A Wild Strain Has Enhanced Epithelial Immunity to a Natural Microsporidian Parasite

English version České info

Infectious diseases caused by microbes create some of the strongest forces in evolution, by killing their hosts, and impairing their ability to produce progeny. Microsporidia are very common microbes that cause disease in all animals, including roundworms, insects, fish and people. We investigated microsporidia infection in the roundworm C. elegans, and found that strains from diverse parts of the world have differing levels of resistance against infection. Interestingly, a C. elegans strain from Hawaii can clear infection but only during the earliest stage of life. This resistance appears to be evolutionarily important, because it is during this early stage of life when infection can greatly reduce the number of progeny produced by the host. Consistent with this idea, if the Hawaiian strain is infected when young, it will ultimately produce more progeny than a susceptible strain of C. elegans. We find that this early life resistance of Hawaiian animals is due to a combination of genetic regions, which together provide enhanced immunity against a natural pathogen, thus enabling this strain to have more offspring.

Vyšlo v časopise: A Wild Strain Has Enhanced Epithelial Immunity to a Natural Microsporidian Parasite. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004583
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004583

Souhrn

Zdroje

1. Morens DM, Fauci AS (2013) Emerging infectious diseases: threats to human health and global stability. PLoS Pathog 9: e1003467. doi: 10.1371/journal.ppat.1003467 23853589

2. Didier ES, Weiss LM (2011) Microsporidiosis: not just in AIDS patients. Current opinion in infectious diseases 24 : 490–495. doi: 10.1097/QCO.0b013e32834aa152 21844802

3. Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56 : 93–116. doi: 10.1146/annurev.micro.56.012302.160854 12142484

4. Texier C, Vidau C, Vigues B, El Alaoui H, Delbac F (2010) Microsporidia: a model for minimal parasite-host interactions. Curr Opin Microbiol 13 : 443–449. doi: 10.1016/j.mib.2010.05.005 20542726

5. Williams BA (2009) Unique physiology of host-parasite interactions in microsporidia infections. Cell Microbiol 11 : 1551–1560. doi: 10.1111/j.1462-5822.2009.01362.x 19673893

6. Corradi N, Pombert JF, Farinelli L, Didier ES, Keeling PJ (2010) The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nature communications 1 : 77. doi: 10.1038/ncomms1082 20865802

7. Lobo ML, xiao L, Antunes F, Matos O (2012) Microsporidia as emerging pathogens and the implication for public health: a 10-year study on HIV-positive and -negative patients. Int J Parasitol 42 : 197–205. doi: 10.1016/j.ijpara.2011.12.002 22265899

8. Sak B, Brady D, Pelikanova M, Kvetonova D, Rost M, et al. (2011) Unapparent microsporidial infection among immunocompetent humans in the Czech Republic. Journal of clinical microbiology 49 : 1064–1070. doi: 10.1128/JCM.01147-10 21191056

9. Sak B, Kvac M, Kucerova Z, Kvetonova D, Sakova K (2011) Latent microsporidial infection in immunocompetent individuals—a longitudinal study. PLoS Negl Trop Dis 5: e1162. doi: 10.1371/journal.pntd.0001162 21629721

10. Graystock P, Yates K, Darvill B, Goulson D, Hughes WO (2013) Emerging dangers: deadly effects of an emergent parasite in a new pollinator host. J Invertebr Pathol 114 : 114–119. doi: 10.1016/j.jip.2013.06.005 23816821

11. Stentiford GD, Feist SW, Stone DM, Bateman KS, Dunn AM (2013) Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems. Trends Parasitol 29 : 567–578. doi: 10.1016/j.pt.2013.08.005 24091244

12. Troemel ER (2011) New Models of Microsporidiosis: Infections in Zebrafish, C. elegans, and Honey Bee. PLoS Pathog 7: e1001243. doi: 10.1371/journal.ppat.1001243 21379567

