Palaeosymbiosis Revealed by Genomic Fossils of in a Strongyloidean Nematode

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Bovine lungworms are economically important nematode parasites of cattle. We have sequenced the genome of the bovine lungworm to provide information for drug and vaccine discovery. Within the lungworm genome we found extensive evidence of an ancient association between the lungworm and a bacterium called Wolbachia. The lungworm Wolbachia is now a “fossil” in the genome, but tells of an ancient infection. Association between lungworms, and related nematode worms, and Wolbachia was not known previously. We have used the lungworm Wolbachia sequence to explore the history of nematode-Wolbachia interactions, particularly the jumping of these symbionts between arthropods and nematodes.

Vyšlo v časopise: Palaeosymbiosis Revealed by Genomic Fossils of in a Strongyloidean Nematode. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004397
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004397

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1. WerrenJH (1997) Biology of Wolbachia. Annual Reviews of Entomology 42 : 587–609.

2. ZugR, HammersteinP (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PloS one 7: e38544.

3. WerrenJH, BaldoL, ClarkME (2008) Wolbachia: master manipulators of invertebrate biology. Nature reviews Microbiology 6 : 741–751.

4. WalkerT, JohnsonPH, MoreiraLA, Iturbe-OrmaetxeI, FrentiuFD, et al. (2011) The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476 : 450–453.

5. LoN, ParaskevopoulosC, BourtzisK, O'NeillSL, WerrenJH, et al. (2007) Taxonomic status of the intracellular bacterium Wolbachia pipientis. International journal of systematic and evolutionary microbiology 57 : 654–657.

6. Comandatore F, Sassera D, Montagna M, Kumar S, Koutsovoulos G, et al. (2013) Phylogenomics and analysis of shared genes suggest a single transition to mutualism in Wolbachia of nematodes. Genome biology and evolution.

7. AugustinosAA, Santos-GarciaD, DionyssopoulouE, MoreiraM, PapapanagiotouA, et al. (2011) Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled? PloS one 6: e28695.

8. BandiC, AndersonTJ, GenchiC, BlaxterML (1998) Phylogeny of Wolbachia in filarial nematodes. Proc Biol Sci 265 : 2407–2413.

9. FosterJ, GanatraM, KamalI, WareJ, MakarovaK, et al. (2005) The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biology 3: e121.

10. GenchiC, SacchiL, BandiC, VencoL (1998) Preliminary results on the effect of tetracycline on the embryogenesis and symbiotic bacteria (Wolbachia) of Dirofilaria immitis. An update and discussion. Parassitologia 40 : 247–249.

11. HoeraufA, Nissen-PahleK, SchmetzC, Henkle-DuhrsenK, BlaxterML, et al. (1999) Tetracycline therapy targets intracellular bacteria in the filarial nematode Litomosoides sigmodontis and results in filarial infertility. J Clin Invest 103 : 11–18.

12. McGarryHF, PfarrK, EgertonG, HoeraufA, AkueJP, et al. (2003) Evidence against Wolbachia symbiosis in Loa loa. Filaria journal 2 : 9.

13. TaylorMJ, CrossHF, BiloK (2000) Inflammatory responses induced by the filarial nematode Brugia malayi are mediated by lipopolysaccharide-like activity from endosymbiotic Wolbachia bacteria. The Journal of experimental medicine 191 : 1429–1436.

14. FennK, BlaxterM (2004) Are filarial nematode Wolbachia obligate mutualist symbionts? Trends in Ecology and Evolution 19 : 163–166.

15. FennK, BlaxterM (2006) Wolbachia genomes: revealing the biology of parasitism and mutualism. Trends Parasitol 22 : 60–65.

16. DarbyAC, ArmstrongSD, BahGS, KaurG, HughesMA, et al. (2012) Analysis of gene expression from the Wolbachia genome of a filarial nematode supports both metabolic and defensive roles within the symbiosis. Genome Res 22 : 2467–2477.

17. CasiraghiM, BordensteinSR, BaldoL, LoN, BeninatiT, et al. (2005) Phylogeny of Wolbachia pipientis based on gltA, groEL and ftsZ gene sequences: clustering of arthropod and nematode symbionts in the F supergroup, and evidence for further diversity in the Wolbachia tree. Microbiology 151 : 4015–4022.

18. LefoulonE, GavotteL, JunkerK, BarbutoM, UniS, et al. (2012) A new type F Wolbachia from Splendidofilariinae (Onchocercidae) supports the recent emergence of this supergroup. Int J Parasitol 42 : 1025–1036.

19. CasiraghiM, BainO, GuerreroR, MartinC, PocacquaV, et al. (2004) Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. International journal for parasitology 34 : 191–203.

