Skip to main content
×
×
Home

Eukaryotic systematics: a user's guide for cell biologists and parasitologists

  • GISELLE WALKER (a1), RICHARD G. DORRELL (a2), ALEXANDER SCHLACHT (a3) and JOEL B. DACKS (a3)
Summary
SUMMARY

Single-celled parasites like Entamoeba, Trypanosoma, Phytophthora and Plasmodium wreak untold havoc on human habitat and health. Understanding the position of the various protistan pathogens in the larger context of eukaryotic diversity informs our study of how these parasites operate on a cellular level, as well as how they have evolved. Here, we review the literature that has brought our understanding of eukaryotic relationships from an idea of parasites as primitive cells to a crystallized view of diversity that encompasses 6 major divisions, or supergroups, of eukaryotes. We provide an updated taxonomic scheme (for 2011), based on extensive genomic, ultrastructural and phylogenetic evidence, with three differing levels of taxonomic detail for ease of referencing and accessibility (see supplementary material at Cambridge Journals On-line). Two of the most pressing issues in cellular evolution, the root of the eukaryotic tree and the evolution of photosynthesis in complex algae, are also discussed along with ideas about what the new generation of genome sequencing technologies may contribute to the field of eukaryotic systematics. We hope that, armed with this user's guide, cell biologists and parasitologists will be encouraged about taking an increasingly evolutionary point of view in the battle against parasites representing real dangers to our livelihoods and lives.

Copyright
Corresponding author
*To whom correspondence should be addressed: Department of Cell Biology, School of Molecular and Systems Medicine, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada, T6 G 2H7. Tel: +1-780-248-1493. Fax: +1-780-492-0450. E-mail: dacks@ualberta.ca.
Department of Anatomy and Structural Biology, University of Otago, P.O. Box 56, Dunedin 9054, New Zealand. E-mails: gw265@cam.ac.uk; giselle.walker@anatomy.otago.ac.nz.
References
Hide All
Adl S. M., Simpson A. G., Farmer M. A., Andersen R. A., Anderson O. R., Barta J. R., Bowser S. S., Brugerolle G., Fensome R. A., Fredericq S., James T. Y., Karpov S., Kugrens P., Krug J., Lane C. E., Lewis L. A., Lodge J., Lynn D. H., Mann D. G., Mccourt R. M., Mendoza L., Moestrup O., Mozley-Standridge S. E., Nerad T. A., Shearer C. A., Smirnov A. V., Spiegel F. W. and Taylor M. F. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology 52, 399451.
Andersen R. A. (2004). Biology and systematics of the heterokont and haptophyte algae. American Journal of Botany 91, 15081522.
Bapteste E., Brinkmann H., Lee J. A., Moore D. V., Sensen C. W., Gordon P., Durufle L., Gaasterland T., Lopez P., Muller M. and Philippe H. (2002). The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proceedings of the National Academy of Sciences, USA 99, 14141419.
Bass D., Chao E. E., Nikolaev S., Yabuki A., Ishida K., Berney C., Pakzad U., Wylezich C. and Cavalier-Smith T. (2009). Phylogeny of novel naked Filose and Reticulose Cercozoa: Granofilosea cl. n. and Proteomyxidea revised. Protist 160, 75109.
Baurain D., Brinkmann H., Petersen J., Rodriguez-Ezpeleta N., Stechmann A., Demoulin V., Roger A. J., Burger G., Lang B. F. and Philippe H. (2010). Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Molecular Biology and Evolution 27, 16981709.
Becker B. and Marin B. (2009). Streptophyte algae and the origin of embryophytes. Annals of Botany 103, 9991004.
Bodyl A., Mackiewicz P. and Stiller J. W. (2009). Early steps in plastid evolution: current ideas and controversies. Bioessays 31, 12191232.
Brinkmann H., Van Der Giezen M., Zhou Y., Poncelin De Raucourt G. and Philippe H. (2005). An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Systematic Biology 54, 743757.
