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Characterization of an Insecticidal Toxin and Pathogenicity of against Insects


Most entomopathogenic bacteria can produce toxin proteins and proliferate in the intestines of insects after natural oral ingestion. These bacteria can evade the systemic and local immune responses of insects. Here, we used insect larva of the diamond back moth (Plutella xylostella), a cruciferous crop pest to study the pathogenic mechanism of infection by novel bacterium Psudomonas taiwanensis. We examined how P. taiwanensis colonizes and escapes the immune response in the gut of P. xylostella and the mechanism of pathogenesis after oral ingestion of P. taiwanensis. Oral ingestion of P. taiwanensis induced severe damage in intestinal cells of P. xylostella and disrupted intestinal epithelial integrity. A toxin protein, the C component of insecticidal toxin protein complex (TccC) contributed to the pathogenicity of P. taiwanensis by thwarting oxidative stress and phagocytosis and inducing apoptosis in the gut cells of the host. Taken together our results shed light on the bacterial pathogenic processes in insect hosts, particularly the mechanism of pathogenesis of P. taiwanensis.


Vyšlo v časopise: Characterization of an Insecticidal Toxin and Pathogenicity of against Insects. PLoS Pathog 10(8): e32767. doi:10.1371/journal.ppat.1004288
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004288

Souhrn

Most entomopathogenic bacteria can produce toxin proteins and proliferate in the intestines of insects after natural oral ingestion. These bacteria can evade the systemic and local immune responses of insects. Here, we used insect larva of the diamond back moth (Plutella xylostella), a cruciferous crop pest to study the pathogenic mechanism of infection by novel bacterium Psudomonas taiwanensis. We examined how P. taiwanensis colonizes and escapes the immune response in the gut of P. xylostella and the mechanism of pathogenesis after oral ingestion of P. taiwanensis. Oral ingestion of P. taiwanensis induced severe damage in intestinal cells of P. xylostella and disrupted intestinal epithelial integrity. A toxin protein, the C component of insecticidal toxin protein complex (TccC) contributed to the pathogenicity of P. taiwanensis by thwarting oxidative stress and phagocytosis and inducing apoptosis in the gut cells of the host. Taken together our results shed light on the bacterial pathogenic processes in insect hosts, particularly the mechanism of pathogenesis of P. taiwanensis.


Zdroje

1. WaterfieldNR, BowenDJ, FetherstonJD, PerryRD, ffrench-ConstantRH (2001) The tc genes of Photorhabdus: a growing family. Trends Microbiol 9: 185–191.

2. Ffrench-ConstantR, WaterfieldN (2006) An ABC guide to the bacterial toxin complexes. Adv Appl Microbiol 58: 169–183.

3. WaterfieldN, DowlingA, SharmaS, DabornPJ, PotterU, et al. (2001) Oral toxicity of Photorhabdus luminescens W14 toxin complexes in Escherichia coli. Appl Environ Microbiol 67: 5017–5024.

4. WaterfieldN, HaresM, YangG, DowlingA, ffrench-ConstantR (2005) Potentiation and cellular phenotypes of the insecticidal Toxin complexes of Photorhabdus bacteria. Cellular Microbiology 7: 373–382.

5. LangAE, SchmidtG, SchlosserA, HeyTD, LarrinuaIM, et al. (2010) Photorhabdus luminescens Toxins ADP-Ribosylate Actin and RhoA to Force Actin Clustering. Science 327: 1139–1142.

6. LiuD, BurtonS, GlancyT, LiZ-S, HamptonR, et al. (2003) Insect resistance conferred by 283-kDa Photorhabdus luminescens protein TcdA in Arabidopsis thaliana. Nature Biotechnology 21: 1222–1228.

7. LeeSC, Stoilova-McphieS, BaxterL, FülöpV, HendersonJ, et al. (2007) Structural Characterisation of the Insecticidal Toxin XptA1, Reveals a 1.15 MDa Tetramer with a Cage-like Structure. Journal of Molecular Biology 366: 1558–1568.

8. OttoH, Tezcan-MerdolD, GirischR, HaagF, RhenM, et al. (2000) The spvB gene-product of the Salmonella enterica virulence plasmid is a mono(ADP-ribosyl)transferase. Mol Microbiol 37: 1106–1115.

9. MooreJD (2001) The Ran-GTPase and cell-cycle control. Bioessays 23: 77–85.

10. Joo LeeP, AhnJ-Y, KimY-H, Wook KimS, KimJ-Y, et al. (2004) Cloning and heterologous expression of a novel insecticidal gene (tccC1) from Xenorhabdus nematophilus strain. Biochemical and Biophysical Research Communications 319: 1110–1116.

11. LemaitreB, HoffmannJ (2007) The Host Defense of Drosophila melanogaster. Annual Review of Immunology 25: 697–743.

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

13. 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.

