Journal of Molecular Evolution

, Volume 62, Issue 4, pp 388–420 | Cite as

Phylogeny and Megasystematics of Phagotrophic Heterokonts (Kingdom Chromista)

  • Thomas Cavalier-SmithEmail author
  • Ema E-Y. Chao


Heterokonts are evolutionarily important as the most nutritionally diverse eukaryote supergroup and the most species-rich branch of the eukaryotic kingdom Chromista. Ancestrally photosynthetic/phagotrophic algae (mixotrophs), they include several ecologically important purely heterotrophic lineages, all grossly understudied phylogenetically and of uncertain relationships. We sequenced 18S rRNA genes from 14 phagotrophic non-photosynthetic heterokonts and a probable Ochromonas, performed phylogenetic analysis of 210–430 Heterokonta, and revised higher classification of Heterokonta and its three phyla: the predominantly photosynthetic Ochrophyta; the non-photosynthetic Pseudofungi; and Bigyra (now comprising subphyla Opalozoa, Bicoecia, Sagenista). The deepest heterokont divergence is apparently between Bigyra, as revised here, and Ochrophyta/Pseudofungi. We found a third universal heterokont signature sequence, and deduce three independent losses of ciliary hairs, several of 1-2 cilia, 10 of photosynthesis, but perhaps only two plastid losses. In Ochrophyta, heterotrophic Oikomonas is sister to the photosynthetic Chrysamoeba, whilst the abundant freshwater predator Spumella is biphyletic; neither clade is specifically related to Paraphysomonas, indicating four losses of photosynthesis by chrysomonads. Sister to Chrysomonadea (Chrysophyceae) is Picophagea cl. nov. (Picophagus, Chlamydomyxa). The diatom-parasite Pirsonia belongs in Pseudofungi. Heliozoan-like actinophryids (e.g. Actinosphaerium) are Opalozoa, not related to pedinellids within Hypogyristea cl. nov. of Ochrophyta as once thought. The zooflagellate class Bicoecea (perhaps the ancestral phenotype of Bigyra) is unexpectedly diverse and a major focus of our study. We describe four new biciliate bicoecean genera and five new species: Nerada mexicana, Labromonas fenchelii (=Pseudobodo tremulans sensu Fenchel), Boroka karpovii (=P. tremulans sensu Karpov), Anoeca atlantica and Cafeteria mylnikovii; several cultures were previously misidentified as Pseudobodo tremulans. Nerada and the uniciliate Paramonas are related to Siluania and Adriamonas; this clade (Pseudodendromonadales emend.) is probably sister to Bicosoeca. Genetically diverse Caecitellus is probably related to Anoeca, Symbiomonas and Cafeteria (collectively Anoecales emend.). Boroka is sister to Pseudodendromonadales/Bicoecales/Anoecales. Placidiales are probably divergent bicoeceans (the GenBank Placidia sequence is a basidiomycete/heterokont chimaera). Two GenBank ‘opalinid’ sequences are fungal; Pseudopirsonia is cercozoan; two previous GenBank ‘Caecitellus’ sequences are Adriamonas.


Heterokonta Oikomonas Anoeca Bicoecea Caecitellus Paramonas Nerada Opalozoa Labromonas Bigyra 



TCS thanks NSERC Canada and NERC UK for research grants; the Canadian Institute for Advanced Research and NERC for fellowship support. We thank A. P. Mylnikov for cultures, D. Caron and R. Gast for the WHOI cultures, E. Harley and M. P. Berman for hospitality at the University of Cape Town, and Fiona Hannah for hospitality at Millport.

