Host Adaptation Is Contingent upon the Infection Route Taken by Pathogens

English version České info

Evolution of pathogen virulence is affected by the route of infection. Also, alternate infection routes trigger different physiological responses on hosts, impinging on host adaptation and on its interaction with pathogens. Yet, how route of infection may shape adaptation to pathogens has not received much attention at the experimental level. We addressed this question through the experimental evolution of an outbred Drosophila melanogaster population infected by two different routes (oral and systemic) with Pseudomonas entomophila. The two selection regimes led to markedly different evolutionary trajectories. Adaptation to infection through one route did not protect from infection through the alternate route, indicating distinct genetic bases. Finally, relatively to the control population, evolved flies were not more resistant to bacteria other than Pseudomonas and showed higher susceptibility to viral infections. These specificities and trade-offs may contribute to the maintenance of genetic variation for resistance in natural populations. Our data shows that the infection route affects host adaptation and thus, must be considered in studies of host-pathogen interaction.

Vyšlo v časopise: Host Adaptation Is Contingent upon the Infection Route Taken by Pathogens. PLoS Pathog 9(9): e32767. doi:10.1371/journal.ppat.1003601
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003601

Souhrn

Zdroje

1. AndersonRM, MayRM (1982) Coevolution of hosts and parasites. Parasitology 85(Pt 2): 411–426.

2. EwaldPW (1995) The evolution of virulence: a unifying link between parasitology and ecology. J Parasitol 81: 659–669.

3. LipstichM, SillerS, NorwakMA (1996) The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50: 1729–1741.

4. EbertD, ManginKL (1997) The influence of host demography on the evolution of virulence of a microsporidian gut parasite. Evolution 51: 1828–1837.

5. MessengerSL, MolineuxIJ, BullJJ (1999) Virulence evolution in a virus obeys a trade-off. Proc Biol Sci 266: 397–404.

6. StewartAD, LogsdonJMJ, KelleySE (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59: 730–739.

7. MagalonH, NideletT, MartinG, KaltzO (2010) Host growth conditions influence experimental evolution of life history and virulence of a parasite with vertical and horizontal transmission. Evolution 64: 2126–2138.

8. EwaldPW (1983) Host–parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 14: 465–485.

9. DayT (2001) Parasite transmission modes and the evolution of virulence. Evol Int J Org Evol 55: 2389–2400.

10. DayT (2002) The evolution of virulence in vector-borne and directly transmitted parasites. Theor Popul Biol 62: 199–213.

11. LeggettHC, CornwallisCK, WestSA (2012) Mechanisms of pathogenesis, infective dose and virulence in human parasites. Plos Pathog 8: e1002512 doi:10.1371/journal.ppat.1002512

12. VizosoDB, EbertD (2005) Phenotypic plasticity of host-parasite interactions in response to the route of infection. J Evol Biol 18: 911–921.

13. Ben-AmiF, RigaudT, EbertD (2011) The expression of virulence during double infections by different parasites with conflicting host exploitation and transmission strategies. J Evol Biol 24: 1307–1316.

14. Schmid-Hempel P (2011) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. New York: Oxford University Press.

15. Schmid-HempelP, EbertD (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18: 27–32.

16. BoughtonRK, JoopG, ArmitageSAO (2011) Outdoor Immunology: methodological considerations for ecologists. Funct Ecol 25: 81–100.

17. RabergL, SimD, ReadAF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318: 812–814.

18. SchneiderDS, AyresJS (2008) Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nat Rev Immunol 8: 889–895.

19. MedzhitovR, SchneiderDS, SoaresMP (2012) Disease tolerance as a defense strategy. Science 335: 936–941.

20. LhocineN, RibeiroPS, BuchonN, WepfA, WilsonR, et al. (2008) PIMS modulates immune tolerance by negatively regulating Drosophila innate immune signaling. Cell Host Microbe 4: 147–158.

21. AyresJS, SchneiderDS (2008) A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. Plos Biol 6: 2764–2773.

22. NeyenC, PoidevinM, RousselA, LemaitreB (2012) Tissue- and ligand-specific sensing of gram-negative infection in drosophila by PGRP-LC isoforms and PGRP-LE. J Immunol 189: 1886–1897.

23. LemaitreB, HoffmannJ (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25: 697–743 doi:10.1146/annurev.immunol.25.022106.141615

24. Shirasu-HizaMM, DionneMS, PhamLN, AyresJS, SchneiderDS (2007) Interactions between circadian rhythm and immunity in Drosophila melanogaster. Curr Biol 17: R353–5.

25. KounatidisI, LigoxygakisP (2012) Drosophila as a model system to unravel the layers of innate immunity to infection. Open Biol 2: 120075.

26. BomanHG, NilssonI, RasmusonB (1972) Inducible antibacterial defence system in Drosophila. Nature 237: 232–235.

27. LemaitreB, NicolasE, MichautL, ReichhartJM, HoffmannJA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86: 973–983.

28. IrvingP, TroxlerL, HeuerTS, BelvinM, KopczynskiC, et al. (2001) A genome-wide analysis of immune responses in Drosophila. Proc Natl Acad Sci U S 98: 15119–15124.

29. De GregorioE, SpellmanPT, RubinGM, LemaitreB (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S 98: 12590–12595.

30. NehmeNT, LiegeoisS, KeleB, GiammarinaroP, PradelE, et al. (2007) A model of bacterial intestinal infections in Drosophila melanogaster. Plos Pathog 3: e173.

