Distinctive Expansion of Potential Virulence Genes in the Genome of the Oomycete Fish Pathogen

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Oomycetes in the class Saprolegniomycetidae of the Eukaryotic kingdom Stramenopila have evolved as severe pathogens of amphibians, crustaceans, fish and insects, resulting in major losses in aquaculture and damage to aquatic ecosystems. We have sequenced the 63 Mb genome of the fresh water fish pathogen, Saprolegnia parasitica. Approximately 1/3 of the assembled genome exhibits loss of heterozygosity, indicating an efficient mechanism for revealing new variation. Comparison of S. parasitica with plant pathogenic oomycetes suggests that during evolution the host cellular environment has driven distinct patterns of gene expansion and loss in the genomes of plant and animal pathogens. S. parasitica possesses one of the largest repertoires of proteases (270) among eukaryotes that are deployed in waves at different points during infection as determined from RNA-Seq data. In contrast, despite being capable of living saprotrophically, parasitism has led to loss of inorganic nitrogen and sulfur assimilation pathways, strikingly similar to losses in obligate plant pathogenic oomycetes and fungi. The large gene families that are hallmarks of plant pathogenic oomycetes such as Phytophthora appear to be lacking in S. parasitica, including those encoding RXLR effectors, Crinkler's, and Necrosis Inducing-Like Proteins (NLP). S. parasitica also has a very large kinome of 543 kinases, 10% of which is induced upon infection. Moreover, S. parasitica encodes several genes typical of animals or animal-pathogens and lacking from other oomycetes, including disintegrins and galactose-binding lectins, whose expression and evolutionary origins implicate horizontal gene transfer in the evolution of animal pathogenesis in S. parasitica.

Vyšlo v časopise: Distinctive Expansion of Potential Virulence Genes in the Genome of the Oomycete Fish Pathogen. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003272
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003272

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Zdroje

1. PhillipsAJ, AndersonVL, RobertsonEJ, SecombesCJ, van WestP (2008) New insights into animal pathogenic oomycetes. TIM 16: 13–19.

2. Van WestP (2006) Saprolegnia parasitica, an oomycete pathogen with a fishy appetite: new challenges for an old problem. Mycologist 20: 99–104.

3. Bruno DW, van West P, GW B (2009) Saprolegnia and other oomycetes. In: Bruno DW, , editors. In: Fish Diseases and Disorders, 2nd edition. CABI. pp. 669–720.

4. DenoeudF, RousselM, NoelB, WawrzyniakI, Da SilvaC, et al. (2011) Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biol 12(3): R29.

5. PattersonDJ (1999) The diversity of eukaryotes. American Naturalist 154: S96–S124.

6. Dieguez-UribeondoJ, GarciaMA, CereniusL, KozubikovaE, BallesterosI, et al. (2009) Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (Oomycetes). Fungal Genet.Biol 46: 365–376.

7. Tyler BM (2009) Effectors. In: Oomycete Genetics and Genomics. John Wiley & Sons, Inc. pp. 361–385.

8. Van West P, Vleeshouwers VG (2004) The Phytophthora infestans -host interaction. In: Talbot NJ, editor. In: Plant Pathogen Interactions, Annual Plant Reviews. Blackwell Scientific Publishers. pp. 219–242.

9. TylerBM (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol Plant Pathol 8: 1–8.

10. GruenwaldNJ, GarbelottoM, GossEM, HeungensK, ProsperoS (2012) Emergence of the sudden oak death pathogen Phytophthora ramorum. TIM 20: 131–138.

11. TylerBM, TripathyS, ZhangX, DehalP, JiangRHY, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261–1266.

12. HaasBJ, KamounS, ZodyMC, JiangRHY, HandsakerRE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.

13. LamourK, MudgeJ, GobenaD, Hurtado-GonzalesOP, SchmutzJ, et al. (2012) Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol Plant-Microbe Interact 25: 1350–1360.

14. LevesqueCA, BrouwerH, CanoL, HamiltonJP, HoltC, et al. (2010) Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11(7): R73.