13. Kirkwood TB, Austad SN (2000) Why do we age? Nature 408 : 233–238. doi: 10.1038/35041682 11089980

14. Ramsden S, Cheung YY, Seroude L (2008) Functional analysis of the Drosophila immune response during aging. Aging Cell 7 : 225–236. doi: 10.1111/j.1474-9726.2008.00370.x 18221416

15. Shanley DP, Aw D, Manley NR, Palmer DB (2009) An evolutionary perspective on the mechanisms of immunosenescence. Trends Immunol 30 : 374–381. doi: 10.1016/j.it.2009.05.001 19541538

16. Youngman MJ, Rogers ZN, Kim DH (2011) A decline in p38 MAPK signaling underlies immunosenescence in Caenorhabditis elegans. PLoS Genet 7: e1002082. doi: 10.1371/journal.pgen.1002082 21625567

17. Ruan Q, Qian F, Yu Z (2014) Effects of polymorphisms in immunity-related genes on the immune system and successful aging. Curr Opin Immunol 29C: 49–55. doi: 10.1016/j.coi.2014.04.003

18. Troemel ER, Felix MA, Whiteman NK, Barriere A, Ausubel FM (2008) Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 6 : 2736–2752. doi: 10.1371/journal.pbio.0060309 19071962

19. Szumowski SC, Botts MR, Popovich JJ, Smelkinson MG, Troemel ER (2014) The small GTPase RAB-11 directs polarized exocytosis of the intracellular pathogen N. parisii for fecal-oral transmission from C. elegans. Proc Natl Acad Sci U S A. doi: 10.1073/pnas.1400696111 24843160

20. Felix MA, Duveau F (2012) Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC biology 10 : 59. doi: 10.1186/1741-7007-10-59 22731941

21. Irazoqui JE, Urbach JM, Ausubel FM (2010) Evolution of host innate defence: insights from Caenorhabditis elegans and primitive invertebrates. Nat Rev Immunol 10 : 47–58. doi: 10.1038/nri2689 20029447

22. Tan MW, Shapira M (2011) Genetic and molecular analysis of nematode-microbe interactions. Cellular microbiology 13 : 497–507. doi: 10.1111/j.1462-5822.2011.01570.x 21276170

23. McGhee JD (2007) The C. elegans intestine. In: Community TCeR, editor. WormBook: WormBook.

24. Andersen EC, Gerke JP, Shapiro JA, Crissman JR, Ghosh R, et al. (2012) Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet 44 : 285–290. doi: 10.1038/ng.1050 22286215

25. Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, et al. (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome research 22 : 2478–2488. doi: 10.1101/gr.142802.112 22813931

26. Andersen EC, Bloom JS, Gerke JP, Kruglyak L (2014) A variant in the neuropeptide receptor npr-1 is a major determinant of Caenorhabditis elegans growth and physiology. PLoS Genet 10: e1004156. doi: 10.1371/journal.pgen.1004156 24586193

27. Bendesky A, Pitts J, Rockman MV, Chen WC, Tan MW, et al. (2012) Long-range regulatory polymorphisms affecting a GABA receptor constitute a quantitative trait locus (QTL) for social behavior in Caenorhabditis elegans. PLoS Genet 8: e1003157. doi: 10.1371/journal.pgen.1003157 23284308

28. Bendesky A, Tsunozaki M, Rockman MV, Kruglyak L, Bargmann CI (2011) Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 472 : 313–318. doi: 10.1038/nature09821 21412235

29. Davies AG, Bettinger JC, Thiele TR, Judy ME, McIntire SL (2004) Natural variation in the npr-1 gene modifies ethanol responses of wild strains of C. elegans. Neuron 42 : 731–743. doi: 10.1016/j.neuron.2004.05.004 15182714

30. de Bono M, Bargmann CI (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94 : 679–689. doi: 10.1016/S0092-8674(00)81609-8 9741632