31. BassetA, KhushRS, BraunA, GardanL, BoccardF, et al. (2000) The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proc Natl Acad Sci U S 97: 3376–3381.

32. VodovarN, VinalsM, LiehlP, BassetA, DegrouardJ, et al. (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proc Natl Acad Sci U S 102: 11414–11419.

33. BuchonN, BroderickNA, PoidevinM, PradervandS, LemaitreB (2009) Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation. Cell Host Microbe 5: 200–211.

34. LimmerS, HallerS, DrenkardE, LeeJ, YuS, et al. (2011) Pseudomonas aeruginosa RhlR is required to neutralize the cellular immune response in a Drosophila melanogaster oral infection model. Proc Natl Acad Sci U S 108: 17378–17383.

35. Vallet-GelyI, LemaitreB, BoccardF (2008) Bacterial strategies to overcome insect defences. Nat Rev Microbiol 6: 302–313 doi:10.1038/nrmicro1870

36. TeixeiraL (2012) Whole-genome expression profile analysis of Drosophila melanogaster immune responses. Brief Funct Genomics 11: 375–386.

37. HaEM, OhCT, BaeYS, LeeWJ (2005) A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847–850.

38. LiehlP, BlightM, VodovarN, BoccardF, LemaitreB (2006) Prevalence of local immune response against oral infection in a Drosophila/Pseudomonas infection model. Plos Pathog 2: e56.

39. RyuJH, HaEM, OhCT, SeolJH, BreyPT, et al. (2006) An essential complementary role of NF-kappaB pathway to microbicidal oxidants in Drosophila gut immunity. Embo J 25: 3693–3701.

40. KuraishiT, BinggeliO, OpotaO, BuchonN, LemaitreB (2011) Genetic evidence for a protective role of the peritrophic matrix against intestinal bacterial infection in Drosophila melanogaster. Proc Natl Acad Sci U S 108: 15966–15971.

41. BuchonN, BroderickNA, ChakrabartiS, LemaitreB (2009) Invasive and indigenous microbiota impact intestinal stem cell activity through multiple pathways in Drosophila. Genes Dev 23: 2333–2344.

42. DionneMS, SchneiderDS (2008) Models of infectious diseases in the fruit fly Drosophila melanogaster. Dis Model Mech 1: 43–49.

43. KaweckiTJ, LenskiRE, EbertD, HollisB, OlivieriI, et al. (2012) Experimental evolution. Trends Ecol Evol 27: 547–560.

44. KraaijeveldAR, GodfrayHC (1997) Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389: 278–280.

45. KraaijeveldAR, GodfrayHC (2008) Selection for resistance to a fungal pathogen in Drosophila melanogaster. Hered Edinb 100: 400–406.

46. YeYH, ChenowethSF, McGrawEA (2009) Effective but costly, evolved mechanisms of defense against a virulent opportunistic pathogen in Drosophila melanogaster. Plos Pathog 5: e1000385.

47. WolfleS, TrienensM, RohlfsM (2009) Experimental evolution of resistance against a competing fungus in Drosophila melanogaster. Oecologia 161: 781–790.

48. WertheimB, KraaijeveldAR, HopkinsMG, Walther BoerM, GodfrayHC (2011) Functional genomics of the evolution of increased resistance to parasitism in Drosophila. Mol Ecol 20: 932–949.

49. DavisMM, EngstromY (2012) Immune response in the barrier epithelia: lessons from the fruit fly Drosophila melanogaster. J Innate Immun 4: 273–283.

50. CharrouxB, RoyetJ (2009) Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response. Proc Natl Acad Sci U S 106: 9797–9802.

51. LazzaroBP, ClarkAG (2003) Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster. Mol Biol Evol 20: 914–923.

52. RoyBA, KirchnerJW (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54: 51–63.

53. ChakrabartiS, LiehlP, BuchonN, LemaitreB (2012) Infection-induced host translational blockage inhibits immune responses and epithelial renewal in the Drosophila gut. Cell Host Microbe 12: 60–70.

54. ChambersMC, LightfieldKL, SchneiderDS (2012) How the fly balances its ability to combat different pathogens. Plos Pathog 8: e1002970 doi:10.1371/journal.ppat.1002970

55. ApidianakisY, MindrinosMN, XiaoW, LauGW, BaldiniRL, et al. (2005) Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc Natl Acad Sci U S 102: 2573–2578.

56. SchlenkeTA, MoralesJ, GovindS, ClarkAG (2007) Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. Plos Pathog 3: 1486–1501.

57. Hill-BurnsEM, ClarkAG (2009) X-linked variation in immune response in Drosophila melanogaster. Genetics 183: 1477–1491.

58. ZbindenM, HaagCR, EbertD (2008) Experimental evolution of field populations of Daphnia magna in response to parasite treatment. J Evol Biol 21: 1068–1078.

59. KraaijeveldAR, LayenSJ, FutermanPH, GodfrayHC (2012) Lack of Phenotypic and Evolutionary Cross-Resistance against Parasitoids and Pathogens in Drosophila melanogaster. Plos One 7: e53002.

60. HodgesTK, LaskowskiKL, SquadritoGL, De LucaM, LeipsJ (2013) Defense traits of larval Drosophila melanogaster exhibit genetically based trade-offs against different species of parasitoids. Evol Int J Org Evol 67: 749–760 doi:10.1111/j.1558-5646.2012.01813.x

61. TeixeiraL, FerreiraA, AshburnerM (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. Plos Biol 6: e2 doi:[]08-PLBI-RA-3425 [pii] 10.1371/journal.pbio.1000002

62. Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. New York: Springer.