15. BaxterL, TripathyS, IshaqueN, BootN, CabralA, et al. (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330: 1549–1551.

16. LinksMG, HolubE, JiangRHY, SharpeAG, HegedusD, et al. (2011) De novo sequence assembly of Albugo candida reveals a small genome relative to other biotrophic oomycetes. BMC Genomics 12: 503.

17. JiangRHY, TylerBM (2012) Mechanisms and evolution of virulence in oomycetes. Annu Rev Phytopathol 50: 295–318.

18. RaffaeleS, KamounS (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Rev Microbiol 10: 417–430.

19. KamounS (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu Rev Phytopathol 44: 41–60.

20. SchornackS, HuitemaE, CanoLM, BozkurtTO, OlivaR, et al. (2009) Ten things to know about oomycete effectors. Mol Plant Pathol 10: 795–803.

21. GrouffaudS, van WestP, AvrovaAO, BirchPRJ, WhissonSC (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology-Sgm 154: 3743–3751.

22. JiangRHY, TripathyS, GoversF, TylerBM (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. PNAS 105: 4874–4879.

23. SchornackS, van DammeM, BozkurtTO, CanoLM, SmokerM, et al. (2010) Ancient class of translocated oomycete effectors targets the host nucleus. PNAS 107: 17421–17426.

24. WhissonSC, BoevinkPC, MolelekiL, AvrovaAO, MoralesJG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115–118.

25. DouD, KaleSD, WangX, JiangRHY, BruceNA, et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. The Plant Cell 20: 1930–1947.

26. GaulinE, MadouiM-A, BottinA, JacquetC, MatheC, et al. (2008) Transcriptome of Aphanomyces euteiches: new oomycete putative pathogenicity factors and metabolic pathways. Plos One 3: e1723.

27. Torto-AlaliboT, TianMY, GajendranK, WaughME, van WestP, et al. (2005) Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors. BMC Microbiology 5: 46.

28. Van WestP, de BruijnI, MinorKL, PhillipsAJ, RobertsonEJ, et al. (2010) The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiology 310: 127–137.

29. KrajaejunT, KhositnithikulR, LerksuthiratT, LowhnooT, RujirawatT, et al. (2011) Expressed sequence tags reveal genetic diversity and putative virulence factors of the pathogenic oomycete Pythium insidiosum. Fungal Biol 115: 683–696.

30. WawraS, BainJ, DurwardE, de BruijnI, MinorKL, et al. (2012) Host-targeting protein 1 (SpHtp1) from the oomycete Saprolegnia parasitica translocates specifically into fish cells in a tyrosine-O-sulphate-dependent manner. PNAS 109: 2096–2101.

31. GrabherrMG, HaasBJ, YassourM, LevinJZ, ThompsonDA, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotech 29: 644–U130.

32. ChamnanpuntJ, ShanWX, TylerBM (2001) High frequency mitotic gene conversion in genetic hybrids of the oomycete Phytophthora sojae. PNAS 98: 14530–14535.

33. MacGregorT, BhattacharyyaM, TylerB, BhatR, SchmitthennerAF, et al. (2002) Genetic and physical mapping of Avrla in Phytophthora sojae. Genetics 160: 949–959.

34. SlamovitsCH, KeelingPJ (2009) Evolution of ultrasmall spliceosomal introns in highly reduced nuclear genomes. Mol Biol Evol 26: 1699–1705.

35. MuotriAR, MarchettoMCN, CoufalNG, GageFH (2007) The necessary junk: new functions for transposable elements. Human Mol Gen 16: R159–R167.

36. JudelsonHS, Ah-FongAMV (2010) The kinome of Phytophthora infestans reveals oomycete-specific innovations and links to other taxonomic groups. BMC Genomics 11: 700.

37. GaulinE, DrameN, LafitteC, Torto-AlaliboT, MartinezY, et al. (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. The Plant Cell 18: 1766–1777.

38. Schneider DJ, Collmer A (2010) Studying plant-pathogen interactions in the genomics era: beyond molecular Koch's Postulates to systems biology. In: VanAlfen NK, Bruening G, Leach JE, editors. Annu. Rev. Phytopathol. Vol 48. pp. 457–479.