Supplementary material

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Supplementary material


  1. Andersen RA (1987) Synurophyceae classis nov., a new class of algae. Am J Bot 74:337–353Google Scholar
  2. Andersen RA, Saunders GW, Paskind MP, Sexton J (1993) Ultrastructure and 18S rRNA gene sequence for Pelagomonas calceolata gen. et sp. nov. and the description of a new algal class, the Pelagophyceae classis nov. J Phycol 29:701–715CrossRefGoogle Scholar
  3. Andersen RA, Van de Peer Y, Potter MD, Sexton JP Kawachi M, LaJeunesse T (1999) Phylogenetic analysis of the SSU rRNA from members of the Chrysophyceae. Protist 150:71–84PubMedGoogle Scholar
  4. Andersen RA, Wetherbee R (1992) Microtubules of the flagellar apMatus are active in prey capture of the chrysophycean alga Epipyxis pulchra. Protoplasma 166:1–7CrossRefGoogle Scholar
  5. Archer W (1875) Memoirs on Chlamydomyxa labyrinthuloides nov. gen. et sp., a new freshwater sarcodic organism. Q J Microsc Sci 15:107–130Google Scholar
  6. Atkins MS, Teske AP, Anderson OR (2000) A survey of flagellate diversity at four deep-sea hydrothermal vents in the pastern Pacific Ocean using structural and molecular approaches. J Eukaryot Microbiol 47:400–411PubMedCrossRefGoogle Scholar
  7. Bailey JC, Bidigare RR, Christensen SJ, Andersen RA (1998) Phaeothamniophyceae classis nova: a new lineage of chromophytes based on photosynthetic pigments, rbcL sequence analysis and ultrastructure. Protist 149:242–263Google Scholar
  8. Barr D, Desaulniers NL (1987) Ultrastructure of the Lagena radicola zoospore, including a comparison with the primary and secondary Saprolegnia zoospores. Can J Bot 65:2161–2176Google Scholar
  9. Barr D, Cavalier-Smith J (2004) Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). Int J Syst Evol Microbiol 54:2393–2404PubMedGoogle Scholar
  10. Bass D, Moreira D, López-García P, Polet S, Chao EE, von der Heyden S, Pawlowski J, Cavalier-Smith T (2005) Polyubiquitin insertions and the phylogeny of Cercozoa and Rhizaria. Protist 156:215–224CrossRefGoogle Scholar
  11. Beam CA, Preparata RM, Himes M, Nanney DL (1993) Ribosomal RNA sequencing of members of the Crypthecodinium cohnii (Dinophyceae) species complex; comparison with soluble enzyme studies. J Eukaryot Microbiol 40:660–667PubMedGoogle Scholar
  12. Ben Ali A, De Baere R, De Wachter R, Van de Peer Y (2002) Evolutionary relationships among heterokont algae (the autotrophic stramenopilesi based on combined analyses of small and large subunit ribosomal RNA. Protist 153:123–132PubMedGoogle Scholar
  13. Ben Ali A, De Baere R, Van der Auwera G, De Wachter R, Van de Peer Y (2001) Phylogenetic relationships amojig algae based on complete large-subunit rRNA sequences. Int J Syst Evol Microbiol 51:737–749PubMedGoogle Scholar
  14. Berney C, Fahrni J, Pawlowski J (2004) How many novel eukaryotic ‘kingdoms’? Pitfalls and limitations of enviroijniental DNA surveys. BMC Biol 2:13PubMedCrossRefGoogle Scholar
  15. Bhattacharya D, Helmchen T, Melkonian M (1995) Molecular evolutionary analyses of nuclear-encoded small subunit ribosomal RNA identify an independent rhizopod lineage containing the Euglyphina and the Chlorarachniophyt. J Eukaryot Microbiol 42:65–69PubMedGoogle Scholar
  16. Bortnick RN, Powell MJ, Bangert TN (1985) Zoospores fine structure of the parasite Olpidiopsis saprolegniae variety saprolegniae (Oomycetes, Lagenidiales). Mycologia 77:861–878Google Scholar
