Variation among strains of Borrelia burgdorferi in host tissue abundance and lifetime transmission determine the population strain structure in nature

. 2023 Aug ; 19 (8) : e1011572. [epub] 20230822

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37607182
Odkazy

PubMed 37607182
PubMed Central PMC10473547
DOI 10.1371/journal.ppat.1011572
PII: PPATHOGENS-D-23-00607
Knihovny.cz E-zdroje

Pathogen life history theory assumes a positive relationship between pathogen load in host tissues and pathogen transmission. Empirical evidence for this relationship is surprisingly rare due to the difficulty of measuring transmission for many pathogens. The comparative method, where a common host is experimentally infected with a set of pathogen strains, is a powerful approach for investigating the relationships between pathogen load and transmission. The validity of such experimental estimates of strain-specific transmission is greatly enhanced if they can predict the pathogen population strain structure in nature. Borrelia burgdorferi is a multi-strain, tick-borne spirochete that causes Lyme disease in North America. This study used 11 field-collected strains of B. burgdorferi, a rodent host (Mus musculus, C3H/HeJ) and its tick vector (Ixodes scapularis) to determine the relationship between pathogen load in host tissues and lifetime host-to-tick transmission (HTT). Mice were experimentally infected via tick bite with 1 of 11 strains. Lifetime HTT was measured by infesting mice with I. scapularis larval ticks on 3 separate occasions. The prevalence and abundance of the strains in the mouse tissues and the ticks were determined by qPCR. We used published databases to obtain estimates of the frequencies of these strains in wild I. scapularis tick populations. Spirochete loads in ticks and lifetime HTT varied significantly among the 11 strains of B. burgdorferi. Strains with higher spirochete loads in the host tissues were more likely to infect feeding larval ticks, which molted into nymphal ticks that had a higher probability of B. burgdorferi infection (i.e., higher HTT). Our laboratory-based estimates of lifetime HTT were predictive of the frequencies of these strains in wild I. scapularis populations. For B. burgdorferi, the strains that establish high abundance in host tissues and that have high lifetime transmission are the strains that are most common in nature.

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Alizon S, Hurford A, Mideo N, Van Baalen M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J Evol Biol. 2009;22(2):245–59. doi: 10.1111/j.1420-9101.2008.01658.x WOS:000262516800002. PubMed DOI

Mackinnon MJ, Gandon S, Read AF. Virulence evolution in response to vaccination: The case of malaria. Vaccine. 2008;26:C42–C52. doi: 10.1016/j.vaccine.2008.04.012 WOS:000258164200007. PubMed DOI PMC

Frank SA. Models of parasite virulence. Q Rev Biol. 1996;71(1):37–78. ISI:A1996UE27500002. doi: 10.1086/419267 PubMed DOI

Cressler CE, McLeod DV, Rozins C, van den Hoogen J, Day T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology. 2016;143(7):915–30. doi: 10.1017/S003118201500092X WOS:000376781100011. PubMed DOI PMC

Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology. 1982;85(OCT):411–26. doi: 10.1017/s0031182000055360 WOS:A1982PP03200017. PubMed DOI

Visher E, Evensen C, Guth S, Lai E, Norfolk M, Rozins C, et al. The three Ts of virulence evolution during zoonotic emergence. P Roy Soc B-Biol Sci. 2021;288(1956). doi: 10.1098/rspb.2021.0900 WOS:000685237300005. PubMed DOI PMC

Fraser C, Hollingsworth TD, Chapman R, de Wolf F, Hanage WP. Variation in HIV-1 set-point viral load: Epidemiological analysis and an evolutionary hypothesis. Proc Natl Acad Sci U S A. 2007;104(44):17441–6. doi: 10.1073/pnas.0708559104 WOS:000250638400039. PubMed DOI PMC

Mackinnon MJ, Read AF. Virulence in malaria: an evolutionary viewpoint. Philos T Roy Soc B. 2004;359(1446):965–86. doi: 10.1098/rstb.2003.1414 WOS:000222444800008. 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 U S A. 2008;105(21):7489–94. doi: 10.1073/pnas.0710909105 WOS:000256378100029. PubMed DOI PMC

Jensen KH, Little T, Skorping A, Ebert D. Empirical support for optimal virulence in a castrating parasite. PLOS Biol. 2006;4(7):1265–9. doi: 10.1371/journal.pbio.0040197 WOS:000238974300018. PubMed DOI PMC

Stearns SC. The evolution of life histories. Oxford: Oxford University Press; 1992.

