Restriction of Genetic Diversity during Infection of the Vector Midgut
Co-infection, the presence of multiple genotypes of the same pathogen species within an infected individual, is common. Genotype diversity, defined as the number of unique genotypes, and the interaction between genotypes, can strongly influence virulence and pathogen transmission. Understanding how genotypic diversity affects transmission of pathogens that naturally cycle among disparate hosts, such as vector-borne pathogens, is especially important as the capacity of the host and vector to sustain genotypic diversity may differ. To address this, we exposed Dermacentor andersoni ticks, via infected mice, to variably diverse populations of Francisella novicida genotypes. Interestingly, we found that ticks served as greater ecological filters for genotypic diversity compared to mice. This loss in genotypic diversity was due to both stochastic and selective forces. Based on these data and a model, we determined that high numbers of ticks in an environment support high genotypic diversity, while genotypic diversity will be lost rapidly in environments with low tick numbers. Together, these results provide evidence that vector population dynamics, vector-to-host ratios, and competition among pathogen genotypes play critical roles in the maintenance of pathogen genotypic diversity.
Vyšlo v časopise:
Restriction of Genetic Diversity during Infection of the Vector Midgut. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004499
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1004499
Souhrn
Co-infection, the presence of multiple genotypes of the same pathogen species within an infected individual, is common. Genotype diversity, defined as the number of unique genotypes, and the interaction between genotypes, can strongly influence virulence and pathogen transmission. Understanding how genotypic diversity affects transmission of pathogens that naturally cycle among disparate hosts, such as vector-borne pathogens, is especially important as the capacity of the host and vector to sustain genotypic diversity may differ. To address this, we exposed Dermacentor andersoni ticks, via infected mice, to variably diverse populations of Francisella novicida genotypes. Interestingly, we found that ticks served as greater ecological filters for genotypic diversity compared to mice. This loss in genotypic diversity was due to both stochastic and selective forces. Based on these data and a model, we determined that high numbers of ticks in an environment support high genotypic diversity, while genotypic diversity will be lost rapidly in environments with low tick numbers. Together, these results provide evidence that vector population dynamics, vector-to-host ratios, and competition among pathogen genotypes play critical roles in the maintenance of pathogen genotypic diversity.
Zdroje
1. ReadAF, TaylorLH (2001) The ecology of genetically diverse infections. Science 292: 1099–1102.
2. LadburyGA, StuenS, ThomasR, BownKJ, WoldehiwetZ, et al. (2008) Dynamic transmission of numerous Anaplasma phagocytophilum genotypes among lambs in an infected sheep flock in an area of anaplasmosis endemicity. Journal of Clinical Microbiology 46: 1686–1691.
3. MideoN (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25: 261–268.
4. BalmerO, TannerM (2011) Prevalence and implications of multiple-strain infections. The Lancet Infectious Diseases 11: 868–878.
5. TsaoK, BentSJ, FishD (2013) Identification of Borrelia burgdorferi ospC genotypes in host tissue and feeding ticks by terminal restriction fragment length polymorphisms. Applied and Environmental Microbiology 79: 958–964.
6. AndersonTJ, HauboldB, WilliamsJT, Estrada-FrancoJG, RichardsonL, et al. (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution 17: 1467–1482.
7. ColognaR, ArmstrongPM, Rico-HesseR (2005) Selection for virulent dengue viruses occurs in humans and mosquitoes. J Virol 79: 853–859.
8. SmithT, BeckHP, KituaA, MwankusyeS, FelgerI, et al. (1999) Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Transactions of the Royal Society of Tropical Medicine and Hygiene 93 Suppl 1: 15–20.
9. EbelGD, CarricaburuJ, YoungD, BernardKA, KramerLD (2004) Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg 71: 493–500.
10. DayKP, KoellaJC, NeeS, GuptaS, ReadAF (1992) Population genetics and dynamics of Plasmodium falciparum: an ecological view. Parasitology 104 Suppl: S35–52.
11. SwansonKI, NorrisDE (2008) Presence of multiple variants of Borrelia burgdorferi in the natural reservoir Peromyscus leucopus throughout a transmission season. Vector Borne and Zoonotic Diseases 8: 397–405.