  17. Caron DA, Lim EL, Dennett MR, Gast RJ, Kosman C, DeLong EF (1999) Molecular phylogenetic analysis of the heterotrophic chrysophyte genus Paraphysomonas (Chrysophycael and the design of rRNA-targeted oligonucleotide probes for two species. J Phycol 35:824–837CrossRefGoogle Scholar
  18. Carranza S, Giribet G, Ribera C, Baguna, Riutort M (1996) Evidence that two types of 18S rDNA coexist in the genome of Dugesid (Schmidted) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Mol Biol Evol 13:824–832PubMedGoogle Scholar
  19. Cash J (1905) The British freshwater Rhizopoda and Heliozoa. Ray Society, LondonGoogle Scholar
  20. Cavalier-Smith T (1974) Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J Cell Sci 16:529–556PubMedGoogle Scholar
  21. Cavalier-Smith T (1981) Eukaryote kingdoms: seven or nine? BioSystems 14:461–481PubMedCrossRefGoogle Scholar
  22. Cavalier-Smith T (1982) The origins of plastids. Biol J Linn Soc 17:289–306Google Scholar
  23. Cavalier-Smith T (1986a) The kingdom Chromista: origin and systematics. In: Round FE, Chapman DJ (eds) Progress in phycological research. Biopress, Bristol, pp 309–347Google Scholar
  24. Cavalier-Smith T (1986b) The kingdoms of organisms. Nature 324:416–417CrossRefGoogle Scholar
  25. Cavalier-Smith T (1989) The kingdom Chromista. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte algae: Problems and perspectives. Clarendon Press, Oxford, pp 381–407Google Scholar
  26. Cavalier-Smith T (1991) Cell diversification in heterotrophic flagellates. In: Patterson DJ, Larsen J (eds) The biology of free-living heterotrophic flagellates. Clarendon Press, Oxford, pp 113–131Google Scholar
  27. Cavalier-Smith T (1992) The number of symbiotic origins of organelles. BioSystems 28:91–106; discussion 107–108PubMedCrossRefGoogle Scholar
  28. Cavalier-Smith T (1993a) Kingdom Protozoa and its 18 phyla. Microbiol Rev 57:953–994Google Scholar
  29. Cavalier-Smith T (1993b) The origin, losses and gains of chloroplasts. In: Lewin RA (ed) Origin of plastids; Symbiogenesis, prochlorophytes and the origins of chloroplasts. Chapman & Hall, New York, pp 291–348Google Scholar
  30. Cavalier-Smith T (1993c) The protozoan phylum Opalozoa. J Euk Microbiol 40:609–615Google Scholar
  31. Cavalier-Smith T (1994) Origin and relationships of Haptophyta. In: Green JC, Leadbeater BSC (eds) The haptophyte algae. Clarendon Press, Oxford, pp 413–435Google Scholar
  32. Cavalier-Smith T (1995a) Membrane heredity, symbiogenesis, and the multiple origins of algae. In: Arai R, Kato M, Doi Y (eds) Biodiversity and evolution. The National Science Museum Foundation, Tokyo, pp 75–114Google Scholar
  33. Cavalier-Smith T (1995b) Zooflagellate phytogeny and classification, Tsitologiia 37:1010–1029Google Scholar
  34. Cavalier-Smith T (1996/7) Amoeboflagellates and mitochondrial cristae in eukaryotic evolution: megasystematics of the new protozoan subkingdoms Eozoa and Neozoa. Arch Protistenk 147:237–258Google Scholar
  35. Cavalier-Smith T (1997) Sagenista,and Bigyra, two phyla of heterotrophic heterokont chromists. Archiv Protistenk 148:253–267Google Scholar
  36. Cavalier-Smith T (1998) A revised six-kingdom system of life. Biol Rev Camb Philos Soc 73:203–266PubMedCrossRefGoogle Scholar
  37. Cavalier-Smith T (1999) Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflgellate, and sporozoan plastid origins and the eukaryotic family tree. J Euk Microbiol 46:347–366Google Scholar
  38. Cavalier-Smith T (2000a) Flagellate megaevolution; the basis for eukaryote diversification. In: Green JC, Leadbeater BSC (eds) The flagellates. Taylor and Francis, London, pp 361–390Google Scholar