39. GuerrieroG, AvinoM, ZhouQ, FugelstadJ, ClergeotP-H, et al. (2010) Chitin synthases from Saprolegnia are involved in tip growth and represent a potential target for anti-oomycete drugs. PLoS Pathogens 6: e1001070–e1001070.

40. MélidaH, Sandoval-SierraJV, Diéguez-UribeondoJ, BuloneV (2013) Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryotic Cell 12: 194–203.

41. Bartnicki-GarciaS (1968) Cell wall chemistry morphogenesis and taxonomy of fungi. Annu Rev Microbiol 22: 87–108.

42. BuloneV, ChanzyH, GayL, GirardV, FevreM (1992) Characterization of chitin and chitin synthase from the cellulosic cell-wall fungus Saprolegnia monoica. Experimental Mycology 16: 8–21.

43. BadreddineI, LafitteC, HeuxL, SkandalisN, SpanouZ, et al. (2008) Cell wall chitosaccharides are essential components and exposed patterns of the phytopathogenic oomycete Aphanomyces euteiches. Eukaryotic Cell 7: 1980–1993.

44. GaulinE, BottinA, DumasB (2010) Sterol biosynthesis in oomycete pathogens. Plant signaling & behavior 5: 258–260.

45. MadouiM-A, Bertrand-MichelJ, GaulinE, DumasB (2009) Sterol metabolism in the oomycete Aphanomyces euteiches, a legume root pathogen. New Phytologist 183: 291–300.

46. CantarelBL, CoutinhoPM, RancurelC, BernardT, LombardV, et al. (2009) The Carbohydrate-active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Research 37: D233–D238.

47. MorrisPF, SchlosserLR, OnaschKD, WittenschlaegerT, AustinR, et al. (2009) Multiple horizontal gene transfer events and domain fusions have created novel regulatory and metabolic networks in the oomycete genome. Plos One 4: e6133.

48. SeidlMF, Van den AckervekenG, GoversF, SnelB (2011) A domain-centric analysis of oomycete plant pathogen genomes reveals unique protein organization. Plant Physiology 155: 628–644.

49. GaulinE, JauneauA, VillalbaF, RickauerM, Esquerre-TugayeMT, et al. (2002) The CBEL glycoprotein of Phytophthora parasitica var. nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. Journal of Cell Science 115: 4565–4575.

50. BjornsdottirB, FridjonssonOH, MagnusdottirS, AndresdottirV, HreggvidssonGO, et al. (2009) Characterisation of an extracellular vibriolysin of the fish pathogen Moritella viscosa. Veterinary Microbiology 136: 326–334.

51. LuY-J, SchornackS, SpallekT, GeldnerN, ChoryJ, et al. (2012) Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cellular Microbiology 14: 682–697.

52. HuitemaE, VleeshouwersV, CakirC, KamounS, GoversF (2005) Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INN, INF2A, and INF2B of Phytophthora infestans. Molecular Plant-Microbe Interactions 18: 183–193.

53. JiangRHY, TylerBM, WhissonSC, HardhamAR, GoversF (2006) Ancient origin of elicitin gene clusters in Phytophthora genomes. Molecular Biology and Evolution 23: 338–351.

54. RaffaeleS, FarrerRA, CanoLM, StudholmeDJ, MacLeanD, et al. (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330: 1540–1543.

55. VernikosGS, ParkhillJ (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22: 2196–2203.

56. BeakesGW, GlocklingSL, SekimotoS (2012) The evolutionary phylogeny of the oomycete “fungi”. Protoplasma 249: 3–19.

57. KüpperFC, MaierI, MüllerG, Loiseaux-De GoerS, GuillouL (2006) Phylogenetic affinities of two eukaryotic pathogens of marine macroalgae, Eurychasma dicksonii (Wright) Magnus and Chytridium polysiphoniae Coh. Cryptogamie, Algologie 27: 165–184.

