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Tytuł artykułu

Helicosporidia: a genomic snapshot of an early transition to parasitism

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EN

Abstrakty

EN
Helicosporidia are gut parasites of invertebrates. These achlorophyllous, non-photosynthetic green algae are the first reported to infect insects. Helicosporidia are members of the green algal class Trebouxiophyceae and are further related to the photosynthetic and non-photosynthetic genera Auxenochlorella and Prototheca, respectively, the latter of which can also turn to parasitism under opportunistic conditions. Molecular analyses suggest that Helicosporidia diverged from other photosynthetic trebouxiophytes less than 200 million years ago and that its adaptation to parasitism is therefore recent. In this minireview, we summarize the current knowledge of helicosporidian genomics. Unlike many well-known parasitic lineages, the Helicosporidium sp. organelle and nuclear genomes have lost surprisingly little in terms of coding content aside from photosynthesis-related genes. While the small size of its nuclear genome compared to other sequenced trebouxiophycean representatives suggests that Helicosporidium is going through a streamlining process, this scenario cannot be ascertained at this stage. Genome expansions and contractions have occurred independently multiple times in the green algae, and the small size of the Helicosporidium genome may reflect a lack of expansion from a lean ancestor state rather than a tendency towards reduction.

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Tom

83

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4

Opis fizyczny

p.377-385,fig.,ref.

Twórcy

autor
  • Department of Biological and Chemical Sciences, Illinois Institute of Technology, Chicago, IL 60616, USA
  • Department of Biological and Chemical Sciences, Illinois Institute of Technology, Chicago, IL 60616, USA

