Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 33, 2015, Pages 10200-10207

  Janouškovec, Jan ^a,b   Tikhonenkov, Denis V ^a,c   Burki, Fabien ^a   Howe, Alexis T ^a   Kolísko, Martin ^a   Mylnikov, Alexander P ^c   Keeling, Patrick J ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^c PAPANIN INSTITUTE FOR BIOLOGY OF INLAND WATERS   (Russian Federation)

Author keywords

Apicomplexa; Chromera; Colpodella; Parasitism origin; Plastid organelle

Indexed keywords

ISOPRENOID; TRANSCRIPTOME; RIBOSOME DNA;

APICOMPLEXA; APICOPLAST; ARTICLE; BIOSYNTHESIS; DINOFLAGELLATE; MONOPHYLY; NONHUMAN; PARASITISM; PHOTOSYNTHESIS; PLASTID GENOME; PRIORITY JOURNAL; SISTER GROUP; ANIMAL; BACTERIAL GENE; BAYES THEOREM; BIOLOGY; CELL LINEAGE; CYTOSOL; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITE; PHYLOGENY; PHYSIOLOGY; PLASTID; STATISTICAL MODEL;

APICOMPLEXA; COLPODELLA; COLPODELLIDAE; DINOPHYCEAE;

ANIMALS; APICOMPLEXA; APICOPLASTS; BASE SEQUENCE; BAYES THEOREM; CELL LINEAGE; COMPUTATIONAL BIOLOGY; CYTOSOL; DNA, RIBOSOMAL; GENES, BACTERIAL; GENOME; LIKELIHOOD FUNCTIONS; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; PARASITES; PHOTOSYNTHESIS; PHYLOGENY; PLASTIDS;

EID: 84939790330     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1423790112     Document Type: Article

References (50)

