Diverse Host-Seeking Behaviors of Skin-Penetrating Nematodes

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Parasitic worms are a significant public health problem. Skin-penetrating worms such as hookworms and the human threadworm Strongyloides stercoralis dwell in the soil before infecting their host. However, how they locate and identify appropriate hosts is not understood. Here we investigated the host-seeking behavior of Str. stercoralis. We found that Str. stercoralis moves quickly and actively searches for hosts to infect. We also found that Str. stercoralis is attracted to human skin and sweat odorants, including many that also attract mosquitoes. We then compared olfactory behavior across parasitic worm species and found that parasites with similar hosts respond similarly to odorants even when they are not closely related, suggesting parasitic worms use olfactory cues to select hosts. A better understanding of host seeking in skin-penetrating worms may lead to novel control strategies.

Vyšlo v časopise: Diverse Host-Seeking Behaviors of Skin-Penetrating Nematodes. PLoS Pathog 10(8): e32767. doi:10.1371/journal.ppat.1004305
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004305

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Zdroje

1. SchaferTW, SkopicA (2006) Parasites of the small intestine. Curr Gastroenterol Rep 8: 312–320.

2. ScharF, TrostdorfU, GiardinaF, KhieuV, MuthS, et al. (2013) Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis 7: e2288.

3. KhieuV, ScharF, MartiH, SayasoneS, DuongS, et al. (2013) Diagnosis, treatment and risk factors of Strongyloides stercoralis in schoolchildren in Cambodia. PLoS Negl Trop Dis 7: e2035.

4. HotezP, HawdonJ, SchadGA (1993) Hookworm larval infectivity, arrest and amphiparatenesis: the Caenorhabditis elegans Daf-c paradigm. Parasitol Today 9: 23–26.

5. SchadGA, AikensLM, SmithG (1989) Strongyloides stercoralis: is there a canonical migratory route through the host? J Parasitol 75: 740–749.

6. YamadaM, MatsudaS, NakazawaM, ArizonoN (1991) Species-specific differences in heterogenic development of serially transferred free-living generations of Strongyloides planiceps and Strongyloides stercoralis. J Parasitol 77: 592–594.

7. AshtonFT, LiJ, SchadGA (1999) Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. Vet Parasitol 84: 297–316.

8. BhopaleVM, KupprionEK, AshtonFT, BostonR, SchadGA (2001) Ancylostoma caninum: the finger cell neurons mediate thermotactic behavior by infective larvae of the dog hookworm. Exp Parasitol 97: 70–76.

9. ChaissonKE, HallemEA (2012) Chemosensory behaviors of parasites. Trends Parasitol 28: 427–436.

10. ForbesWM, AshtonFT, BostonR, ZhuX, SchadGA (2004) Chemoattraction and chemorepulsion of Strongyloides stercoralis infective larvae on a sodium chloride gradient is mediated by amphidial neuron pairs ASE and ASH, respectively. Vet Parasitol 120: 189–198.

11. LopezPM, BostonR, AshtonFT, SchadGA (2000) The neurons of class ALD mediate thermotaxis in the parasitic nematode, Strongyloides stercoralis. Int J Parasitol 30: 1115–1121.

12. KogaM, NuamtanongS, DekumyoyP, YoonuanT, MaipanichW, et al. (2005) Host-finding behavior of Strongyloides stercoralis infective larvae to sodium cation, human serum, and sweat. Southeast Asian J Trop Med Public Health 36: 93–98.

13. KogaM, TadaI (2000) Strongyloides ratti: chemotactic responses of third-stage larvae to selected serum proteins and albumins. J Helminthol 74: 247–252.

14. SaferD, BrenesM, DunipaceS, SchadG (2007) Urocanic acid is a major chemoattractant for the skin-penetrating parasitic nematode Strongyloides stercoralis. Proc Natl Acad Sci USA 104: 1627–1630.

15. DownesMJ, GriffinCT (1996) Dispersal behavior and transmission strategies of the entomopathogenic nematodes Heterorhabditis and Steinernema. Biocontrol Sci Techn 6: 347–356.