12. OberleM, BalmerO, BrunR, RoditiI (2010) Bottlenecks and the maintenance of minor genotypes during the life cycle of Trypanosoma brucei. PLoS Pathogens 6: e1001023.
13. ManskeM, MiottoO, CampinoS, AuburnS, Almagro-GarciaJ, et al. (2012) Analysis of Plasmodium falciparum diversity in natural infections by deep sequencing. Nature 487: 375–379.
14. RomanoCM, LauckM, SalvadorFS, LimaCR, Villas-BoasLS, et al. (2013) Inter- and intra-host viral diversity in a large seasonal DENV2 outbreak. PloS One 8: e70318.
15. AnderssonM, SchermanK, RabergL (2013) Multiple-strain infections of Borrelia afzelii: a role for within-host interactions in the maintenance of antigenic diversity? The American Naturalist 181: 545–554.
16. MannBR, McMullenAR, GuzmanH, TeshRB, BarrettAD (2013) Dynamic transmission of West Nile virus across the United States-Mexican border. Virology 436: 75–80.
17. RudenkoN, GolovchenkoM, BelfioreNM, GrubhofferL, OliverJHJr (2014) Divergence of Borrelia burgdorferi sensu lato spirochetes could be driven by the host: diversity of Borrelia strains isolated from ticks feeding on a single bird. Parasites & Vectors 7: 4.
18. AndersonRM (1999) The pandemic of antibiotic resistance. Nature Medicine 5: 147–149.
19. PolicastroPF, RaffelSJ, SchwanTG (2013) Borrelia hermsii acquisition order in superinfected ticks determines transmission efficiency. Infection and Immunity 81: 2899–2908.
20. WargoAR, de RoodeJC, HuijbenS, DrewDR, ReadAF (2007) Transmission stage investment of malaria parasites in response to in-host competition. Proceedings Biological Sciences/The Royal Society 274: 2629–2638.
21. BellAS, de RoodeJC, SimD, ReadAF (2006) Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution; International Journal of Organic Evolution 60: 1358–1371.
22. TroyEB, LinT, GaoL, LazinskiDW, CamilliA, et al. (2013) Understanding barriers to Borrelia burgdorferi dissemination during infection using massively parallel sequencing. Infection and Immunity 81: 2347–2357.
23. GoethertHK, ShaniI, TelfordSR3rd (2004) Genotypic diversity of Francisella tularensis infecting Dermacentor variabilis ticks on Martha's Vineyard, Massachusetts. Journal of Clinical Microbiology 42: 4968–4973.
24. GoethertHK, TelfordSR3rd (2009) Nonrandom distribution of vector ticks (Dermacentor variabilis) infected by Francisella tularensis. PLoS Pathogens 5: e1000319.
25. GoethertHK, TelfordSR3rd (2011) Differential mortality of dog tick vectors due to infection by diverse Francisella tularensis tularensis genotypes. Vector Borne and Zoonotic Diseases 11: 1263–1268.
26. ChampionMD, ZengQ, NixEB, NanoFE, KeimP, et al. (2009) Comparative genomic characterization of Francisella tularensis strains belonging to low and high virulence subspecies. PLoS Pathogens 5: e1000459.
27. BerradaZL, TelfordSR3rd (2010) Diversity of Francisella species in environmental samples from Martha's Vineyard, Massachusetts. Microbial Ecology 59: 277–283.
28. JohanssonA, GöranssonI, LarssonP, SjöstedtA (2001) Extensive allelic variation among Francisella tularensis strains in a short-sequence tandem repeat region. Journal of Clinical Microbiology 39: 3140–3146.
29. ReifKE, PalmerGH, UetiMW, ScolesGA, MargolisJJ, et al. (2011) Dermacentor andersoni transmission of Francisella tularensis subsp. novicida reflects bacterial colonization, dissemination, and replication coordinated with tick feeding. Infection and Immunity 79: 4941–4946.
30. NarasimhanS, RajeevanN, LiuL, ZhaoYO, HeisigJ, et al. (2014) Gut Microbiota of the Tick Vector Ixodes scapularis Modulate Colonization of the Lyme Disease Spirochete. Cell Host & Microbe 15: 58–71.
31. UetiMW, ReaganJOJr, KnowlesDPJr, ScolesGA, ShkapV, et al. (2007) Identification of midgut and salivary glands as specific and distinct barriers to efficient tick-borne transmission of Anaplasma marginale. Infection and Immunity 75: 2959–2964.
