed Central  Google Scholar 

Qiu WG, Bosler EM, Campbell JR, Ugine GD, Wang IN, Luft BJ, et al. A population genetic study of Borrelia burgdorferi sensu stricto from eastern Long Island, New York, suggested frequency-dependent selection, gene flow and host adaptation. Hereditas. 1997;127:203–16.

CAS  PubMed  Article  Google Scholar 

Qiu WG, Dykhuizen DE, Acosta MS, Luft BJ. 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;160:833–49.

CAS  PubMed  PubMed Central  Google Scholar 

Brisson D, Drecktrah D, Eggers C, Samuels DS. Genetics of Borrelia burgdorferi. Annu Rev Genet. 2012;46:515–36.

CAS  PubMed  Article  Google Scholar