14. LiehlP, BlightM, VodovarN, BoccardF, LemaitreB (2006) Prevalence of Local Immune Response against Oral Infection in a Drosophila/Pseudomonas Infection Model. PLoS Pathogens 2: e56.

15. VodovarN, VallenetD, CruveillerS, RouyZ, BarbeV, et al. (2006) Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nature Biotechnology 24: 673–679.

16. VodovarN (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. Proceedings of the National Academy of Sciences 102: 11414–11419.

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

18. ApidianakisY, PitsouliC, PerrimonN, RahmeL (2009) Synergy between bacterial infection and genetic predisposition in intestinal dysplasia. Proc Natl Acad Sci U S A 106: 20883–20888.

19. JiangH, PatelPH, KohlmaierA, GrenleyMO, McEwenDG, et al. (2009) Cytokine/Jak/Stat signaling mediates regeneration and homeostasis in the Drosophila midgut. Cell 137: 1343–1355.

20. WangLT, TaiCJ, WuYC, ChenYB, LeeFL, et al. (2009) Pseudomonas taiwanensis sp. nov., isolated from soil. International Journal of Systematic and Evolutionary Microbiology 60: 2094–2098.

21. WangS-L, ChenS-J, WangC-L (2008) Purification and characterization of chitinases and chitosanases from a new species strain Pseudomonas sp. TKU015 using shrimp shells as a substrate. Carbohydrate Research 343: 1171–1179.

22. WangS-L, ChenH-J, LiangT-W, LinY-D (2009) A novel nattokinase produced by Pseudomonas sp. TKU015 using shrimp shells as substrate. Process Biochemistry 44: 70–76.

23. LiuJ-R, LinY-D, ChangS-T, ZengY-F, WangS-L (2010) Molecular Cloning and Characterization of an Insecticidal Toxin from Pseudomonas taiwanensis. Journal of Agricultural and Food Chemistry 58: 12343–12349.

24. LangAE, SchmidtG, SheetsJJ, AktoriesK (2011) Targeting of the actin cytoskeleton by insecticidal toxins from Photorhabdus luminescens. Naunyn Schmiedebergs Arch Pharmacol 383: 227–235.

25. HakimRS, BaldwinK, SmaggheG (2010) Regulation of Midgut Growth, Development, and Metamorphosis. Annual Review of Entomology 55: 593–608.

26. HurstMRH, JonesSA, BinglinT, HarperLA, JacksonTA, et al. (2011) The Main Virulence Determinant of Yersinia entomophaga MH96 Is a Broad-Host-Range Toxin Complex Active against Insects. Journal of Bacteriology 193: 1966–1980.

27. LoebMJ, MartinPA, HakimRS, GotoS, TakedaM (2001) Regeneration of cultured midgut cells after exposure to sublethal doses of toxin from two strains of Bacillus thuringiensis. J Insect Physiol 47: 599–606.

28. TanakaS, YoshizawaY, SatoR (2012) Response of midgut epithelial cells to Cry1Aa is toxin-dependent and depends on the interplay between toxic action and the host apoptotic response. FEBS Journal 279: 1071–1079.

29. Meneses-AcostaA, MendoncaR, MerchantH, CovarrubiasL, RamirezO (2001) Comparative characterization of cell death between Sf9 insect cells and hybridoma cultures. Biotechnol Bioeng 72: 441–457.

30. RyooHD, GorencT, StellerH (2004) Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev Cell 7: 491–501.

31. Shahidi-NoghabiS, DammeEJMV, IgaM, SmaggheG (2010) Exposure of insect midgut cells to Sambucus nigra L. agglutinins I and II causes cell death via caspase-dependent apoptosis. Journal of Insect Physiology 56: 1101–1107.

32. BradshawM, DineenSS, MaksND, JohnsonEA (2004) Regulation of neurotoxin complex expression in Clostridium botulinum strains 62A, Hall A-hyper, and NCTC 2916. Anaerobe 10: 321–333.

33. SaujetL, MonotM, DupuyB, SoutourinaO, Martin-VerstraeteI (2011) The key sigma factor of transition phase, SigH, controls sporulation, metabolism, and virulence factor expression in Clostridium difficile. Journal of bacteriology 193: 3186–3196.

34. WhistlerCA, CorbellNA, SarniguetA, ReamW, LoperJE (1998) The two-component regulators GacS and GacA influence accumulation of the stationary-phase sigma factor sigmaS and the stress response in Pseudomonas fluorescens Pf-5. J Bacteriol 180: 6635–6641.