1. Moore RB, et al. (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451(7181):959-963.
2. Simpson AGB, Patterson DJ (1996) Ultrastructure and identification of the predatory flagellate Colpodella pugnax Cienkowski (Apicomplexa) with a description of Colpodella turpis n. sp. and a review of the genus. Syst Parasitol 33(3):187-198.
3. Oborník M, et al. (2012) Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist 163(2):306-323.
4. Cavalier-Smith T, Chao EE (2004) Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur J Protistol 40(3):185-212.
5. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N (1996) Plastid in human parasites. Nature 381(6582):482.
6. Wilson RJ, et al. (1996) Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. J Mol Biol 261(2):155-172.
7. Janouškovec J, Horák A, Oborník M, Lukeš J, Keeling PJ (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci USA 107(24):10949-10954.
8. Bodył A, Stiller JW, Mackiewicz P (2009) Chromalveolate plastids: Direct descent or multiple endosymbioses? Trends Ecol Evol 24(3):119-121, author reply 121-122.
9. Janouškovec J, Horák A, Barott KL, Rohwer FL, Keeling PJ (2012) Global analysis of plastid diversity reveals apicomplexan-related lineages in coral reefs. Curr Biol 22(13):R518-R519.
10. Gile GH, Slamovits CH (2014) Transcriptomic analysis reveals evidence for a cryptic plastid in the colpodellid Voromonas pontica, a close relative of chromerids and apicomplexan parasites. PLoS ONE 9(5):e96258.
11. Mylnikov A, Mylnikova Z (2008) Feeding spectra and pseudoconoid structure in predatory alveolate flagellates. Inland Water Biol 1(3):210-216.
12. Oborník M, et al. (2011) Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of apicomplexa, Chromera velia. Protist 162(1):115-130.
13. Tikhonenkov DV, et al. (2014) Description of Colponema vietnamica sp.n. and Acavomonas peruviana n. gen. n. sp., two new alveolate phyla (Colponemidia nom. nov. and Acavomonidia nom. nov.) and their contributions to reconstructing the ancestral state of alveolates and eukaryotes. PLoS ONE 9(4):e95467.
14. Wasmuth J, Daub J, Peregrín-Alvarez JM, Finney CAM, Parkinson J (2009) The origins of apicomplexan sequence innovation. Genome Res 19(7):1202-1213.
15. Huang J, et al. (2004) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol 5(11):R88.
16. Yuan CL, et al. (2012) Colpodella spp.-like parasite infection in woman, China. Emerg Infect Dis 18(1):125-127.
17. Burki F, Okamoto N, Pombert J-F, Keeling PJ (2012) The evolutionary history of haptophytes and cryptophytes: Phylogenomic evidence for separate origins. Proc Biol Sci 279(1736):2246-2254.
18. Ralph SA, et al. (2004) Tropical infectious diseases: Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2(3):203-216.
19. Seeber F, Soldati-Favre D (2010) Metabolic pathways in the apicoplast of apicomplexa. International Review of Cell and Molecular Biology (Elsevier), 161-228. Available at linkinghub. elsevier.com/retrieve/articleSelectSinglePerm?Redirect=www.sciencedirect.com/science/article/pii/S1937644810810056?via%3Dihub&key=ab8c9b9be510bed9d51196fc9df26ca6a3ef88cd. Accessed September 1, 2014.
20. Abrahamsen MS, et al. (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304(5669):441-445.
21. Yeh E, DeRisi JL (2011) Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol 9(8):e1001138.
22. Butterfield ER, Howe CJ, Nisbet RER (2013) An analysis of dinoflagellate metabolism using EST data. Protist 164(2):218-236.
23. Kořený L, Sobotka R, Janouškovec J, Keeling PJ, Oborník M (2011) Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell 23(9):3454-3462.
24. Vaughan AM, et al. (2009) Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell Microbiol 11(3):506-520.
25. van Dooren GG, Kennedy AT, McFadden GI (2012) The use and abuse of heme in apicomplexan parasites. Antioxid Redox Signal 17(4):634-656.
26. Zhu G, Marchewka MJ, Woods KM, Upton SJ, Keithly JS (2000) Molecular analysis of a Type I fatty acid synthase in Cryptosporidium parvum. Mol Biochem Parasitol 105(2):253-260.
27. Mazumdar J, Striepen B (2007) Make it or take it: Fatty acid metabolism of apicomplexan parasites. Eukaryot Cell 6(10):1727-1735.
28. Li Z-H, Ramakrishnan S, Striepen B, Moreno SNJ (2013) Toxoplasma gondii relies on both host and parasite isoprenoids and can be rendered sensitive to atorvastatin. PLoS Pathog 9(10):e1003665.
29. Dellibovi-Ragheb TA, Gisselberg JE, Prigge ST (2013) Parasites FeS up: Iron-sulfur cluster biogenesis in eukaryotic pathogens. PLoS Pathog 9(4):e1003227.
30. Barbrook AC, Howe CJ, Purton S (2006) Why are plastid genomes retained in nonphotosynthetic organisms? Trends Plant Sci 11(2):101-108.
31. Smith DR, Lee RW (2014) A plastid without a genome: Evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol 164(4):1812-1819.
32. El Bakkouri M, et al. (2010) The Clp chaperones and proteases of the human malaria parasite Plasmodium falciparum. J Mol Biol 404(3):456-477.
33. Pino P, et al. (2010) Mitochondrial translation in absence of local tRNA aminoacylation and methionyl tRNA Met formylation in Apicomplexa. Mol Microbiol 76(3):706-718.
34. Goodman CD, McFadden GI (2014) Ycf93 (Orf105), a small apicoplast-encoded membrane protein in the relict plastid of the malaria parasite Plasmodium falciparum that is conserved in Apicomplexa. PLoS ONE 9(4):e91178.
35. Chen F, Mackey AJ, Stoeckert CJ, Jr, Roos DS (2006) OrthoMCL-DB: Querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34(Database issue):D363-D368.
36. de Leon JC, et al. (2013) A SAS-6-like protein suggests that the Toxoplasma conoid complex evolved from flagellar components. Eukaryot Cell 12(7):1009-1019.
37. Okamoto N, Keeling PJ (2014) The 3D structure of the apical complex and association with the flagellar apparatus revealed by serial TEM tomography in Psammosa pacifica, a distant relative of the Apicomplexa. PLoS ONE 9(1):e84653.
38. Seow F, et al. (2005) The plastidic DNA replication enzyme complex of Plasmodium falciparum. Mol Biochem Parasitol 141(2):145-153.
39. Munro JB, Jacob CG, Silva JC (2013) A novel clade of unique eukaryotic ribonucleotide reductase R2 subunits is exclusive to apicomplexan parasites. J Mol Evol 77(3):92-106.
40. Lagal V, et al. (2010) Toxoplasma gondii protease TgSUB1 is required for cell surface processing of micronemal adhesive complexes and efficient adhesion of tachyzoites. Cell Microbiol 12(12):1792-1808.
41. Bullen HE, et al. (2009) A novel family of Apicomplexan glideosome-associated proteins with an inner membrane-anchoring role. J Biol Chem 284(37):25353-25363.
42. Gordon JL, Buguliskis JS, Buske PJ, Sibley LD (2010) Actin-like protein 1 (ALP1) is a component of dynamic, high molecular weight complexes in Toxoplasma gondii. Cytoskeleton (Hoboken) 67(1):23-31.
43. Beck JR, et al. (2010) A novel family of Toxoplasma IMC proteins displays a hierarchical organization and functions in coordinating parasite division. PLoS Pathog 6(9):e1001094.
44. Mylnikov AP (2009) Ultrastructure and phylogeny of colpodellids (Colpodellida, Alveolata). Biol Bull 36(6):582-590.
45. Templeton TJ, et al. (2004) The Cryptosporidium oocyst wall protein is a member of a multigene family and has a homolog in Toxoplasma. Infect Immun 72(2):980-987.
46. Bushkin GG, et al. (2013) Evidence for a structural role for acid-fast lipids in oocyst walls of Cryptosporidium, Toxoplasma, and Eimeria. MBio 4(5):e00387-13.
47. Dorrell RG, Drew J, Nisbet RER, Howe CJ (2014) Evolution of chloroplast transcript processing in Plasmodium and its chromerid algal relatives. PLoS Genet 10(1):e1004008.
48. Briggs LJ, Davidge JA, Wickstead B, Ginger ML, Gull K (2004) More than one way to build a flagellum: Comparative genomics of parasitic protozoa. Curr Biol 14(15):R611-R612.
49. Tomavo S, Slomianny C, Meissner M, Carruthers VB (2013) Protein trafficking through the endosomal system prepares intracellular parasites for a home invasion. PLoS Pathog 9(10):e1003629.
50. Sloves P-J, et al. (2012) Toxoplasma sortilin-like receptor regulates protein transport and is essential for apical secretory organelle biogenesis and host infection. Cell Host Microbe 11(5):515-527.