Mackinnon MJ, Read AF. Genetic relationships between parasite virulence and transmission in the rodent malaria PubMed DOI

Raberg L. Infection intensity and infectivity of the tick-borne pathogen PubMed

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, PubMed DOI PMC

Acevedo MA, Dillemuth FP, Flick AJ, Faldyn MJ, Elderd BD. Virulence-driven trade-offs in disease transmission: A meta-analysis. Evolution. 2019;73(4):636–47. doi: 10.1111/evo.13692 WOS:000467993300001. PubMed DOI

Bambini S, Piet J, Muzzi A, Keijzers W, Comandi S, De Tora L, et al. An analysis of the sequence variability of meningococcal fHbp, NadA and NHBA over a 50-year period in the Netherlands. PLOS ONE. 2013;8(5). doi: 10.1371/journal.pone.0065043 WOS:000319385300005. PubMed DOI PMC

Buckee CO, Gupta S, Kriz P, Maiden MCJ, Jolley KA. Long-term evolution of antigen repertoires among carried meningococci. P Roy Soc B-Biol Sci. 2010;277(1688):1635–41. doi: 10.1098/rspb.2009.2033 WOS:000276997700003. 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. Scientific Reports. 2017;7(1851). doi: 10.1038/s41598-017-01821-1 PubMed DOI PMC

Raberg L, Hagstrom A, Andersson M, Bartkova S, Scherman K, Strandh M, et al. Evolution of antigenic diversity in the tick-transmitted bacterium PubMed DOI

Weinberger DM, Trzcinski K, Lu Y-J, Bogaert D, Brandes A, Galagan J, et al. Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLOS Pathog. 2009;5(6). doi: 10.1371/journal.ppat.1000476 WOS:000268444500023. PubMed DOI PMC

Steere AC, Strle F, Wormser GP, Hu LDT, Branda JA, Hovius JR, et al. Lyme borreliosis. Nature Reviews Disease Primers. 2016;2. doi: 10.1038/nrdp.2016.90 WOS:000397870500001. PubMed DOI PMC

Stanek G, Reiter M. The expanding Lyme PubMed DOI

Kurtenbach K, Hanincova K, Tsao JI, Margos G, Fish D, Ogden NH. Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nat Rev Microbiol. 2006;4:660–9. doi: 10.1038/nrmicro1475 PubMed DOI

Piesman J, Gern L. Lyme borreliosis in Europe and North America. Parasitology. 2004;129:S191–S220. doi: 10.1017/s0031182003004694 WOS:000230134600013. PubMed DOI

Baum E, Hue F, Barbour AG. Experimental infections of the reservoir species PubMed DOI PMC

Genné D, Rossel M, Sarr A, Battilotti F, Rais O, Rego ROM, et al. Competition between strains of PubMed DOI PMC

Jacquet M, Durand J, Rais O, Voordouw MJ. Cross-reactive acquired immunity influences transmission success of the Lyme disease pathogen, PubMed DOI

Wang G, Ojaimi C, Iyer R, Saksenberg V, McClain SA, Wormser GP, et al. Impact of genotypic variation of PubMed 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 PubMed DOI PMC

Brisson D, Dykhuizen DE. PubMed PMC

Derdakova M, Dudioak V, Brei B, Brownstein JS, Schwartz I, Fish D. Interaction and transmission of two PubMed DOI PMC