Brown M. W., Spiegel F. W. and Silberman J. D. (2009). Phylogeny of the “forgotten” cellular slime mold, Fonticula alba, reveals a key evolutionary branch within Opisthokonta. Molecular Biology and Evolution 26, 26992709.
Brugerolle G., Bricheux G., Philippe H. and Coffea G. (2002). Collodictyon triciliatum and Diphylleia rotans (=Aulacomonas submarina) form a new family of flagellates (Collodictyonidae) with tubular mitochondrial cristae that is phylogenetically distant from other flagellate groups. Protist 153, 5970.
Bui E. T., Bradley P. J. and Johnson P. J. (1996). A common evolutionary origin for mitochondria and hydrogenosomes. Proceedings of the National Academy of Sciences, USA 93, 96519656.
Burki F., Inagaki Y., Brate J., Archibald J. M., Keeling P. J., Cavalier-Smith T., Sakaguchi M., Hashimoto T., Horak A., Kumar S., Klaveness D., Jakobsen K. S., Pawlowski J. and Shalchian-Tabrizi K. (2009). Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, Telonemia and Centroheliozoa, are related to photosynthetic chromalveolates. Genome Biology and Evolution 1, 231238.
Burki F., Shalchian-Tabrizi K., Minge M., Skjaeveland A., Nikolaev S. I., Jakobsen K. S. and Pawlowski J. (2007). Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2, e790.
Burki F., Shalchian-Tabrizi K. and Pawlowski J. (2008). Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes. Biology Letters 4, 366369.
Cantacessi C., Mitreva M., Campbell B. E., Hall R. S., Young N. D., Jex A. R., Ranganathan S. and Gasser R. B. (2010 a). First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infection Genetics and Evolution 10, 11991207.
Cantacessi C., Mitreva M., Jex A. R., Young N. D., Campbell B. E., Hall R. S., Doyle M. A., Ralph S. A., Rabelo E. M., Ranganathan S., Sternberg P. W., Loukas A. and Gasser R. B. (2010 b). Massively parallel sequencing and analysis of the Necator americanus transcriptome. PLoS Neglected Tropical Disease 4, e684.
Cavalier-Smith T. (1981). Eukaryote kingdoms: seven or nine? Biosystems 14, 461481.
Cavalier-Smith T. (1983). A 6-kingdom classification and a unified phylogeny. In Endocytobiology II (eds. Schenk H. E. A. and Schwemmler W.), pp. 10271034. Walter de Gruyter, Berlin.
Cavalier-Smith T. (1987). Eukaryotes with no mitochondria. Nature 326, 332333.
Cavalier-Smith T. (1999). Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. Journal of Eukaryotic Microbiology 46, 347366.
Cavalier-Smith T. (2010). Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biology Letters 6, 342345.
Clark C. G. and Roger A. J. (1995). Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proceedings of the National Academy of Sciences, USA 92, 65186521.
Dacks J. B., Marinets A., Doolittle W. F., Cavalier-Smith T. and Logsdon J. M. Jr. (2002). Analyses of RNA Polymerase II genes from free-living protists: phylogeny, long branch attraction, and the eukaryotic big bang. Molecular Biology and Evolution 19, 830840.
Diguistini S., Liao N. Y., Platt D., Robertson G., Seidel M., Chan S. K., Docking T. R., Birol I., Holt R. A., Hirst M., Mardis E., Marra M. A., Hamelin R. C., Bohlmann J., Breuil C. and Jones S. J. (2009). De novo genome sequence assembly of a filamentous fungus using Sanger, 454 and Illumina sequence data. Genome Biology 10, R94.
Dunning Hotopp J. C., Clark M. E., Oliveira D. C., Foster J. M., Fischer P., Torres M. C., Giebel J. D., Kumar N., Ishmael N., Wang S., Ingram J., Nene R. V., Shepard J., Tomkins J., Richards S., Spiro D. J., Ghedin E., Slatko B. E., Tettelin H. and Werren J. H. (2007). Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 17531756.