35. De la Torre-ZavalaS, AguileraS, Ibarra-LacletteE, Hernandez-FloresJL, Hernandez-MoralesA, et al. (2011) Gene expression of Pht cluster genes and a putative non-ribosomal peptide synthetase required for phaseolotoxin production is regulated by GacS/GacA in Pseudomonas syringae pv. phaseolicola. Res Microbiol 162: 488–498.

36. HaEM, OhCT, RyuJH, BaeYS, KangSW, et al. (2005) An antioxidant system required for host protection against gut infection in Drosophila. Developmental cell 8: 125–132.

37. TzouP, De GregorioE, LemaitreB (2002) How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Current opinion in microbiology 5: 102–110.

38. HultmarkD (2003) Drosophila immunity: paths and patterns. Current opinion in immunology 15: 12–19.

39. MeuschD, GatsogiannisC, EfremovRG, LangAE, HofnagelO, et al. (2014) Mechanism of Tc toxin action revealed in molecular detail. Nature 508: 61–65.

40. KalmanM, GentryDR, CashelM (1991) Characterization of the Escherichia coli K12 gltS glutamate permease gene. Mol Gen Genet 225: 379–386.

41. TolnerB, PoolmanB, KoningsWN (1992) Characterization and functional expression in Escherichia coli of the sodium/proton/glutamate symport proteins of Bacillus stearothermophilus and Bacillus caldotenax. Mol Microbiol 6: 2845–2856.

42. ShibayamaK, WachinoJ, ArakawaY, SaidijamM, RutherfordNG, et al. (2007) Metabolism of glutamine and glutathione via gamma-glutamyltranspeptidase and glutamate transport in Helicobacter pylori: possible significance in the pathophysiology of the organism. Mol Microbiol 64: 396–406.

43. HendriksenWT, KloostermanTG, BootsmaHJ, EstevaoS, de GrootR, et al. (2008) Site-specific contributions of glutamine-dependent regulator GlnR and GlnR-regulated genes to virulence of Streptococcus pneumoniae. Infect Immun 76: 1230–1238.

44. TalaA, MonacoC, NagorskaK, ExleyRM, CorbettA, et al. (2011) Glutamate utilization promotes meningococcal survival in vivo through avoidance of the neutrophil oxidative burst. Molecular microbiology 81: 1330–1342.

45. DonaldsonDM, RobertsRR, LarsenHS, TewJG (1974) Interrelationship between serum beta-lysin, lysozyme, and the antibody-complement system in killing Escherichia coli. Infect Immun 10: 657–666.

46. Patterson-DelafieldJ, MartinezRJ, LehrerRI (1980) Microbicidal cationic proteins in rabbit alveolar macrophages: a potential host defense mechanism. Infect Immun 30: 180–192.

47. AgueroME, AronL, DeLucaAG, TimmisKN, CabelloFC (1984) A plasmid-encoded outer membrane protein, TraT, enhances resistance of Escherichia coli to phagocytosis. Infect Immun 46: 740–746.

48. AuC, DeanP, ReynoldsSE, ffrench-ConstantRH (2004) Effect of the insect pathogenic bacterium Photorhabdus on insect phagocytes. Cell Microbiol 6: 89–95.

49. SukupolviS, O'ConnorCD (1990) TraT lipoprotein, a plasmid-specified mediator of interactions between gram-negative bacteria and their environment. Microbiol Rev 54: 331–341.

50. TombJF, WhiteO, KerlavageAR, ClaytonRA, SuttonGG, et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539–547.

51. FanY, BergmannA (2010) The cleaved-Caspase-3 antibody is a marker of Caspase-9-like DRONC activity in Drosophila. Cell Death Differ 17: 534–539.

52. SimonR, PrieferU, PuhlerA (1983) A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria. Nat Biotech 1: 784–791.

53. McClintockJT, DoughertyEM, WeinerRM (1986) Semipermissive Replication of a Nuclear Polyhedrosis Virus of Autographa californica in a Gypsy Moth Cell Line. J Virol 57: 197–204.

54. SchweizerHP, HoangTT (1995) An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15–22.

55. DatsenkoKA (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences 97: 6640–6645.

56. RoehmNW, RodgersGH, HatfieldSM, GlasebrookAL (1991) An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT. J Immunol Methods 142: 257–265.

57. van EngelandM, NielandLJ, RamaekersFC, SchutteB, ReutelingspergerCP (1998) Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31: 1–9.

58. PortaH, Muñoz-MinuttiC, SoberónM, BravoA (2011) Induction of Manduca sexta Larvae Caspases Expression in Midgut Cells by Bacillus thuringiensis Cry1Ab Toxin. Psyche: A Journal of Entomology 2011: 1–7.

59. HuangC-H, ChiouS-H (2011) Proteomic analysis of upregulated proteins in Helicobacter pylori under oxidative stress induced by hydrogen peroxide. The Kaohsiung Journal of Medical Sciences 27: 544–53.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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