Genné D, Sarr A, Gomez-Chamorro A, Durand J, Cayol C, Rais O, et al. Competition between strains of PubMed DOI PMC

Genné D, Sarr A, Rais O, Voordouw MJ. Competition between strains of PubMed DOI PMC

Hanincova K, Ogden NH, Diuk-Wasser M, Pappas CJ, Iyer R, Fish D, et al. Fitness variation of 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 PubMed DOI PMC

Rynkiewicz EC, Brown J, Tufts DM, Huang C-I, Kampen H, Bent SJ, et al. Closely-related PubMed DOI PMC

Tonetti N, Voordouw MJ, Durand J, Monnier S, Gern L. Genetic variation in transmission success of the Lyme borreliosis pathogen PubMed DOI

Voordouw MJ, Lachish S, Dolan MC. The Lyme disease pathogen has no effect on the survival of its rodent reservoir host. PLOS ONE. 2015;10(2). doi: 10.1371/journal.pone.0118265 WOS:000350322700110. PubMed DOI PMC

Schwanz LE, Voordouw MJ, Brisson D, Ostfeld RS. PubMed DOI

Barbour AG. Infection resistance and tolerance in PubMed DOI PMC

Moody KD, Terwilliger GA, Hansen GM, Barthold SW. Experimental PubMed

Zinck CB, Thampy PR, Rego ROM, Brisson D, Ogden NH, Voordouw M. PubMed DOI PMC

Tyler S, Tyson S, Dibernardo A, Drebot M, Feil EJ, Graham M, et al. Whole genome sequencing and phylogenetic analysis of strains of the agent of Lyme disease PubMed DOI PMC

Margos G, Tsao JI, Castillo-Ramirez S, Girard YA, Hamer SA, Hoen AG, et al. Two boundaries separate PubMed DOI PMC

Mechai S, Margos G, Feil EJ, Lindsay LR, Ogden NH. Complex population structure of PubMed DOI PMC

Ogden NH, Margos G, Aanensen DM, Drebot MA, Feil EJ, Hanincova K, et al. Investigation of genotypes of PubMed DOI PMC

Dolan MC, Piesman J, Schneider BS, Schriefer M, Brandt K, Zeidner NS. Comparison of disseminated and nondisseminated strains of PubMed DOI PMC

Ma Y, Seiler KP, Eichwald EJ, Weis JH, Teuscher C, Weis JJ. Distinct characteristics of resistance to PubMed PMC

Barthold SW, Persing DH, Armstrong AL, Peeples RA. Kinetics of PubMed PMC

Courtney JW, Kostelnik LM, Zeidner NS, Massung RF. Multiplex real-time PCR for detection of PubMed DOI PMC

Schrader C, Schielke A, Ellerbroek L, Johne R. PCR inhibitors—occurrence, properties and removal. J Appl Microbiol. 2012;113(5):1014–26. doi: 10.1111/j.1365-2672.2012.05384.x WOS:000310281100002. PubMed DOI

Sidstedt M, Hedman J, Romsos EL, Waitara L, Wadso L, Steffen CR, et al. Inhibition mechanisms of hemoglobin, immunoglobulin G, and whole blood in digital and real-time PCR. Anal Bioanal Chem. 2018;410(10):2569–83. doi: 10.1007/s00216-018-0931-z WOS:000427797800010. PubMed DOI PMC

Travinsky B, Bunikis J, Barbour AG. Geographic differences in genetic locus linkages for PubMed DOI PMC

Zinck CB, Raveendran Thampy P, Uhlemann E-M, Adam H, Wachter J, Suchan D, et al. Variation among strains of PubMed PMC

R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2021.

LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: Effects of host diversity and community composition on Lyme disease risk. Proc Natl Acad Sci U S A. 2003;100(2):567–71. doi: 10.1073/pnas.0233733100 PubMed DOI PMC

Cayol C, Giermek A, Gomez-Chamorro A, Hytönen J, Kallio ER, Mappes T, et al. PubMed DOI PMC

Bunikis J, Tsao J, Luke CJ, Luna MG, Fish D, Barbour AG. PubMed

Wright SD, Nielsen SW. Experimental infection of the white-footed mouse with PubMed

Randolph SE. Ticks are not insects: consequences of contrasting vector biology for transmission potential. Parasitol Today. 1998;14(5):186–92. doi: 10.1016/s0169-4758(98)01224-1 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 U S A. 2005;102(21):7624–8. doi: 10.1073/pnas.0500078102 ISI:000229417500041. PubMed DOI PMC

Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, et al. Experimental infection of north American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis. 2003;9(3):311–22. doi: 10.3201/eid0903.020628 WOS:000181507700005. PubMed DOI PMC

Lee WY, Moriarty TJ, Wong CHY, Zhou H, Strieter RM, van Rooijen N, et al. An intravascular immune response to PubMed DOI PMC

Tsao J. Reviewing molecular adaptations of Lyme borreliosis spirochetes in the context of reproductive fitness in natural transmission cycles. Vet Res (Paris). 2009;40(2). doi: 10.1051/vetres/2009019 PubMed DOI PMC

Shih CM, Chao LL, Yu CP. Chemotactic migration of the Lyme disease spirochete ( PubMed

Van Gundy TJ, Ullmann AJ, Brandt KS, Gilmore RD. A transwell assay method to evaluate PubMed DOI PMC

Ogden NH, Trudel L, Artsob H, Barker IK, Beauchamp G, Charron DF, et al. PubMed DOI

Barbour AG, Bunikis J, Travinsky B, Hoen AG, Diuk-Wasser MA, Fish D, et al. Niche partitioning of PubMed DOI PMC

Diuk-Wasser MA, Gatewood AG, Cortinas MR, Yaremych-Hamer S, Tsao J, Kitron U, et al. Spatiotemporal patterns of host-seeking Ixodes scapularis nymphs (Acari: Iodidae) in the United States. J Med Entomol. 2006;43(2):166–76. doi: 10.1603/0022-2585(2006)043[0166:Spohis]2.0.Co;2 WOS:000236184600006. PubMed DOI

Hanincova K, Kurtenbach K, Diuk-Wasser M, Brei B, Fish D. Epidemic spread of Lyme borreliosis, Northeastern United States. Emerg Infect Dis. 2006;12(4):604–11. doi: 10.3201/eid1204.051016 PubMed DOI PMC

Mechai S, Margos G, Feil EJ, Barairo N, Lindsay LR, Michel P, et al. Evidence for host-genotype associations of PubMed DOI PMC

Vuong HB, Canham CD, Fonseca DM, Brisson D, Morin PJ, Smouse PE, et al. Occurrence and transmission efficiencies of PubMed DOI PMC

Brunner J, LoGiudice K, Ostfeld R. Estimating reservoir competence of PubMed

Mather TN, Wilson ML, Moore SI, Ribeiro JMC, Spielman A. Comparing the relative potential of rodents as reservoirs of the Lyme disease spirochete ( PubMed

Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F. Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLOS Biol. 2006;4(6):1058–68. doi: 10.1371/journal.pbio.0040145 PubMed DOI PMC

Ostfeld RS, Schauber EM, Canham CD, Keesing F, Jones CG, Wolff JO. Effects of acorn production and mouse abundance on abundance and Borrelia burgdorferi infection prevalence of nymphal PubMed DOI

Jones CG, Ostfeld RS, Richard MP, Schauber EM, Wolff JO. Chain reactions linking acorns to gypsy moth outbreaks and Lyme disease risk. Science. 1998;279(5353):1023–6. doi: 10.1126/science.279.5353.1023 WOS:000072006400045. PubMed DOI

Adams B, Walter KS, Diuk-Wasser MA. Host Specialisation, Immune Cross-Reaction and the Composition of Communities of Co-circulating Borrelia Strains. Bull Math Biol. 2021;83(6). doi: 10.1007/s11538-021-00896-2 WOS:000646565000001. PubMed DOI PMC