Duraisingh M. T., Voss T. S., Marty A. J., Duffy M. F., Good R. T., Thompson J. K., Freitas-Junior L. H., Scherf A., Crabb B. S. and Cowman A. F. (2005). Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121, 1324.
Edvardsen B., Eikrem W., Green J. C., Andersen R. A., Moon-Van-Der-Staay S. Y. and Medlin L. K. (2000). Phylogenetic reconstructions of the Haptophyta inferred from 18S ribosomal DNA sequences and available morphological data. Phycologia 39, 1935.
Elias M., Patron N. J. and Keeling P. J. (2009). The RAB family GTPase Rab1A from Plasmodium falciparum defines a unique paralog shared by chromalveolates and rhizaria. Journal of Eukaryotic Microbiology 56, 348356.
Fast N. M., Kissinger J. C., Roos D. S. and Keeling P. J. (2001). Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Molecular Biology and Evolution 18, 418426.
Foissner W., Blatterer H. and Foissner I. (1988). The Hemimastigophora (Hemimastix amphikineta nov. gen., nov. spec.), a new protistan phylum from Gondwanan soils. European Journal of Protistology 23, 361383.
Fritz-Laylin L. K., Prochnik S. E., Ginger M. L., Dacks J. B., Carpenter M. L., Field M. C., Kuo A., Paredez A., Chapman J., Pham J., Shu S., Neupane R., Cipriano M., Mancuso J., Tu H., Salamov A., Lindquist E., Shapiro H., Lucas S., Grigoriev I. V., Cande W. Z., Fulton C., Rokhsar D. S. and Dawson S. C. (2010). The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140, 631642.
Frommolt R., Werner S., Paulsen H., Goss R., Wilhelm C., Zauner S., Maier U. G., Grossman A. R., Bhattacharya D. and Lohr M. (2008). Ancient recruitment by chromists of green algal genes encoding enzymes for carotenoid biosynthesis. Molecular Biology and Evolution 25, 26532667.
Godoy P. D., Nogueira-Junior L. A., Paes L. S., Cornejo A., Martins R. M., Silber A. M., Schenkman S. and Elias M. C. (2009). Trypanosome prereplication machinery contains a single functional orc1/cdc6 protein, which is typical of archaea. Eukaryotic Cell 8, 15921603.
Hackett J. D., Yoon H. S., Li S., Reyes-Prieto A., Rummele S. E. and Bhattacharya D. (2007). Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Molecular Biology and Evolution 24, 17021713.
Hampl V., Hug L., Leigh J. W., Dacks J. B., Lang B. F., Simpson A. G. and Roger A. J. (2009). Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups”. Proceedings of the National Academy of Sciences, USA 106, 38593864.
Hibbett D. S., Binder M., Bischoff J. F., Blackwell M., Cannon P. F., Eriksson O. E., Huhndorf S., James T., Kirk P. M., Lucking R., Thorsten Lumbsch H., Lutzoni F., Matheny P. B., Mclaughlin D. J., Powell M. J., Redhead S., Schoch C. L., Spatafora J. W., Stalpers J. A., Vilgalys R., Aime M. C., Aptroot A., Bauer R., Begerow D., Benny G. L., Castlebury L. A., Crous P. W., Dai Y. C., Gams W., Geiser D. M., Griffith G. W., Gueidan C., Hawksworth D. L., Hestmark G., Hosaka K., Humber R. A., Hyde K. D., Ironside J. E., Koljalg U., Kurtzman C. P., Larsson K. H., Lichtwardt R., Longcore J., Miadlikowska J., Miller A., Moncalvo J. M., Mozley-Standridge S., Oberwinkler F., Parmasto E., Reeb V., Rogers J. D., Roux C., Ryvarden L., Sampaio J. P., Schussler A., Sugiyama J., Thorn R. G., Tibell L., Untereiner W. A., Walker C., Wang Z., Weir A., Weiss M., White M. M., Winka K., Yao Y. J. and Zhang N. (2007). A higher-level phylogenetic classification of the Fungi. Mycological Research 111, 509547.