20. HaegemanA, VanholmeB, JacobJ, VandekerckhoveTT, ClaeysM, et al. (2009) An endosymbiotic bacterium in a plant-parasitic nematode: member of a new Wolbachia supergroup. International journal for parasitology 39 : 1045–1054.

21. BordensteinSR, FitchDH, WerrenJH (2003) Absence of wolbachia in nonfilariid nematodes. Journal of nematology 35 : 266–270.

22. ElsworthB, WasmuthJ, BlaxterM (2011) NEMBASE4: the nematode transcriptome resource. International journal for parasitology 41 : 881–894.

23. BlaxterM (2011) Nematodes: the worm and its relatives. PLoS biology 9: e1001050.

24. FerriE, BainO, BarbutoM, MartinC, LoN, et al. (2011) New insights into the evolution of Wolbachia infections in filarial nematodes inferred from a large range of screened species. PloS one 6: e20843.

25. BlaxterM (2007) Symbiont Genes in Host Genomes: Fragments with a Future? Cell Host and Microbe 2 : 211–213.

26. FennK, ConlonC, JonesM, QuailMA, HolroydNE, et al. (2006) Phylogenetic relationships of the Wolbachia of nematodes and arthropods. PLoS Pathog 2: e94.

27. Dunning Hotopp JC, Clark ME, Oliveira DCSG, Foster JM, Fischer P, et al. (2007) Widespread Lateral Gene Transfer from Intracellular Bacteria to Multicellular Eukaryotes. Science Epub ahead of print on ScienceExpress Aug 30, 2007.

28. McNultySN, AbubuckerS, SimonGM, MitrevaM, McNultyNP, et al. (2012) Transcriptomic and proteomic analyses of a Wolbachia-free filarial parasite provide evidence of trans-kingdom horizontal gene transfer. PloS one 7: e45777.

29. McNultySN, FischerK, CurtisKC, WeilGJ, BrattigNW, et al. (2013) Localization of Wolbachia-like gene transcripts and peptides in adult Onchocerca flexuosa worms indicates tissue specific expression. Parasites & vectors 6 : 2.

30. IoannidisP, JohnstonKL, RileyDR, KumarN, WhiteJR, et al. (2013) Extensively duplicated and transcriptionally active recent lateral gene transfer from a bacterial Wolbachia endosymbiont to its host filarial nematode Brugia malayi. BMC Genomics 14 : 639.

31. McNultySN, FosterJM, MitrevaM, Dunning HotoppJC, MartinJ, et al. (2010) Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One 5: e11029.

32. CasiraghiM, AndersonTJ, BandiC, BazzocchiC, GenchiC (2001) A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology 122 Pt 1 : 93–103.

33. DesjardinsCA, CerqueiraGC, GoldbergJM, Dunning HotoppJC, HaasBJ, et al. (2013) Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature genetics 45 : 495–500.

34. KatzourakisA (2013) Paleovirology: inferring viral evolution from host genome sequence data. Philos Trans R Soc Lond B Biol Sci 368 : 20120493.

35. KatzourakisA, GiffordRJ (2010) Endogenous viral elements in animal genomes. PLoS Genet 6: e1001191.

36. KumarS, KoutsovoulosG, KaurG, BlaxterM (2012) Toward 959 nematode genomes. Worm 1 : 1–9.

37. KumarS, JonesM, KoutsovoulosG, ClarkeM, BlaxterM (2013) Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots. Frontiers in Genetics 4 : 237.

38. BaiX, AdamsBJ, CicheTA, CliftonS, GauglerR, et al. (2013) A lover and a fighter: the genome sequence of an entomopathogenic nematode Heterorhabditis bacteriophora. PloS one 8: e69618.

39. ParraG, BradnamK, KorfI (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23 : 1061–1067.

40. CantacessiC, GasserRB, StrubeC, SchniederT, JexAR, et al. (2011) Deep insights into Dictyocaulus viviparus transcriptomes provides unique prospects for new drug targets and disease intervention. Biotechnology advances 29 : 261–271.

41. CantarelBL, KorfI, RobbSM, ParraG, RossE, et al. (2008) MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome research 18 : 188–196.

42. StankeM, KellerO, GunduzI, HayesA, WaackS, et al. (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Research 34: W435–439.

43. The C. elegans Genome Sequencing Consortium (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282 : 2012–2018.

44. SchwarzEM, KorhonenPK, CampbellBE, YoungND, JexAR, et al. (2013) The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus. Genome biology 14: R89.

45. LaingR, KikuchiT, MartinelliA, TsaiIJ, BeechRN, et al. (2013) The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome biology 14: R88.

46. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13 : 2178–2189.

47. ElsworthB, JonesM, BlaxterM (2013) Badger–an accessible genome exploration environment. Bioinformatics 29 : 2788–2789.