Bibliografia

  • 1. Walker DM, Oghumu S, Gupta G, McGwire BS, Drew ME, Satoskar AR. Mechanisms of cellular invasion by intracellular parasites. CellMol Life Sci. 2014;71(7):1245–1263. http://dx.doi.org/10.1007/s00018-013-1491-1
  • 2. Jackson AP. Genome evolution in trypanosomatid parasites. Parasitology. 2014 (in press). http://dx.doi.org/10.1017/S0031182014000894
  • 3. Wijayawardena BK, Minchella DJ, DeWoody JA. Hosts, parasites, and horizontal gene transfer. Trends Parasitol. 2013;29(7):329–338. http://dx.doi.org/10.1016/j.pt.2013.05.001
  • 4. Corradi N, Selman M. Latest progress in microsporidian genome research. J Eukaryot Microbiol. 2013;60(3):309–312. http://dx.doi.org/10.1111/jeu.12030
  • 5. Raffaele S, Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nat Rev Microbiol. 2012;10:417–430.http://dx.doi.org/10.1038/nrmicro2790
  • 6. Blouin NA, Lane CE. Red algal parasites: models for a life history evolution that leaves photosynthesis behind again and again. Bioessays.2012;34(3):226–235. http://dx.doi.org/10.1002/bies.201100139
  • 7. Selman M, Pombert JF, Solter L, Farinelli L, Weiss LM, Keeling P, et al. Acquisition of an animal gene by microsporidian intracellular parasites.Curr Biol. 2011;21(15):R576–R577. http://dx.doi.org/10.1016/j.cub.2011.06.017
  • 8. Pombert JF, Selman M, Burki F, Bardell FT, Farinelli L, Solter LF, et al. Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites.Proc Natl Acad Sci USA. 2012;109(31):12638–12643. http://dx.doi. org/10.1073/pnas.1205020109
  • 9. Anderson MT, Seifert HS. Opportunity and means: horizontal gene transfer from the human host to a bacterial pathogen. mBio.2011;2(1):e00005–11. http://dx.doi.org/10.1128/mBio.00005-11
  • 10. Kishore SP, Stiller JW, Deitsch KW. Horizontal gene transfer of epigenetic machinery and evolution of parasitism in the malaria parasitePlasmodium falciparum and other apicomplexans. BMC Evol Biol.2013;13(1):37. http://dx.doi.org/10.1186/1471-2148-13-37
  • 11. Lee SC, Weiss LM, Heitman J. Generation of genetic diversity in microsporidia via sexual reproduction and horizontal gene transfer. Commun Integr Biol. 2009;2(5):414–417. http://dx.doi.org/10.4161/ cib.2.5.8846
  • 12. Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, Flannagan SE, et al. Genetic analysis of a high-level vancomycin-resistant isolateof Staphylococcus aureus. Science. 2003;302(5650):1569–1571. http://dx.doi.org/10.1126/science.1090956
  • 13. Nakabachi A, Nikoh N, Oshima K, Inoue H, Ohkuma M, Hongoh Y, et al. Horizontal gene acquisition of Liberibacter plant pathogens from a bacteriome-confined endosymbiont of their psyllid vector. PLoS ONE. 2013;8(12):e82612. http://dx.doi.org/10.1371/journal.pone.0082612
  • 14. Grant JR, Katz LA. Phylogenomic study indicates widespread lateral gene transfer in Entamoeba and suggests a past intimate relationshipwith parabasalids. Genome Biol Evol. 2014;6(9):2350–2360. http://dx.doi.org/10.1093/gbe/evu179
  • 15. Richards TA, Soanes DM, Jones MDM, Vasieva O, Leonard G, Paszkiewicz K, et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci USA. 2011;108(37):15258–15263. http://dx.doi.org/10.1073/ pnas.1105100108
  • 16. Gardiner DM, Kazan K, Manners JM. Cross-kingdom gene transfer facilitates the evolution of virulence in fungal pathogens. Plant Sci.2013;210:151–158. http://dx.doi.org/10.1016/j.plantsci.2013.06.002
  • 17. Soanes D, Richards TA. Horizontal gene transfer in eukaryotic plant pathogens. Annu Rev Phytopathol. 2014;52(1):583–614. http://dx.doi.org/10.1146/annurev-phyto-102313-050127
  • 18. Slamovits CH, Fast NM, Law JS, Keeling PJ. Genome compaction and stability in microsporidian intracellular parasites. Curr Biol.2004;14(10):891–896. http://dx.doi.org/10.1016/j.cub.2004.04.041
  • 19. Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, Becnel JJ, et al. Microsporidian genome analysis reveals evolutionary strategiesfor obligate intracellular growth. Genome Res. 2012;22(12):2478–2488.http://dx.doi.org/10.1101/gr.142802.112
  • 20. Burki F, Corradi N, Sierra R, Pawlowski J, Meyer GR, Abbott CL, et al. Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in rhizaria. Curr Biol. 2013;23(16):1541–1547. http://dx.doi.org/10.1016/j.cub.2013.06.033
  • 21. Rich SM, Xu G. Resolving the phylogeny of malaria parasites. Proc Natl Acad Sci USA. 2011;108(32):12973–12974. http://dx.doi.org/10.1073/pnas.1110141108
