A Lack of Parasitic Reduction in the Obligate Parasitic Green Alga

English version České info

Helicosporidium is a highly-adapted obligate parasite of animals. Its evolutionary origins were unclear for almost a century, but molecular analysis ultimately and surprisingly showed that it is a green alga, which means it has undergone an evolutionary transition from autotrophy to parasitism comparable to that of the malaria parasite Plasmodium and its relatives. Such transitions are often associated with the loss of biological functions that are no longer necessary in their novel environment and with the development of molecular mechanisms, sometimes quite sophisticated, to invade and take advantage of their hosts. Yet, very little is actually known about the early stages of the transition of a free-living organism to an obligate intracellular parasite. Here we sequenced the genome and transcriptome of Helicosporidium, and use it to show that the outcome of this transition is quite different from that of Plasmodium.

Vyšlo v časopise: A Lack of Parasitic Reduction in the Obligate Parasitic Green Alga. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004355
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004355

Souhrn

Zdroje

1. BouciasDG, BecnelJJ, WhiteSE, BottM (2001) In vivo and in vitro development of the protist Helicosporidium sp. J Eukaryot Microbiol 48 : 460–470.

2. TartarA (2013) The non-photosynthetic algae Helicosporidium spp.: Emergence of a novel group of insect pathogens. Insects 4 : 375–391.

3. BläskeV-U, BouciasDG (2004) Influence of Helicosporidium spp. (Chlorophyta: Trebouxiophyceae) infection on the development and survival of three noctuid species. Environ Entomol 33 : 54–61.

4. ConklinT, BläskeV-U, BecnelJJ, BouciasDG (2005) Infectivity of two isolates of Helicosporidium spp. (Chlorophyta: Trebouxiophyceae) in heterologous host insects. Florida Entomol 88 : 431–440.

5. Bläske-LietzeV-U, BouciasDG (2005) Pathogenesis of Helicosporidium sp. (Chlorophyta: Trebouxiophyceae) in susceptible noctuid larvae. J Invertebr Pathol 90 : 161–168.

6. Bläske-LietzeV-U, ShapiroAM, DentonJS, BottsM, BecnelJJ, et al. (2006) Development of the insect pathogenic alga Helicosporidium. J Eukaryot Microbiol 53 : 165–176.

7. TartarA, BouciasDG, AdamsBJ, BecnelJJ (2002) Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a green alga (Chlorophyta). Int J Syst Evol Microbiol 52 : 273–279.

8. TartarA, BouciasDG, BecnelJJ, AdamsBJ (2003) Comparison of plastid 16S rRNA (rrn16) genes from Helicosporidium spp.: evidence supporting the reclassification of Helicosporidia as green algae (Chlorophyta). Int J Syst Evol Microbiol 53 : 1719–1723.

9. KeelingPJ, SlamovitsCH (2005) Causes and effects of nuclear genome reduction. Curr Opin Genet Dev 15 : 601–608.

10. BlouinNA, LaneCE (2012) Red algal parasites: models for a life history evolution that leaves photosynthesis behind again and again. Bioessays 34 : 226–235.

11. JanouškovecJ, HorákA, OborníkM, LukešJ, KeelingPJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107 : 10949–10954.

12. EscalanteAA, AyalaFJ (1995) Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci U S A 92 : 5793–5797.

13. LeliaertF, SmithDR, MoreauH, HerronMD, VerbruggenH, et al. (2012) Phylogeny and molecular evolution of the green algae. CRC Crit Rev Plant Sci 31 : 1–46.

14. De WeverA, LeliaertF, VerleyenE, VanormelingenP, Van der GuchtK, et al. (2009) Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc Biol Sci 276 : 3591–3599.

15. TartarA, BouciasDG (2004) The non-photosynthetic, pathogenic green alga Helicosporidium sp. has retained a modified, functional plastid genome. FEMS Microbiol Lett 233 : 153–157.

16. BlancG, AgarkovaI, GrimwoodJ, KuoA, BrueggemanA, et al. (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13: R39.

17. BlancG, DuncanG, AgarkovaI, BorodovskyM, GurnonJ, et al. (2010) The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell 22 : 2943–2955.

18. Tartar A (2004) Incertae sedis no more: The phylogenetic affinity of Helicosporidia University of Florida.

19. KarpowiczSJ, ProchnikSE, GrossmanAR, MerchantSS (2011) The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J Biol Chem 286 : 21427–21439.

20. De KoningAP, KeelingPJ (2006) The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol 4 : 12.

21. GodmanJ, BalkJ (2008) Genome analysis of Chlamydomonas reinhardtii reveals the existence of multiple, compartmentalized iron-sulfur protein assembly machineries of different evolutionary origins. Genetics 179 : 59–68.

22. Dellibovi-RaghebTa, GisselbergJE, PriggeST (2013) Parasites FeS up: iron-sulfur cluster biogenesis in eukaryotic pathogens. PLoS Pathog 9: e1003227.

23. CeruttiH, MaX, MsanneJ, RepasT (2011) RNA-mediated silencing in Algae: biological roles and tools for analysis of gene function. Eukaryot Cell 10 : 1164–1172.

24. Casas-MollanoJA, RohrJ, KimE-J, BalassaE, van DijkK, et al. (2008) Diversification of the core RNA interference machinery in Chlamydomonas reinhardtii and the role of DCL1 in transposon silencing. Genetics 179 : 69–81.