32. TaylorLH, WallikerD, ReadAF (1997) Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 115 (Pt 2) 121–132.
33. TaylorLH, WallikerD, ReadAF (1997) Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proceedings Biological Sciences/The Royal Society 264: 927–935.
34. de RoodeJC, HelinskiME, AnwarMA, ReadAF (2005) Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. The American Naturalist 166: 531–542.
35. de RoodeJC, PansiniR, CheesmanSJ, HelinskiME, HuijbenS, et al. (2005) Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences of the United States of America 102: 7624–7628.
36. BrackneyDE, PeskoKN, BrownIK, DeardorffER, KawatachiJ, et al. (2011) West Nile virus genetic diversity is maintained during transmission by Culex pipiens quinquefasciatus mosquitoes. PLoS One 6: e24466.
37. CiotaAT, EhrbarDJ, Van SlykeGA, PayneAF, WillseyGG, et al. (2012) Quantification of intrahost bottlenecks of West Nile virus in Culex pipiens mosquitoes using an artificial mutant swarm. Infection, Genetics and Evolution 12: 557–564.
38. EswarappaSM, EstrelaS, BrownSP (2012) Within-host dynamics of multi-species infections: facilitation, competition and virulence. PloS One 7: e38730.
39. JosephSB, SwanstromR (2014) HIV/AIDS. A fitness bottleneck in HIV-1 transmission. Science 345: 136–137.
40. CarlsonJM, SchaeferM, MonacoDC, BatorskyR, ClaiborneDT, et al. (2014) HIV transmission. Selection bias at the heterosexual HIV-1 transmission bottleneck. Science 345: 1254031.
41. RegoRO, BestorA, StefkaJ, RosaPA (2014) Population bottlenecks during the infectious cycle of the Lyme disease spirochete Borrelia burgdorferi. PloS One 9: e101009.
42. JerzakGV, BrownI, ShiPY, KramerLD, EbelGD (2008) Genetic diversity and purifying selection in West Nile virus populations are maintained during host switching. Virology 374: 256–260.
43. ForresterNL, GuerboisM, SeymourRL, SprattH, WeaverSC (2012) Vector-borne transmission imposes a severe bottleneck on an RNA virus population. PLoS Pathogens 8: e1002897.
44. DarkMJ, HerndonDR, KappmeyerLS, GonzalesMP, NordeenE, et al. (2009) Conservation in the face of diversity: multistrain analysis of an intracellular bacterium. BMC Genomics 10: 16.
45. HerndonDR, UetiMW, ReifKE, NohSM, BraytonKA, et al. (2013) Identification of multilocus genetic heterogeneity in Anaplasma marginale subsp. central and its restriction following tick-borne transmission. Infection and Immunity 81: 1852–1858.
46. RodriquezJL, PalmerGH, KnowlesDPJr, BraytonKA (2005) Distinctly different msp2 pseudogene repertoires in Anaplasma marginale strains that are capable of superinfection. Gene 361: 127–132.
47. TettelinH, MasignaniV, CieslewiczMJ, DonatiC, MediniD, et al. (2005) Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proceedings of the National Academy of Sciences of the United States of America 102: 13950–13955.
48. FaburayB, JongejanF, TaoufikA, CeesayA, GeysenD (2008) Genetic diversity of Ehrlichia ruminantium in Amblyomma variegatum ticks and small ruminants in The Gambia determined by restriction fragment profile analysis. Veterinary Microbiology 126: 189–199.
49. ZnazenA, KhroufF, ElleuchN, LahianiD, MarrekchiC, et al. (2013) Multispacer typing of Rickettsia isolates from humans and ticks in Tunisia revealing new genotypes. Parasites & Vectors 6: 367.
50. FutseJE, BraytonKA, DarkMJ, KnowlesDPJr, PalmerGH (2008) Superinfection as a driver of genomic diversification in antigenically variant pathogens. Proceedings of the National Academy of Sciences of the United States of America 105: 2123–2127.
51. GallagherLA, RamageE, JacobsMA, KaulR, BrittnacherM, et al. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proceedings of the National Academy of Sciences of the United States of America 104: 1009–1014.
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
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