58. BatemanA, RawlingsND (2003) The CHAP domain: a large family of amidases including GSP amidase and peptidoglycan hydrolases. Trends in Biochemical Sciences 28: 234–237.

59. Hunt S, Green J, Artymiuk PJ (2010) Hemolysin E (HlyE, ClyA, SheA) and related toxins. In: Anderluh G, Lakey J, editors. Proteins: Membrane Binding and Pore Formation. pp. 116–126.

60. OzekiY, MatsuiT, SuzukiM, TitaniK (1991) Amino acid sequence and molecular characterization of a D-galactoside -specific lectin purified from sea-urchin (Anthocidaris crassipina) eggs. Biochemistry 30: 2391–2394.

61. OzekiY, YokotaY, KatoKH, TitaniK, MatsuiT (1995) Developmental expression of D-galactoside-binding lectin in sea urchin (Anthocidaris crassipina) eggs. Experimental Cell Research 216: 318–324.

62. OgawaT, WatanabeM, NaganumaT, MuramotoK (2011) Diversified carbohydrate-binding lectins from marine resources. Journal of amino acids 2011: 838914–838914.

63. McLaneM, SanchezE, WongA, Paquette-StraubC, PerezJC (2004) Disintegrins. Curr Drug Targets Cardiovasc Haematol Disord 4: 327–355.

64. EbstrupT, SaalbachG, EgsgaardH (2005) A proteomics study of in vitro cyst germination and appressoria formation in Phytophthora infestans. Proteomics 5: 2839–2848.

65. ShanWX, MarshallJS, HardhamAR (2004) Gene expression in germinated cysts of Phytophthora nicotianae. Molecular Plant Pathology 5: 317–330.

66. Torto-AlaliboTA, TripathyS, SmithBM, ArredondoFD, ZhouL, et al. (2007) Expressed sequence tags from Phytophthora sojae reveal genes specific to development and infection. Molecular Plant-Microbe Interactions 20: 781–793.

67. YeW, WangX, TaoK, LuY, DaiT, et al. (2011) Digital gene expression profiling of the Phytophthora sojae transcriptome. Molecular Plant-Microbe Interactions 24: 1530–1539.

68. RosenblumEB, StajichJE, MaddoxN, EisenMB (2008) Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 105: 17034–17039.

69. McDowellJM (2011) Genomes of obligate plant pathogens reveal adaptations for obligate parasitism. Proceedings of the National Academy of Sciences of the United States of America 108: 8921–8922.

70. StuelandS, HataiK, SkaarI (2005) Morphological and physiological characteristics of Saprolegnia spp. strains pathogenic to Atlantic salmon, Salmo salar L. Journal of Fish Diseases 28: 445–453.

71. WolfK, QuimbyMC (1962) Established eurythermic line of fish cell in vitro. Science 135: 1065–1066.

72. LennonNJ, LintnerRE, AndersonS, AlvarezP, BarryA, et al. (2010) A scalable, fully automated process for construction of sequence-ready barcoded libraries for 454. Genome Biology 11: R15.

73. FisherS, BarryA, AbreuJ, MinieB, NolanJ, et al. (2011) A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biology 12: R1.

74. LevinJZ, YassourM, AdiconisX, NusbaumC, ThompsonDA, et al. (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nature Methods 7: 709–U767.

75. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.

76. McKennaA, HannaM, BanksE, SivachenkoA, CibulskisK, et al. (2010) The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research 20: 1297–1303.

77. HaasBJ, DelcherAL, MountSM, WortmanJR, SmithRK, et al. (2003) Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Research 31: 5654–5666.

78. RhindN, ChenZ, YassourM, ThompsonDA, HaasBJ, et al. (2011) Comparative functional genomics of the fission yeasts. Science 332: 930–936.

79. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.

80. BenjaminiY, HochbergY (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289–300.

81. KanehisaM, GotoS, KawashimaS, OkunoY, HattoriM (2004) The KEGG resource for deciphering the genome. Nucleic Acids Research 32: D277–D280.

82. Hudson L, Hay F (1980) Practical Immunology. London, UK: Blackwell Scientific Publications. pp. 1–9, 113–137, 227–229.