25. HalaryS, McInerneyJO, LopezP, BaptesteE (2013) EGN: a wizard for construction of gene and genome similarity networks. BMC Evol Biol 13 : 146.

26. KapaunE, ReisserW (1995) A chitin-like glycan in the cell wall of a Chlorella sp. (Chlorococcales, Chlorophyceae). 197 : 577–582.

27. ZhuQ, ArakaneY, BeemanRW, KramerKJ, MuthukrishnanS (2008) Characterization of recombinant chitinase-like proteins of Drosophila melanogaster and Tribolium castaneum. Insect Biochem Mol Biol 38 : 467–477.

28. KhajuriaC, BuschmanLL, ChenM-S, MuthukrishnanS, ZhuKY (2010) A gut-specific chitinase gene essential for regulation of chitin content of peritrophic matrix and growth of Ostrinia nubilalis larvae. Insect Biochem Mol Biol 40 : 621–629.

29. WatanabeT, KoboriK, MiyashitaK, FujiinT, SakaiH, et al. (1993) Identification of glutamic acid 204 and aspartic acid 200 in chitinase A1 of Bacillus circulans WL-12 as essential residues for chitinase activity. J Biol Chem 268 : 18567–18572.

30. Parakkottil ChothiM, DuncanGA, ArmirottiA, AbergelC, GurnonJR, et al. (2010) Identification of an L-rhamnose synthetic pathway in two nucleocytoplasmic large DNA viruses. J Virol 84 : 8829–8838.

31. JeanniardA, DuniganDD, GurnonJR, Agarkova IV, KangM, et al. (2013) Towards defining the chloroviruses: a genomic journey through a genus of large DNA viruses. BMC Genomics 14 : 158.

32. PombertJ-F, SelmanM, BurkiF, BardellFT, FarinelliL, et al. (2012) Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc Natl Acad Sci U S A 109 : 12638–12643.

33. DerelleE, FerrazC, RombautsS, RouzéP, WordenAZ, et al. (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA 103 : 11647–11652.

34. WordenAZ, LeeJ, MockT, RouzéP, SimmonsMP, et al. (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science (80-) 324 : 268–272.

35. PalenikB, GrimwoodJ, AertsA, RouzéP, SalamovA, et al. (2007) The tiny eukaryote Ostreococcus provides genomic insights into the paradox of plankton speciation. Proc Natl Acad Sci U S A 104 : 7705–7710.

36. ShenZ, Jacobs-LorenaM (1997) Characterization of a novel gut-specific chitinase gene from the human malaria vector Anopheles gambiae. J Biol Chem 272 : 28895–28900.

37. VinetzJM, ValenzuelaJG, SpechtCA, AravindL, LangerRC, et al. (2000) Chitinases of the avian malaria parasite Plasmodium gallinaceum, a class of enzymes necessary for parasite invasion of the mosquito midgut. J Biol Chem 275 : 10331–10341.

38. ShahabuddinM, ToyoshimaT, AikawaM, KaslowDC (1993) Transmission-blocking activity of a chitinase inhibitor and activation of malarial parasite chitinase by mosquito protease. Proc Natl Acad Sci U S A 90 : 4266–4270.

39. BoisvertS, LavioletteF, CorbeilJ (2010) Ray: Simultaneous assembly of reads from a mix of high-throughput sequencing technologies. J Comput Biol 17 : 1519–1533.

40. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic Local Alignment Search Tool. J Mol Biol 215 : 403–410.

41. PombertJ-F, KeelingPJ (2010) The mitochondrial genome of the entomoparasitic green alga Helicosporidium. PLoS One 5: e8954.

42. RiceP, LongdenI, BleasbyA (2000) EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16 : 276–277.

43. WuTD, WatanabeCK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21 : 1859–1875.

44. CantarelBL, KorfI, RobbSMC, ParraG, RossE, et al. (2008) MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res 18 : 188–196.

45. HoltC, YandellM (2011) MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. BMC Bioinformatics 12 : 491.

46. StankeM, DiekhansM, BaertschR, HausslerD (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24 : 637–644.

47. JurkaJ, KapitonovVV, PavlicekA, KlonowskiP, KohanyO, et al. (2005) Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 110 : 462–467.

48. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

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

50. KanehisaM, GotoS, FurumichiM, TanabeM, HirakawaM (2010) KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38: D355–360.

51. KanehisaM, GotoS, SatoY, FurumichiM, TanabeM (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40: D109–114.

52. QuevillonE, SilventoinenV, PillaiS, HarteN, MulderN, et al. (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33: W116–W120.

53. LetunicI, DoerksT, BorkP (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40: D302–D305.

54. RechsteinerM, RogersSW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21 : 267–271.

55. EmanuelssonO, NielsenH, BrunakS, von HeijneG (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300 : 1005–1016.

56. TardifM, AtteiaA, SpechtM, CogneG, RollandN, et al. (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29 : 3625–3639.

57. KatohK, StandleyDM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30 : 772–780.

58. DarribaD, TaboadaGL, DoalloR, PosadaD (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27 : 1164–1165.

59. GuindonS, DufayardJ-F, LefortV, AnisimovaM, HordijkW, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59 : 307–321.

60. LeSQ, GascuelO (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25 : 1307–1320.

61. KapraunDF (2007) Nuclear DNA content estimates in green algal lineages: Chlorophyta and Streptophyta. Ann Bot 99 : 677–701.

62. KapraunDF (2005) Nuclear DNA content estimates in multicellular green, red and brown algae: phylogenetic considerations. Ann Bot 95 : 7–44.