48. KumarS, BlaxterML (2011) Simultaneous genome sequencing of symbionts and their hosts. Symbiosis 55 : 119–126.

49. AzizRK, BartelsD, BestAA, DeJonghM, DiszT, et al. (2008) The RAST Server: rapid annotations using subsystems technology. BMC genomics 9 : 75.

50. MilneI, BayerM, CardleL, ShawP, StephenG, et al. (2010) Tablet–next generation sequence assembly visualization. Bioinformatics 26 : 401–402.

51. KentBN, BordensteinSR (2010) Phage WO of Wolbachia: lambda of the endosymbiont world. Trends Microbiol 18 : 173–181.

52. KondoN, NikohN, IjichiN, ShimadaM, FukatsuT (2002) Genome fragment of Wolbachia endosymbiont transferred to X chromosome of host insect. Proc Natl Acad Sci U S A 99 : 14280–14285.

53. Dunning-HotoppJC, ClarkME, OliveiraDC, FosterJM, FischerP, et al. (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317 : 1753–1756.

54. GodelC, KumarS, KoutsovoulosG, LudinP, NilssonD, et al. (2012) The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 26 : 4650–4661.

55. HosokawaT, KogaR, KikuchiY, MengXY, FukatsuT (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences of the United States of America 107 : 769–774.

56. TsaiKH, HuangCG, WangLC, YuYW, WuWJ, et al. (2007) Molecular evidence for the endosymbiont Wolbachia in a non-filaroid nematode, Angiostrongylus cantonensis. Journal of biomedical science 14 : 607–615.

57. FosterJM, KumarS, FordL, JohnstonKL, BenR, et al. (2008) Absence of Wolbachia endobacteria in the non-filariid nematodes Angiostrongylus cantonensis and A. costaricensis. Parasites & vectors 1 : 31.

58. ThamsborgSM, BoaME, MakundiAE, KassukuAA (1998) Lungworm infection (Dictyocaulus viviparus) on dairy cattle farms in tropical highlands of Tanzania. Tropical animal health and production 30 : 93–96.

59. ChartierC (1990) [Dominant characteristics of helminth parasitism in cattle in Ituri (Haut-Zaire). I. The helminth fauna]. Rev Elev Med Vet Pays Trop 43 : 75–84.

60. Andrews S (2013) fastqc. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.

61. Aronesty E (2011) ea-utils: Command-line tools for processing biological sequencing data.

62. Brown CT, Howe A, Zhang Q, Pyrkosz AB, Brom TH (2012) A Reference-Free Algorithm for Computational Normalization of Shotgun Sequencing Data. arXiv q-bio: http://arxiv.org/abs/1203.4802.

63. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome research 18 : 821–829.

64. NadalinF, VezziF, PolicritiA (2012) GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics 13 Suppl 14: S8.

65. RanganathanS, NagarajSH, HuM, StrubeC, SchniederT, et al. (2007) A transcriptomic analysis of the adult stage of the bovine lungworm, Dictyocaulus viviparus. BMC genomics 8 : 311.

66. HarrisTW, BaranJ, BieriT, CabunocA, ChanJ, et al. (2013) WormBase 2014: new views of curated biology. Nucleic Acids Research 42: D789–793.

67. BoratynGM, CamachoC, CooperPS, CoulourisG, FongA, et al. (2013) BLAST: a more efficient report with usability improvements. Nucleic Acids Research 41: W29–33.

68. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 : 2688–2690.

69. RonquistF, TeslenkoM, van der MarkP, AyresDL, DarlingA, et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic biology 61 : 539–542.

70. LartillotN, LepageT, BlanquartS (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25 : 2286–2288.

71. LetunicI, BorkP (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Research 39: W475–478.

72. Rambaut A (2012) FigTree version 1.4. http://tree.bio.ed.ac.uk/software/figtree/.

73. PezzementiL, KrejciE, ChatonnetA, SelkirkME, MatthewsJB (2012) A tetrameric acetylcholinesterase from the parasitic nematode Dictyocaulus viviparus associates with the vertebrate tail proteins PRiMA and ColQ. Molecular and biochemical parasitology 181 : 40–48.

74. BlaxterML, De LeyP, GareyJR, LiuLX, ScheldemanP, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392 : 71–75.

75. FolmerO, BlackM, HoehW, LutzR, VrijenhoekR (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular marine biology and biotechnology 3 : 294–299.

76. KorfI (2004) Gene finding in novel genomes. BMC Bioinformatics 5 : 59.

77. LomsadzeA, Ter-HovhannisyanV, ChernoffYO, BorodovskyM (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Research 33 : 6494–6506.

78. EdgarRC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5 : 113.