  39. Cavalier-Smith T (2000b) Membrane heredity and early chloroplast evolution, Trends Plant Sci 5:174–182CrossRefGoogle Scholar
  40. Cavalier-Smith T (2002a) The phagotrophic origin eukaryotes and phylogenetic classification of Protozoa. Int J Syst Evol Microbiol 52:297–354Google Scholar
  41. Cavalier-Smith T (2002b) The neomuran orign of archaebacteria, the negibacterial of the universal tree and bacterial megaclassification. Int J Syst Evol Microbiol 52:7–76Google Scholar
  42. Cavalier-Smith T (2003a) The excavate protozoan phyla Metamonada Grassé emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malammonas): their evolutionary affinities and new higher taxa. Int J Syst Evol Microbiol 53:1741–1758Google Scholar
  43. Cavalier-Smith T (2003b) Genomic reduction and evolution of novel genetic membranes and protein-targetng machinery in eukaryote-eukaryote chimaeras (meta-algae). Phil Trans R Soc B 358:109–134CrossRefGoogle Scholar
  44. Cavalier-Smith T (2003e) Protist phytogeny and the high-level classification of Protozoa. Eur J Protistol 39:338–348Google Scholar
  45. Cavalier-Smith T (2004c) Chromalveolate diversity and cell megaevolution: interplay of membranes, genomes and cytoakeleton. In: Hirt RP, Horner DS (eds) Organelles, genomes and eukaryote phytogeny. CRC Press, London, pp 75–108Google Scholar
  46. Cavalier-Snfiith T (2004b) Only six kingdoms of life. Proc Soc Lond B 271:1251–1262CrossRefGoogle Scholar
  47. Cavalier-Smith T, Allsopp MTEP, Chao EE (1994) Thraustochytrids are comjsts not fungi: 18S rRNA signatures of Heterokonta. Phil Trans R Soc Lond B 145:209–220Google Scholar
  48. Cavalier-Smith T, Chao EE (1995) The opalozoan Apusomonas is related to the common ancestor of animals, fungi, and choanoflagellates. Proc R Soc Lond B 261:1–6Google Scholar
  49. Cavalier-Smith T, Chao EE (1996) 18S rRNA sequence of Heterosigma carterae (Raphidophyceae), and the phylogeny of heterokont algae (Ochrophyta). Phycologia 35:500–510Google Scholar
  50. Cavalier-Smith T, Chao EE (2003a) Molecular phylogeny of centrohelid heliozoa, a novel lineage of bikont eukaryotes that arose by ciliary loss. J Mol Evol 56:387–396Google Scholar
  51. Cavalier-Smith T, Chao EE (2003b) Phylogeny and classification of phylum Cercozoa (Protozoa), Protist 154:341–358Google Scholar
  52. Cavalier-Smith T, Chao EE (2003c) Phylogeny of Choanozoa, Apusozoa, and other Protozoa and early eukaryote megaevolution. J Mol Evol 56:540–563Google Scholar
  53. Cavalier-Smith T, Chao EE, Allsopp MTEP (1995) Ribosomal RNA evidence for chloroplast loss within Heterokonta; Pedingllid relationships and a revised classification of ochristan algae. Archiv Protistenk 145:209–220Google Scholar
  54. Cavalier-Smith T, Chao EE, Thompson CE, Hourihane SL (1995/1996) Oikomonas, a distinctive zooflagellate related to chrysomonads. Arch Protistenkd 146:273–279Google Scholar
  55. Cole DG (2003) Intraflagellar transport in the unicellular green alga, Chlamydomonas reinhardtii. Protist 154:181–191PubMedCrossRefGoogle Scholar
  56. Dawson SC, Pace NR (2002) Novel kingdom-level eukaryotic diversity in anoxic environments. Proc Natl Acad USA 99:8324–8329PubMedCrossRefGoogle Scholar
  57. Delwiche CF (1999) Tracing thefhread of plastid diversity through the tapestry of life. Am Nat 154:181–191CrossRefGoogle Scholar
  58. Dick M (2001) Straminipilous fungi. CABI International, WallingfordGoogle Scholar
  59. Dzik J (1995) Yunnanozoon and the ancestry of chordates. Acta Palaeont Polon 40:341–360Google Scholar