Holder M. and Lewis P. O. (2003). Phylogeny estimation: traditional and Bayesian approaches. Nature Reviews Genetics 4, 275284.
Horn D. and Barry J. D. (2005). The central roles of telomeres and subtelomeres in antigenic variation in African trypanosomes. Chromosome Research 13, 525533.
Huang J., Mullapudi N., Lancto C. A., Scott M., Abrahamsen M. S. and Kissinger J. C. (2004). Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biology 5, R88.
Iida K., Takishita K., Ohshima K. and Inagaki Y. (2007). Assessing the monophyly of chlorophyll-c containing plastids by multi-gene phylogenies under the unlinked model conditions. Molecular Phylogenetics and Evolution 45, 227238.
Imanian B., Pombert J. F. and Keeling P. J. (2010). The complete plastid genomes of the two ‘dinotoms’ Durinskia baltica and Kryptoperidinium foliaceum. PLoS One 5, e10711.
James T. Y., Kauff F., Schoch C. L., Matheny P. B., Hofstetter V., Cox C. J., Celio G., Gueidan C., Fraker E., Miadlikowska J., Lumbsch H. T., Rauhut A., Reeb V., Arnold A. E., Amtoft A., Stajich J. E., Hosaka K., Sung G. H., Johnson D., O'rourke B., Crockett M., Binder M., Curtis J. M., Slot J. C., Wang Z., Wilson A. W., Schussler A., Longcore J. E., O'donnell K., Mozley-Standridge S., Porter D., Letcher P. M., Powell M. J., Taylor J. W., White M. M., Griffith G. W., Davies D. R., Humber R. A., Morton J. B., Sugiyama J., Rossman A. Y., Rogers J. D., Pfister D. H., Hewitt D., Hansen K., Hambleton S., Shoemaker R. A., Kohlmeyer J., Volkmann-Kohlmeyer B., Spotts R. A., Serdani M., Crous P. W., Hughes K. W., Matsuura K., Langer E., Langer G., Untereiner W. A., Lucking R., Budel B., Geiser D. M., Aptroot A., Diederich P., Schmitt I., Schultz M., Yahr R., Hibbett D. S., Lutzoni F., Mclaughlin D. J., Spatafora J. W. and Vilgalys R. (2006). Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443, 818822.
Joseph S. J., Fernandez-Robledo J. A., Gardner M. J., El-Sayed N. M., Kuo C. H., Schott E. J., Wang H., Kissinger J. C. and Vasta G. R. (2010). The Alveolate Perkinsus marinus: biological insights from EST gene discovery. BMC Genomics 11, 228.
Karpov S. A. and Zhukov B. F. (1986). Ultrastructure and taxonomic position of Apusomonas proboscidea Alexeieff. Archiv für Protistenkund, 131, 1326.
Keeling P. J. (2001). Foraminifera and cercozoa are related in actin phylogeny: two orphans find a home? Molecular Biology and Evolution 18, 15511557.
Keeling P. J. and Fast N. M. (2002). Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Reviews Microbiology 56, 93116.
Kim E., Simpson A. G. and Graham L. E. (2006). Evolutionary relationships of apusomonads Inferred from taxon-rich analyses of six nuclear-encoded genes. Molecular Biology and Evolution 23, 24552466.
Koopmann R., Muhammad K., Perbandt M., Betzel C. and Duszenko M. (2009). Trypanosoma brucei ATG8: structural insights into autophagic-like mechanisms in protozoa. Autophagy 5, 10851091.