31. Kammenga JE, Doroszuk A, Riksen JA, Hazendonk E, Spiridon L, et al. (2007) A Caenorhabditis elegans wild type defies the temperature-size rule owing to a single nucleotide polymorphism in tra-3. PLoS Genet 3: e34. doi: 10.1371/journal.pgen.0030034 17335351

32. McGrath PT, Rockman MV, Zimmer M, Jang H, Macosko EZ, et al. (2009) Quantitative mapping of a digenic behavioral trait implicates globin variation in C. elegans sensory behaviors. Neuron 61 : 692–699. doi: 10.1016/j.neuron.2009.02.012 19285466

33. Palopoli MF, Rockman MV, TinMaung A, Ramsay C, Curwen S, et al. (2008) Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454 : 1019–1022. doi: 10.1038/nature07171 18633349

34. Reddy KC, Andersen EC, Kruglyak L, Kim DH (2009) A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 323 : 382–384. doi: 10.1126/science.1166527 19150845

35. Rockman MV, Kruglyak L (2009) Recombinational landscape and population genomics of Caenorhabditis elegans. PLoS Genet 5: e1000419. doi: 10.1371/journal.pgen.1000419 19283065

36. Twumasi-Boateng K, Wang TW, Tsai L, Lee KH, Salehpour A, et al. (2012) An age-dependent reversal in the protective capacities of JNK signaling shortens Caenorhabditis elegans lifespan. Aging cell 11 : 659–667. doi: 10.1111/j.1474-9726.2012.00829.x 22554143

37. Gallo RL, Hooper LV (2012) Epithelial antimicrobial defence of the skin and intestine. Nature reviews 12 : 503–516. doi: 10.1038/nri3228 22728527

38. Benjamin JL, Sumpter R Jr., Levine B, Hooper LV (2013) Intestinal epithelial autophagy is essential for host defense against invasive bacteria. Cell Host Microbe 13 : 723–734. doi: 10.1016/j.chom.2013.05.004 23768496

39. Nkinin SW, Asonganyi T, Didier ES, Kaneshiro ES (2007) Microsporidian infection is prevalent in healthy people in Cameroon. Journal of clinical microbiology 45 : 2841–2846. doi: 10.1128/JCM.00328-07 17609328

40. Barreiro LB, Quintana-Murci L (2010) From evolutionary genetics to human immunology: how selection shapes host defence genes. Nature reviews Genetics 11 : 17–30. doi: 10.1038/nrg2698 19953080

41. Thomas JH (2006) Adaptive evolution in two large families of ubiquitin-ligase adapters in nematodes and plants. Genome research 16 : 1017–1030. doi: 10.1101/gr.5089806 16825662

42. Collins CA, Brown EJ (2010) Cytosol as battleground: ubiquitin as a weapon for both host and pathogen. Trends in cell biology 20 : 205–213. doi: 10.1016/j.tcb.2010.01.002 20129784

43. Bakowski MA, Desjardins CA, Smelkinson MG, Dunbar TA, Lopez-Moyado IF, et al. (2014) Ubiquitin-Mediated Response to Microsporidia and Virus Infection in C. elegans. PLoS pathogens 10: e1004200. doi: 10.1371/journal.ppat.1004200 24945527

44. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77 : 71–94. 4366476

45. Stiernagle T (2006) Maintenance of C. elegans. In: Community TCeR, editor. WormBook: WormBook.

46. Estes KA, Szumowski SC, Troemel ER (2011) Non-lytic, actin-based exit of intracellular parasites from C. elegans intestinal cells. PLoS Pathog 7: e1002227. doi: 10.1371/journal.ppat.1002227 21949650

47. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19 : 889–890. doi: 10.1093/bioinformatics/btg112 12724300

48. Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142 : 285–294. 8770605

49. Bloom JS, Ehrenreich IM, Loo WT, Lite TL, Kruglyak L (2013) Finding the sources of missing heritability in a yeast cross. Nature 494 : 234–237. doi: 10.1038/nature11867 23376951