16. RamotD, JohnsonBE, BerryTL, CarnellL, GoodmanMB (2008) The parallel worm tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS ONE 3: e2208.

17. LiuY, WangL, LiuJ, DiY (2013) A study of human skin and surface temperatures in stable and unstable thermal environments. J Therm Biol 38: 440–448.

18. LeeH, ChoiMK, LeeD, KimHS, HwangH, et al. (2012) Nictation, a dispersal behavior of the nematode Caenorhabditis elegans, is regulated by IL2 neurons. Nat Neurosci 15: 107–112.

19. GriffinCT (2012) Perspectives on the behavior of entomopathogenic nematodes from dispersal to reproduction: traits contributing to nematode fitness and biocontrol efficacy. J Nematol 44: 177–184.

20. WilsonMJ, EhlersR-U, GlazerI (2012) Entomopathogenic nematode foraging strategies – is Steinernema carpocapsae really an ambush forager? Nematol 14: 389–394.

21. HallemEA, DillmanAR, HongAV, ZhangY, YanoJM, et al. (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21: 377–383.

22. DillmanAR, GuillerminML, LeeJH, KimB, SternbergPW, et al. (2012) Olfaction shapes host-parasite interactions in parasitic nematodes. Proc Natl Acad Sci USA 109: E2324–2333.

23. LaznikZ, TrdanS (2013) An investigation on the chemotactic responses of different entomopathogenic nematode strains to mechanically damaged maize root volatile compounds. Exp Parasitol 134: 349–355.

24. AliJG, AlbornHT, StelinskiLL (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. J Chem Ecol 36: 361–368.

25. AliJG, AlbornHT, Campos-HerreraR, KaplanF, DuncanLW, et al. (2012) Subterranean, herbivore-induced plant volatile increases biological control activity of multiple beneficial nematode species in distinct habitats. PLoS ONE 7: e38146.

26. AliJG, AlbornHT, StelinskiLL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant-parasitic nematodes. J Ecol 99: 26–35.

27. HiltpoldI, BaroniM, ToepferS, KuhlmannU, TurlingsTC (2010) Selection of entomopathogenic nematodes for enhanced responsiveness to a volatile root signal helps to control a major root pest. J Exp Biol 213: 2417–2423.

28. KollnerTG, HeldM, LenkC, HiltpoldI, TurlingsTC, et al. (2008) A maize (E)-β-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20: 482–494.

29. RasmannS, KollnerTG, DegenhardtJ, HiltpoldI, ToepferS, et al. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732–737.

30. RasmannS, AliJG, HelderJ, van der PuttenWH (2012) Ecology and evolution of soil nematode chemotaxis. J Chem Ecol 38: 615–628.

31. QiuYT, SmallegangeRC, van LoonJJ, TakkenW (2011) Behavioural responses of Anopheles gambiae sensu stricto to components of human breath, sweat and urine depend on mixture composition and concentration. Med Vet Entomol 25: 247–255.

32. AlkalayI, SuetsuguS, ConstantineH, SteinM (1971) Carbon dioxide elimination across human skin. Am J Physiol 220: 1434–1436.

33. TurlingsTC, HiltpoldI, RasmannS (2012) The importance of root-produced volatiles as foraging cues for entomopathogenic nematodes. Plant Soil 358: 51–60.

34. ZajacAM (2006) Gastrointestinal nematodes of small ruminants: life cycle, anthelmintics, and diagnosis. Vet Clin North Am Food Anim Pract 22: 529–541.

35. PleilJD, LindstromAB (1995) Measurement of volatile organic compounds in exhaled breath as collected in evacuated electropolished canisters. J Chromatogr B Biomed Appl 665: 271–279.

36. ManssonHL (2008) Fatty acids in bovine milk fat. Food Nutr Res 52: 10.

37. PovoloM, PelizzolaV, RaveraD, ContariniG (2009) Significance of the nonvolatile minor compounds of the neutral lipid fraction as markers of the origin of dairy products. J Agric Food Chem 57: 7387–7394.