Leander B. S. and Keeling P. J. (2003). Morphostasis in alveolate evolution. Trends in Ecology and Evolution 18, 395402.
Li S., Nosenko T., Hackett J. D. and Bhattacharya D. (2006). Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the chromalveolates. Molecular Biology and Evolution 23, 663674.
Lucas I. A. N. (1970). Observation on the ultrastructure of representatives of the genera Hemiselmis and Chroomonas (Cryptophyceae). British Phycological Journal 5, 2937.
Minge M. A., Silberman J. D., Orr R. J., Cavalier-Smith T., Shalchian-Tabrizi K., Burki F., Skjaeveland A. and Jakobsen K. S. (2009). Evolutionary position of breviate amoebae and the primary eukaryote divergence. Proceedings of the Royal Society of London B Biological Sciences 276, 597604.
Moore R. B., Obornik M., Janouskovec J., Chrudimsky T., Vancova M., Green D. H., Wright S. W., Davies N. W., Bolch C. J., Heimann K., Slapeta J., Hoegh-Guldberg O., Logsdon J. M. and Carter D. A. (2008). A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451, 959963.
Moreira D., Le Guyader H. and Phillippe H. (2000). The origin of red algae and the evolution of chloroplasts. Nature 405, 6972.
Morrison H. G., Mcarthur A. G., Gillin F. D., Aley S. B., Adam R. D., Olsen G. J., Best A. A., Cande W. Z., Chen F., Cipriano M. J., Davids B. J., Dawson S. C., Elmendorf H. G., Hehl A. B., Holder M. E., Huse S. M., Kim U. U., Lasek-Nesselquist E., Manning G., Nigam A., Nixon J. E., Palm D., Passamaneck N. E., Prabhu A., Reich C. I., Reiner D. S., Samuelson J., Svard S. G. and Sogin M. L. (2007). Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317, 19211926.
Moustafa A., Beszteri B., Maier U. G., Bowler C., Valentin K. and Bhattacharya D. (2009). Genomic footprints of a cryptic plastid endosymbiosis in diatoms. Science 324, 17241726.
Nosenko T. and Bhattacharya D. (2007). Horizontal gene transfer in chromalveolates. BMC Evolutionary Biology 7, 173.
Nozaki H., Maruyama S., Matsuzaki M., Nakada T., Kato S. and Misawa K. (2009). Phylogenetic positions of Glaucophyta, green plants (Archaeplastida) and Haptophyta (Chromalveolata) as deduced from slowly evolving nuclear genes. Molecular Phylogenetics and Evolution 53, 872880.
Obornik M., Janouskovec J., Chrudimsky T. and Lukes J. (2009). Evolution of the apicoplast and its hosts: from heterotrophy to autotrophy and back again. International Journal for Parasitology 39, 112.
Okamoto N., Chantangsi C., Horak A., Leander B. S. and Keeling P. J. (2009). Molecular phylogeny and description of the novel katablepharid Roombia truncata gen. et sp. nov., and establishment of the Hacrobia taxon nov. PLoS One 4, e7080.
Okamoto N. and Mcfadden G. I. (2008). The mother of all parasites. Future Microbiology 3, 391395.
Page F. C. (1987). The classification of “naked” amoebae (Phylum Rhizopoda). Archiv für Protistenkunde 133, 199217.
Parfrey L. W., Grant J., Tekle Y. I., Lasek-Nesselquist E., Morrison H. G., Sogin M. L., Patterson D. J. and Katz L. A. (2010). Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. Systematic Biology 59, 518533.
Philippe H. and Germot A. (2000). Phylogeny of eukaryotes based on ribosomal RNA: long-branch attraction and models of sequence evolution. Molecular Biology and Evolution 17, 830834.
Philippe H., Lopez P., Brinkmann H., Budin K., Germot A., Laurent J., Moreira D., Muller M. and Le Guyader H. (2000). Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proceedings of the Royal Society of London B Biological Sciences 267, 12131221.