  • 22. Keeling P. Five questions about microsporidia. PLoS Pathog. 2009;5(9):e1000489. http://dx.doi.org/10.1371/journal.ppat.1000489
  • 23. Keilin D. On the life-history of Helicosporidium parasiticum, n.g., n.sp., a new type of protist parasitic in the larva of Dasyhelea obscura Winn.(Diptera, Ceratopogonidae) and in some other arthropods. Parasitology.1921;13(02):97. http://dx.doi.org/10.1017/S003118200001235X
  • 24. Boucias DG, Becnel JJ, White SE, Bott M. In vivo and in vitro development of the protist Helicosporidium sp. J Eukaryot Microbiol.2001;48(4):460–470. http://dx.doi.org/10.1111/j.1550-7408.2001.tb00180.x
  • 25. Tartar A, Boucias DG, Adams BJ, Becnel JJ. Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a greenalga (Chlorophyta). Int J Syst Evol Microbiol. 2002;52(1):273–279.
  • 26. Tartar A, Boucias DG, Becnel JJ, Adams BJ. Comparison of plastid 16S rRNA (rrn16) genes from Helicosporidium spp.: evidence supportingthe reclassification of Helicosporidia as green algae (Chlorophyta). Int JSyst Evol Microbiol. 2003;53(6):1719–1723. http://dx.doi.org/10.1099/ijs.0.02559-0
  • 27. de Koning AP, Keeling PJ. The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highlyreduced and structured. BMC Biol. 2006;4(1):12. http://dx.doi.org/10.1186/1741-7007-4-12
  • 28. Pombert JF, Keeling PJ. The mitochondrial genome of the entomoparasitic green alga Helicosporidium. PLoS ONE. 2010;5(1):e8954. http://dx.doi.org/10.1371/journal.pone.0008954
  • 29. de Koning AP, Keeling PJ. Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastidin a parasitic alga. Eukaryot Cell. 2004;3(5):1198–1205. http://dx.doi.org/10.1128/EC.3.5.1198-1205.2004
  • 30. de Koning A. Expressed sequence tag (EST) survey of the highly adapted green algal parasite, Helicosporidium. Protist. 2005;156(2):181– 190. http://dx.doi.org/10.1016/j.protis.2005.02.005
  • 31. Pombert JF, Blouin NA, Lane C, Boucias D, Keeling PJ. A lack of parasitic reduction in the obligate parasitic green alga Helicosporidium. PLoS Genet. 2014;10(5):e1004355. http://dx.doi.org/10.1371/journal.pgen.1004355
  • 32. Tartar A. The non-photosynthetic algae Helicosporidium spp.: emergence of a novel group of insect pathogens. Insects. 2013;4(3):375–391.http://dx.doi.org/10.3390/insects4030375
  • 33. Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, et al. Phylogeny and molecular evolution of the green algae. CritRev Plant Sci. 2012;31(1):1–46. http://dx.doi.org/10.1080/07352689.2011.615705
  • 34. Lass-Florl C, Mayr A. Human protothecosis. Clin Microbiol Rev. 2007;20(2):230–242. http://dx.doi.org/10.1128/CMR.00032-06
  • 35. de Wever A, Leliaert F, Verleyen E, Vanormelingen P, van der Gucht K, Hodgson DA, et al. Hidden levels of phylodiversity in Antarctic green algae: further evidence for the existence of glacial refugia. Proc Biol Sci.2009;276(1673):3591–3599. http://dx.doi.org/10.1098/rspb.2009.0994
  • 36. Hedges SB. The origin and evolution of model organisms. Nat Rev Genet. 2002;3(11):838–849. http://dx.doi.org/10.1038/nrg929
  • 37. Escalante AA, Ayala FJ. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci USA.1995;92(13):5793–5797. http://dx.doi.org/10.1073/pnas.92.13.5793
  • 38. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, et al. Genome sequence of the human malaria parasite Plasmodium falciparum.Nature. 2002;419(6906):498–511. http://dx.doi.org/10.1038/nature01097
  • 39. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N. Plastid in human parasites. Nature. 1996;381(6582):482–482. http://dx.doi. org/10.1038/381482a0
  • 40. Kohler S. A plastid of probable green algal origin in apicomplexan parasites. Science. 1997;275(5305):1485–1489. http://dx.doi.org/10.1126/science.275.5305.1485
  • 41. Lim L, McFadden GI. The evolution, metabolism and functions of the apicoplast. Philos Trans R Soc Lond B Biol Sci. 2010;365(1541):749–763. http://dx.doi.org/10.1098/rstb.2009.0273
  • 42. Nair SC, Striepen B. What do human parasites do with a chloroplast anyway? PLoS Biol. 2011;9(8):e1001137. http://dx.doi.org/10.1371/journal.pbio.1001137
  • 43. Mayorga J, Barba-Gómez JF, Verduzco-Martínez AP, Muñoz-Estrada VF, Welsh O. Protothecosis. Clin Dermatol. 2012;30(4):432–436. http://dx.doi.org/10.1016/j.clindermatol.2011.09.016