38. HaenleinGFW (2004) Goat milk in human nutrition. Small Ruminant Res 51: 155–163.

39. Viney ME, Lok JB (2007) Strongyloides spp. In WormBook, www.WormBook.org.

40. MooreJG, JessopLD, OsborneDN (1987) Gas-chromatographic and mass-spectrometric analysis of the odor of human feces. Gastroenterology 93: 1321–1329.

41. DiawaraA, SchwenkenbecherJM, KaplanRM, PrichardRK (2013) Molecular and biological diagnostic tests for monitoring benzimidazole resistance in human soil-transmitted helminths. Am J Trop Med Hyg 88: 1052–1061.

42. BilgramiAL, GaugerR, Shapiro-IlanDI, AdamsBJ (2006) Source of trait deterioration in entomopathogenic nematodes Heterorhabditis bacteriophora and Steinernema carpocapsae during in vivo culture. Nematology 8: 397–409.

43. Lok JB (2007) Strongyloides stercoralis: a model for translational research on parasitic nematode biology. In WormBook, www.WormBook.org.

44. ShaoH, LiX, NolanTJ, MasseyHCJr, PearceEJ, et al. (2012) Transposon-mediated chromosomal integration of transgenes in the parasitic nematode Strongyloides ratti and establishment of stable transgenic lines. PLoS Pathog 8: e1002871.

45. WhiteGF (1927) A method for obtaining infective nematode larvae from cultures. Science 66: 302–303.

46. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

47. BargmannCI, HartwiegE, HorvitzHR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74: 515–527.

48. CampbellJF, KayaHK (2000) Influence of insect-associated cues on the jumping behavior of entomopathogenic nematodes (Steinernema spp.). Behavior 137: 591–609.

49. O'HalloranDM, BurnellAM (2003) An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora. Parasitol 127: 375–385.

50. HammerØ, HarperDAT, RyanPD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4: 9pp.

51. KingJY, FerraraR, TabibiazarR, SpinJM, ChenMM, et al. (2005) Pathway analysis of coronary atherosclerosis. Physiol Genomics 23: 103–118.

52. MukabanaWR, MweresaCK, OtienoB, OmusulaP, SmallegangeRC, et al. (2012) A novel synthetic odorant blend for trapping of malaria and other African mosquito species. J Chem Ecol 38: 235–244.

53. VerhulstNO, MbadiPA, KissGB, MukabanaWR, van LoonJJ, et al. (2011) Improvement of a synthetic lure for Anopheles gambiae using compounds produced by human skin microbiota. Malar J 10: 28.

54. SmallegangeRC, Bukovinszkine-KissG, OtienoB, MbadiPA, TakkenW, et al. (2012) Identification of candidate volatiles that affect the behavioural response of the malaria mosquito Anopheles gambiae sensu stricto to an active kairomone blend: laboratory and semi-field assays. Physiol Entomol 37: 60–71.

55. MathewN, AyyanarE, ShanmugaveluS, MuthuswamyK (2013) Mosquito attractant blends to trap host seeking Aedes aegypti. Parasitol Res 112: 1305–1312.

56. MboeraLE, TakkenW, MdiraKY, PickettJA (2000) Sampling gravid Culex quinquefasciatus (Diptera: Culicidae) in Tanzania with traps baited with synthetic oviposition pheromone and grass infusions. J Med Entomol 37: 172–176.

57. LealWS, BarbosaRM, XuW, IshidaY, SyedZ, et al. (2008) Reverse and conventional chemical ecology approaches for the development of oviposition attractants for Culex mosquitoes. PLoS ONE 3: e3045.

58. MillarJG, ChaneyJD, MullaMS (1992) Identification of oviposition attractants for Culex quiquefasciatus from fermented Bermuda grass infusions. J Am Mosq Control Assoc 8: 11–17.