Philippe H. and Telford M. J. (2006). Large-scale sequencing and the new animal phylogeny. Trends in Ecology and Evolution 21, 614620.
Pusnik M., Charriere F., Maser P., Waller R. F., Dagley M. J., Lithgow T. and Schneider A. (2009). The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. Molecular Biology and Evolution 26, 671680.
Reeb V. C., Peglar M. T., Yoon H. S., Bai J. R., Wu M., Shiu P., Grafenberg J. L., Reyes-Prieto A., Rummele S. E., Gross J. and Bhattacharya D. (2009). Interrelationships of chromalveolates within a broadly sampled tree of photosynthetic protists. Molecular Phylogenetics and Evolution 53, 202211.
Reyes-Prieto A., Moustafa A. and Bhattacharya D. (2008). Multiple genes of apparent algal origin suggest ciliates may once have been photosynthetic. Current Biology 18, 956962.
Richards T. A. and Cavalier-Smith T. (2005). Myosin domain evolution and the primary divergence of eukaryotes. Nature 436, 11131118.
Rodriguez-Ezpeleta N., Brinkmann H., Burey S. C., Roure B., Burger G., Loffelhardt W., Bohnert H. J., Philippe H. and Lang B. F. (2005). Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Current Biology 15, 13251330.
Roger A. J., Clark C. G. and Doolittle W. F. (1996). A possible mitochondrial gene in the early-branching amitochondriate protist Trichomonas vaginalis. Proceedings of the National Academy of Science, USA 93, 1461814622.
Roger A. J., Svard S. G., Tovar J., Clark C. G., Smith M. W., Gillin F. D. and Sogin M. L. (1998). A mitochondrial-like chaperonin 60 gene in Giardia lamblia: Evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proceedings of the National Academy of Sciences, USA 95, 229234.
Rogozin I. B., Basu M. K., Csuros M. and Koonin E. V. (2009). Analysis of rare genomic changes does not support the unikont-bikont phylogeny and suggests cyanobacterial symbiosis as the point of primary radiation of eukaryotes. Genome Biology and Evolution 1, 99113.
Sanchez Puerta M. V. and Delwiche C. F. (2008). A hypothesis for plastid evolution in chromalveolates. Journal of Phycology 44, 10971107.
Saunders G. and Hommersand Mh. (2004). Assessing red algal supraordinal diversity and taxonomy in the context of contemporary systematic data. American Journal of Botany 91, 14941507.
Shadwick L. L., Spiegel F. W., Shadwick J. D., Brown M. W. and Silberman J. D. (2009). Eumycetozoa=Amoebozoa?: SSUrDNA phylogeny of protosteloid slime molds and its significance for the amoebozoan supergroup. PLoS One 4, e6754.
Shalchian-Tabrizi K., Minge M. A., Espelund M., Orr R., Ruden T., Jakobsen K. S. and Cavalier-Smith T. (2008). Multigene phylogeny of choanozoa and the origin of animals. PLoS One 3, e2098.
Simon N., Cras A. L., Foulon E. and Lemee R. (2009). Diversity and evolution of marine phytoplankton. Comptes Rendus Biologies 332, 159170.
Simpson A. G. (2003). Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). International Journal of Systematic and Evolutionary Microbiology 53, 17591777.
Slamovits C. H. and Keeling P. J. (2008). Plastid-derived genes in the nonphotosynthetic alveolate Oxyrrhis marina. Molecular Biology and Evolution 25, 12971306.
Smith R. and Patterson D. (1986). Analyses of heliozoan interrelationships: an example of the potentials and limitations of ultrastructural approaches to the study of protistan phylogeny. Proceedings of the Royal Society of London B Biological Sciences 227, 325366.
Snow R. W., Guerra C. A., Noor A. M., Myint H. Y. and Hay S. I. (2005). The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434, 214217.