Springer MS, Murphy WJ, Eizirik E, O’Brien SJ. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proc Natl Acad Sci U S A. 2003;100(3):1056–61. doi: 10.1073/pnas.0334222100 WOS:000180838100053. PubMed DOI PMC

Swanson KI, Norris DE. Presence of multiple variants of PubMed DOI PMC

Andersson M, Scherman K, Raberg L. Multiple-strain infections of PubMed

Strandh M, Raberg L. Within-host competition between PubMed DOI PMC

Pérez D, Kneubühler Y, Rais O, Jouda F, Gern L. PubMed

Bourgeois B, Koloski C, Foley-Eby A, Zinck CB, Hurry G, Boulanger N, et al. Clobetasol increases the abundance of PubMed DOI

Klein SL, Flanagan KL. Sex differences in immune responses. Nat Rev Immunol. 2016;16(10):626–38. doi: 10.1038/nri.2016.90 WOS:000384551900010. PubMed DOI

Trigunaite A, Dimo J, Jorgensen TN. Suppressive effects of androgens on the immune system. Cell Immunol. 2015;294(2):87–94. doi: 10.1016/j.cellimm.2015.02.004 WOS:000351480800006. PubMed DOI

vom Steeg LG, Klein SL. SeXX Matters in Infectious Disease Pathogenesis. PLOS Pathog. 2016;12(2). doi: 10.1371/journal.ppat.1005374 WOS:000378152900005. PubMed DOI PMC

Tschirren B, Andersson M, Scherman K, Westerdahl H, Mittl PRE, Raberg L. Polymorphisms at the innate immune receptor TLR2 are associated with PubMed PMC

Zawada SG, von Fricken ME, Weppelmann TA, Sikaroodi M, Gillevet PM. Optimization of tissue sampling for PubMed DOI PMC

Hamer SA, Hickling GJ, Sidge JL, Walker ED, Tsao JI. Synchronous phenology of juvenile Ixodes scapularis, vertebrate host relationships, and associated patterns of PubMed DOI

Devevey G, Brisson D. The effect of spatial heterogeneity on the aggregation of ticks on white-footed mice. Parasitology. 2012;139:915–25. PubMed PMC

Ostfeld RS, Brisson D, Oggenfuss K, Devine J, Levy MZ, Keesing F. Effects of a zoonotic pathogen, PubMed DOI PMC

Perkins SE, Cattadori IM, Tagliapietra V, Rizzoli AP, Hudson PJ. Empirical evidence for key hosts in persistence of a tick-borne disease. Int J Parasitol. 2003;33:909–17. doi: 10.1016/s0020-7519(03)00128-0 PubMed DOI

Bouchard C, Beauchamp G, Nguon S, Trudel L, Milord F, Lindsay LR, et al. Associations between PubMed DOI

Hofmeister EK, Ellis BA, Glass GE, Childs JE. Longitudinal study of infection with PubMed

Graves C, Ros VID, Stevenson B, Sniegowski P, Brisson D. Natural selection promotes antigenic evolvability. PLOS Pathog. 2013;9(11):e1003766. doi: 10.1371/journal.ppat.1003766 PubMed DOI PMC

Donahue JG, Piesman J, Spielman A. Reservoir competence of white-footed mice for Lyme disease spirochetes. Am J Trop Med Hyg. 1987;36:92–6. doi: 10.4269/ajtmh.1987.36.92 PubMed DOI

Richter D, Klug B, Spielman A, Matuschka FR. Adaptation of diverse Lyme disease spirochetes in a natural rodent reservoir host. Infect Immun. 2004;72(4):2442–4. doi: 10.1128/IAI.72.4.2442-2444.2004 WOS:000220481600076. PubMed DOI PMC

Gatewood AG, Liebman KA, Vourc’h G, Bunikis J, Hamer SA, Cortinas R, et al. Climate and tick seasonality are predictors of PubMed DOI PMC

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