Helicosporidia: a genomic snapshot of an early transition to parasitism
Abstract
Keywords
Full Text:
PDFReferences
Walker DM, Oghumu S, Gupta G, McGwire BS, Drew ME, Satoskar AR. Mechanisms of cellular invasion by intracellular parasites. Cell Mol Life Sci. 2014;71(7):1245–1263. http://dx.doi.org/10.1007/s00018-013-1491-1
Jackson AP. Genome evolution in trypanosomatid parasites. Parasitology. 2014 (in press). http://dx.doi.org/10.1017/S0031182014000894
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
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
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
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
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
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
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
Kishore SP, Stiller JW, Deitsch KW. Horizontal gene transfer of epigenetic machinery and evolution of parasitism in the malaria parasite Plasmodium falciparum and other apicomplexans. BMC Evol Biol. 2013;13(1):37. http://dx.doi.org/10.1186/1471-2148-13-37
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
Weigel LM, Clewell DB, Gill SR, Clark NC, McDougal LK, Flannagan SE, et al. Genetic analysis of a high-level vancomycin-resistant isolate of Staphylococcus aureus. Science. 2003;302(5650):1569–1571. http://dx.doi.org/10.1126/science.1090956
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
Grant JR, Katz LA. Phylogenomic study indicates widespread lateral gene transfer in Entamoeba and suggests a past intimate relationship with parabasalids. Genome Biol Evol. 2014;6(9):2350–2360. http://dx.doi.org/10.1093/gbe/evu179
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
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
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
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
Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, Becnel JJ, et al. Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res. 2012;22(12):2478–2488. http://dx.doi.org/10.1101/gr.142802.112
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
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
Keeling P. Five questions about microsporidia. PLoS Pathog. 2009;5(9):e1000489. http://dx.doi.org/10.1371/journal.ppat.1000489
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
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
Tartar A, Boucias DG, Adams BJ, Becnel JJ. Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a green alga (Chlorophyta). Int J Syst Evol Microbiol. 2002;52(1):273–279.
Tartar A, Boucias DG, Becnel JJ, Adams BJ. 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. 2003;53(6):1719–1723. http://dx.doi.org/10.1099/ijs.0.02559-0
de Koning AP, Keeling PJ. The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol. 2006;4(1):12. http://dx.doi.org/10.1186/1741-7007-4-12
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
de Koning AP, Keeling PJ. Nucleus-encoded genes for plastid-targeted proteins in Helicosporidium: functional diversity of a cryptic plastid in a parasitic alga. Eukaryot Cell. 2004;3(5):1198–1205. http://dx.doi.org/10.1128/EC.3.5.1198-1205.2004
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
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
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
Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, et al. Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci. 2012;31(1):1–46. http://dx.doi.org/10.1080/07352689.2011.615705
Lass-Florl C, Mayr A. Human protothecosis. Clin Microbiol Rev. 2007;20(2):230–242. http://dx.doi.org/10.1128/CMR.00032-06
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
Hedges SB. The origin and evolution of model organisms. Nat Rev Genet. 2002;3(11):838–849. http://dx.doi.org/10.1038/nrg929
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
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
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
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
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
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
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
Knauf U, Hachtel W. The genes encoding subunits of ATP synthase are conserved in the reduced plastid genome of the heterotrophic alga Prototheca wickerhamii. Mol Genet Genomics. 2002;267(4):492–497. http://dx.doi.org/10.1007/s00438-002-0681-6
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
Martin WF, Müller M. Origin of mitochondria and hydrogenosomes. New York, NY: Springer; 2007.
Goldberg AV, Molik S, Tsaousis AD, Neumann K, Kuhnke G, Delbac F, et al. Localization and functionality of microsporidian iron–sulphur cluster assembly proteins. Nature. 2008;452(7187):624–628. http://dx.doi.org/10.1038/nature06606
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).
Schneider RE, Brown MT, Shiflett AM, Dyall SD, Hayes RD, Xie Y, et al. The Trichomonas vaginalis hydrogenosome proteome is highly reduced relative to mitochondria, yet complex compared with mitosomes. Int J Parasitol. 2011;41(13-14):1421–1434. http://dx.doi.org/10.1016/j.ijpara.2011.10.001
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
Pombert JF, Otis C, Turmel M, Lemieux C. The mitochondrial genome of the prasinophyte Prasinoderma coloniale reveals two trans-spliced group I introns in the large subunit rRNA gene. PLoS ONE. 2013;8(12):e84325. http://dx.doi.org/10.1371/journal.pone.0084325
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
Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, Robbens S, et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci USA. 2006;103(31):11647–11652. http://dx.doi.org/10.1073/pnas.0604795103
Prochnik SE, Umen J, Nedelcu AM, Hallmann A, Miller SM, Nishii I, et al. Genomic analysis of organismal complexity in the multicellular green alga Volvox carteri. Science. 2010;329(5988):223–226. http://dx.doi.org/10.1126/science.1188800
Godman J, Balk J. Genome analysis of Chlamydomonas reinhardtii reveals the existence of multiple, compartmentalized iron-sulfur protein assembly machineries of different evolutionary origins. Genetics. 2008;179(1):59–68. http://dx.doi.org/10.1534/genetics.107.086033
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
Blanc G, Agarkova I, Grimwood J, Kuo A, Brueggeman A, Dunigan DD, et al. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol. 2012;13(5):R39. http://dx.doi.org/10.1186/gb-2012-13-5-r39
Blanc G, Duncan G, Agarkova I, Borodovsky M, Gurnon J, Kuo A, et al. The Chlorella variabilis NC64A genome reveals adaptation to photosymbiosis, coevolution with viruses, and cryptic sex. Plant Cell. 2010;22(9):2943–2955. http://dx.doi.org/10.1105/tpc.110.076406
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
Gao C, Wang Y, Shen Y, Yan D, He X, Dai J, et al. Oil accumulation mechanisms of the oleaginous microalga Chlorella protothecoides revealed through its genome, transcriptomes, and proteomes. BMC Genomics. 2014;15(1):582. http://dx.doi.org/10.1186/1471-2164-15-582
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
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 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
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
DOI: https://doi.org/10.5586/asbp.2014.039
|
|
|