Sogin M. L. (1991). Early evolution and the origin of eukaryotes. Current Opinions in Genetics and Development 1, 457463.
Sogin M. L. and Silberman J. D. (1998). Evolution of the protists and protistan parasites from the perspective of molecular systematics. International Journal for Parasitology 28, 1120.
Stechmann A. and Cavalier-Smith T. (2002). Rooting the eukaryote tree by using a derived gene fusion. Science 297, 8991.
Steuernagel B., Taudien S., Gundlach H., Seidel M., Ariyadasa R., Schulte D., Petzold A., Felder M., Graner A., Scholz U., Mayer K. F., Platzer M. and Stein N. (2009). De novo 454 sequencing of barcoded BAC pools for comprehensive gene survey and genome analysis in the complex genome of barley. BMC Genomics 10, 547.
Takishita K., Yamaguchi H., Maruyama T. and Inagaki Y. (2009). A hypothesis for the evolution of nuclear-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase genes in “chromalveolate” members. PLoS One 4, e4737.
Taylor F. J. (1999). Ultrastructure as a control for protistan molecular phylogeny. American Naturalist 154, S125S136.
Tovar J., Leon-Avila G., Sanchez L. B., Sutak R., Tachezy J., Van Der Giezen M., Hernandez M., Muller M. and Lucocq J. M. (2003). Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172176.
Van Der Giezen M. (2009). Hydrogenosomes and mitosomes: conservation and evolution of functions. Journal of Eukaryotic Microbiology 56, 221231.
Walker G., Dacks J. B. and Embley T. M. (2006). Ultrastructural description of Breviata anathema, n. gen., n. sp., the organism previously studied as “Mastigamoeba invertens. Journal of Eukaryotic Microbiology 53, 6578.
Whittaker R. H. (1969). New concepts of the kingdoms of organisms. Science 163, 150159.
Worden A. Z., Lee J. H., Mock T., Rouze P., Simmons M. P., Aerts A. L., Allen A. E., Cuvelier M. L., Derelle E., Everett M. V., Foulon E., Grimwood J., Gundlach H., Henrissat B., Napoli C., Mcdonald S. M., Parker M. S., Rombauts S., Salamov A., Von Dassow P., Badger J. H., Coutinho P. M., Demir E., Dubchak I., Gentemann C., Eikrem W., Gready J. E., John U., Lanier W., Lindquist E. A., Lucas S., Mayer K. F., Moreau H., Not F., Otillar R., Panaud O., Pangilinan J., Paulsen I., Piegu B., Poliakov A., Robbens S., Schmutz J., Toulza E., Wyss T., Zelensky A., Zhou K., Armbrust E. V., Bhattacharya D., Goodenough U. W., Van De Peer Y. and Grigoriev I. V. (2009). Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324, 268272.
Yadav V. P., Mandal P. K., Rao D. N. and Bhattacharya S. (2009). Characterization of the restriction enzyme-like endonuclease encoded by the Entamoeba histolytica non-long terminal repeat retrotransposon EhLINE1. FEBS Journal 276, 70707082.
Yoon H. S., Hackett J. D., Ciniglia C., Pinto G. and Bhattacharya D. (2004). A molecular timeline for the origin of photosynthetic eukaryotes. Molecular Biology and Evolution 21, 809818.
Yubuki N. and Leander B. S. (2008). Ultrastructure and molecular phylogeny of Stephanopogon minuta: an enigmatic microeukaryote from marine interstitial environments. European Journal of Protistology 44, 241253.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Type Description Title
PDF
Supplementary materials

Walker Supplementary Material
Walker Supplementary Material

 PDF (3.6 MB)
3.6 MB
PDF
Supplementary materials

Walker Supplementary Material
Walker Supplementary Table

 PDF (166 KB)
166 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 34
Total number of PDF views: 126 *
Loading metrics...

Abstract views

Total abstract views: 661 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd January 2018. This data will be updated every 24 hours.