• This record comes from PubMed

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

. 2021 Aug ; 15 (8) : 2390-2400. [epub] 20210303

Language English Country Great Britain, England Media print-electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Links

PubMed 33658621
PubMed Central PMC8319436
DOI 10.1038/s41396-021-00939-5
PII: 10.1038/s41396-021-00939-5
Knihovny.cz E-resources

Pathogen species often consist of genetically distinct strains, which can establish mixed infections or coinfections in the host. In coinfections, interactions between pathogen strains can have important consequences for their transmission success. We used the tick-borne bacterium Borrelia afzelii, which is the most common cause of Lyme disease in Europe, as a model multi-strain pathogen to investigate the relationship between coinfection, competition between strains, and strain-specific transmission success. Mus musculus mice were infected with one or two strains of B. afzelii, strain transmission success was measured by feeding ticks on mice, and the distribution of each strain in six different mouse organs and the ticks was measured using qPCR. Coinfection and competition reduced the tissue infection prevalence of both strains and changed their bacterial abundance in some tissues. Coinfection and competition also reduced the transmission success of the B. afzelii strains from the infected hosts to feeding ticks. The ability of the B. afzelii strains to establish infection in the host tissues was strongly correlated with their transmission success to the tick vector. Our study demonstrates that coinfection and competition between pathogen strains inside the host tissues can have major consequences for their transmission success.

See more in PubMed

Read AF, Taylor LH. The ecology of genetically diverse infections. Science. 2001;292:1099–102. doi: 10.1126/science.1059410. PubMed DOI

Balmer O, Tanner M. Prevalence and implications of multiple-strain infections. Lancet Infect Dis. 2011;11:868–78. doi: 10.1016/S1473-3099(11)70241-9. PubMed DOI

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. doi: 10.1073/pnas.0500078102. PubMed DOI PMC

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. doi: 10.1073/pnas.0710909105. PubMed DOI PMC

Alizon S, de Roode JC, Michalakis Y. Multiple infections and the evolution of virulence. Ecol Lett. 2013;16:556–67. doi: 10.1111/ele.12076. PubMed DOI

Mideo N. Parasite adaptations to within-host competition. Trends Parasitol. 2009;25:261–8. doi: 10.1016/j.pt.2009.03.001. PubMed DOI

Bashey F. Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philos T R Soc B. 2015;370:1–8. doi: 10.1098/rstb.2014.0301. PubMed DOI PMC

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

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. doi: 10.1086/669905. PubMed DOI

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. doi: 10.1890/08-2291.1. PubMed DOI

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. doi: 10.1098/rstb.2014.0293. PubMed DOI PMC

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. doi: 10.1111/j.0014-3820.2006.tb01215.x. PubMed DOI

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. doi: 10.1098/rspb.2004.2695. PubMed DOI PMC

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. PubMed PMC

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. doi: 10.3389/fcimb.2019.00431. PubMed DOI PMC

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. PubMed PMC

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. PubMed PMC

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. PubMed PMC

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. doi: 10.1186/s13071-014-0608-1. PubMed DOI PMC

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. doi: 10.1016/j.ttbdis.2012.06.008. PubMed DOI

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. doi: 10.1016/j.meegid.2015.09.012. PubMed DOI

Raberg L. Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii. J Evol Biol. 2012;25:1448–53. doi: 10.1111/j.1420-9101.2012.02515.x. PubMed DOI

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. doi: 10.1038/s41598-017-16749-9. PubMed DOI PMC

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. doi: 10.1099/mic.0.26944-0. PubMed DOI

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. doi: 10.1128/JCM.41.11.5059-5065.2003. PubMed DOI PMC

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. doi: 10.1128/AEM.02296-15. PubMed DOI PMC

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. doi: 10.1128/AEM.02552-16. PubMed DOI PMC

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. doi: 10.1038/s41598-016-0028-x. PubMed DOI PMC

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. doi: 10.1111/j.1420-9101.2010.02148.x. PubMed DOI

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. doi: 10.1111/jeb.13075. PubMed DOI

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. doi: 10.1016/j.ttbdis.2011.06.003. PubMed DOI

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. doi: 10.1186/s13071-016-1964-9. PubMed DOI PMC

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. doi: 10.1038/s41598-017-05231-1. PubMed DOI PMC

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. PubMed PMC

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. doi: 10.1016/j.ttbdis.2015.02.007. PubMed DOI

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. doi: 10.1038/s41598-019-43160-3. PubMed DOI PMC

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. doi: 10.1128/AEM.01887-19. PubMed DOI PMC

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. doi: 10.1128/mBio.00434-12. PubMed DOI PMC

Zhong X, Nouri M, Råberg L. Colonization and pathology of Borrelia afzelii in its natural hosts. Ticks Tick Borne Dis. 2019;10:822–7. doi: 10.1016/j.ttbdis.2019.03.017. PubMed DOI

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. doi: 10.1128/IAI.69.7.4303-4312.2001. PubMed DOI PMC

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. doi: 10.1086/343043. PubMed DOI PMC

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. doi: 10.1086/491659. PubMed DOI

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. doi: 10.1128/AEM.70.11.6783-6788.2004. PubMed DOI PMC

Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2009;8:15–25. doi: 10.1038/nrmicro2259. PubMed DOI PMC

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. PubMed PMC

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. doi: 10.1086/591684. PubMed DOI

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. doi: 10.1086/505160. PubMed DOI

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. doi: 10.1016/j.meegid.2013.09.013. PubMed DOI PMC

Tilly K, Rosa PA, Stewart PE. Biology of infection with Borrelia burgdorferi. Infect Dis Clin North Am. 2008;22:217–34. doi: 10.1016/j.idc.2007.12.013. PubMed DOI PMC

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. doi: 10.1086/587530. PubMed DOI

Mackinnon MJ, Read AF. Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution. 1999;53:689–703. doi: 10.1111/j.1558-5646.1999.tb05364.x. PubMed DOI

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. doi: 10.1017/S003118200200272X. PubMed DOI

Brisson D, Dykhuizen DE. ospC diversity in Borrelia burgdorferi: different hosts are different niches. Genetics. 2004;168:713–22. doi: 10.1534/genetics.104.028738. PubMed DOI PMC

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. doi: 10.1093/genetics/151.1.15. PubMed DOI PMC

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. doi: 10.1111/j.1601-5223.1997.00203.x. PubMed DOI

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. doi: 10.1093/genetics/160.3.833. PubMed DOI PMC

Brisson D, Drecktrah D, Eggers C, Samuels DS. Genetics of Borrelia burgdorferi. Annu Rev Genet. 2012;46:515–36. doi: 10.1146/annurev-genet-011112-112140. PubMed DOI PMC

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...