  • 44. Knauf U, Hachtel W. The genes encoding subunits of ATP synthase are conserved in the reduced plastid genome of the heterotrophic algaPrototheca wickerhamii. Mol Genet Genomics. 2002;267(4):492–497.http://dx.doi.org/10.1007/s00438-002-0681-6
  • 45. Makiuchi T, Nozaki T. Highly divergent mitochondrion-related organelles in anaerobic parasitic protozoa. Biochimie. 2014;100:3–17. http://dx.doi.org/10.1016/j.biochi.2013.11.018
  • 46. Martin WF, Müller M. Origin of mitochondria and hydrogenosomes. New York, NY: Springer; 2007.
  • 47. Goldberg AV, Molik S, Tsaousis AD, Neumann K, Kuhnke G, Delbac F, et al. Localization and functionality of microsporidian iron–sulphurcluster assembly proteins. Nature. 2008;452(7187):624–628. http://dx.doi.org/10.1038/nature06606
  • 48. Vávra J, Lukeš J. Microsporidia and “the art of living together”. In: Rollinson D, editor. . New York, NY: Elsevier; 2013. p. 253–319. (vol 82).
  • 49. Schneider RE, Brown MT, Shiflett AM, Dyall SD, Hayes RD, Xie Y, et al. The Trichomonas vaginalis hydrogenosome proteome ishighly reduced relative to mitochondria, yet complex compared withmitosomes. Int J Parasitol. 2011;41(13-14):1421–1434. http://dx.doi.org/10.1016/j.ijpara.2011.10.001
  • 50. Smith DR, Hamaji T, Olson BJSC, Durand PM, Ferris P, Michod RE, et al. Organelle genome complexity scales positively with organism size in volvocine green algae. Mol Biol Evol. 2013;30(4):793–797.http://dx.doi.org/10.1093/molbev/mst002
  • 51. Pombert JF, Otis C, Turmel M, Lemieux C. The mitochondrial genome of the prasinophyte Prasinoderma coloniale reveals two transspliced group I introns in the large subunit rRNA gene. PLoS ONE.2013;8(12):e84325. http://dx.doi.org/10.1371/journal.pone.0084325
  • 52. Kapraun DF. Nuclear DNA content estimates in green algal lineages: Chlorophyta and Streptophyta. Ann Bot. 2006;99(4):677–701. http:// dx.doi.org/10.1093/aob/mcl294
  • 53. Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, et al. Genome analysis of the smallest free-living eukaryoteOstreococcus tauri unveils many unique features. Proc Natl AcadSci USA. 2006;103(31):11647–11652. http://dx.doi.org/10.1073/pnas.0604795103
  • 54. Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, et al. Genomic analysis of organismal complexity in the multicellulargreen alga Volvox carteri. Science. 2010;329(5988):223–226. http://dx.doi.org/10.1126/science.1188800
  • 55. Godman J, Balk J. Genome analysis of Chlamydomonas reinhardtii reveals the existence of multiple, compartmentalized iron-sulfur proteinassembly machineries of different evolutionary origins. Genetics.2008;179(1):59–68. http://dx.doi.org/10.1534/genetics.107.086033
  • 56. Yandell M, Ence D. A beginner’s guide to eukaryotic genome annotation. Nat Rev Genet. 2012;13(5):329–342. http://dx.doi.org/10.1038/nrg3174
  • 57. Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD, et al. The genome of the polar eukaryotic microalga Coccomyxasubellipsoidea reveals traits of cold adaptation. Genome Biol.2012;13(5):R39. http://dx.doi.org/10.1186/gb-2012-13-5-r39
  • 58. Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, et al. The Chlorella variabilis NC64A genome reveals adaptation tophotosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell.2010;22(9):2943–2955. http://dx.doi.org/10.1105/tpc.110.076406
  • 59. Chung WJ, Okamura K, Martin R, Lai EC. Endogenous RNA interference provides a somatic defense against Drosophila transposons. Curr Biol. 2008;18(11):795–802. http://dx.doi.org/10.1016/j.cub.2008.05.006
  • 60. Gao C, Wang Y, Shen Y, Yan D, He X, Dai J, et al. Oil accumulation mechanisms of the oleaginous microalga Chlorella protothecoidesrevealed through its genome, transcriptomes, and proteomes. BMC Genomics.2014;15(1):582. http://dx.doi.org/10.1186/1471-2164-15-582
  • 61. Kapraun DF. Nuclear DNA content estimates in multicellular green, red and brown algae: phylogenetic considerations. Ann Bot. 2005;95(1):7–44. http://dx.doi.org/10.1093/aob/mci002
  • 62. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel . New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol.2010;59(3):307–321. http://dx.doi.org/10.1093/sysbio/syq010
  • 63. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27(2):221–224. http://dx.doi.org/10.1093/molbev/msp259

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