  60. Edgcomb VP, Kysela DT, Teske A, de Vera Gomez A, Sogin ML (2002) Benthic eukaryotic diversity in the Guaymas Basin hydrothermal vent environment. Proc Natl Acad Sci USA 99:7658–7662PubMedCrossRefGoogle Scholar
  61. Fast NM, Kissinger JC, Roos DS, Keeling PJ (2001) Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18:418–426PubMedGoogle Scholar
  62. Fenchel T (1982) Ecology of heterotrophic microflagellate. I. Some important forms and their functional morphology. Mar Ecol Prog Ser 8:211–223Google Scholar
  63. Fenchel T, Patterson DJ (1988) Cafeteria roenbergensis nov. gen., nov. sp., a heterotrophic microflagellate from marine plankton. Mar Microb Food Webs 3:9–19Google Scholar
  64. Foth BJ, McFadden GI (2003) The apicoplast: a plastidHp Plasmodium falciparum and other Apicomplexan parasites. Int Rev Cytol 224:57–110PubMedGoogle Scholar
  65. Gibbs SP (1962) Nuclear envelope-chloroplast relationships in algae. J Cell Biol 14:433–444PubMedCrossRefGoogle Scholar
  66. Goertzen LR, Theriot EC (2003) Effect of taxon sampling, character weighting, and combined data on the interpretation of relationships among the heterokont algae. J Phycol 39:423–439Google Scholar
  67. Grassé P-P, Deflandre G (1952) Ordre des Bicocidea, In: Grassé P-P (ed) Traité de Zoologie: Anatomic, Systématique, Biologie: I Fasc. 1 Phylogénie. Protozoaires: Généralités, Flagellés. Masson, Paris, pp 599–591Google Scholar
  68. Griessmann K (1913) Ueber marine Flagellaten. Archiv Protistenk 32:1–78Google Scholar
  69. Guillou L, Chrétiennot-Dinet M-J, Medlin LK, Claustre H, Loiseaux de Göer S, Vaulot D (1999a) Bolidomonas: a new genus itvo species belonging to a new algal class, the Bolidophyceae (Heterokonta). J Phycol 35:368–381CrossRefGoogle Scholar
  70. Guillou L, Chrétiennot-Dinet MJ, Boulben S, Moon-van der Staay SY, Vaulot D (1999b) Symbiomonas scintillans gen. et sp. nov. and Picophagus flagellatus gen. et sp. nov.) (Heterokonta): two new heterotrophic flagellates of picoplanktonic size. Protist 150:383–398Google Scholar
  71. Gunderson JH, Sogin ML, Wollett G, Hollingdale M, de la Cruz VF, Waters AP, McCutchan TF (1987) Structurally distinct, stage-specific ribosomes occur inPlasmodium. Science 238:933–937PubMedGoogle Scholar
  72. Harper JT, Keeling PJ (2003) Nucleus-encoded, plastid-targeted glyceraldehyde-3-phosphate dehydrogenase (GAPDH) indicates a single origin for chromalveolate plastids. Mol Biol Evol 20:1730–1735PubMedGoogle Scholar
  73. Bibberd DJ (1971) The ultrastructure and taxonomy of the Chrysophyceae and Prymnesiophyceae (Haptophyceae): a survey with some new observations on the ultrastructure of the Chrysophyceae. Biol J Linn Soc 72:55–80Google Scholar
  74. Hibberd DJ (1985) Observations on the ultrastructure of new species of Pseudodendromona Bourrelly (P. operculifera and P. insignis) and Cyathobodo Petersen and Hansea. (C. peltatus and C. gemmatus), Pseudodendromonadida ord, nov.). Archiv Protistenk 129:3–11Google Scholar
  75. Hillis DM, Pollock DD, McGuire JA, Zwickl DJ (2003) Is sparse taxon sampling a problem for phylogenetic inference? Syst Biol 52:124–126PubMedGoogle Scholar
  76. Honda D, Inouye I (2002) Ultrastructure and taxonomy of a marine photosynthetic stramenopile Phaeomonas parva gen. et sp, nov, (Pinguiophyceae) with emphasis on the flagellar apparatus architecture. Phycol Res 50:75–89Google Scholar
  77. Honda D, Yokochi T, Nakahara T, Raghukumar S, Nakagiri A, Schaumann K, Higashihara T (1999) Molecular phytogeny of labyrinthulids and thraustophytrids based on the sequencing of 18S ribosomal RNA gene. J Eukaryot Microbiol 46:637–647PubMedGoogle Scholar
  78. James-Clark H (1868) On the Spongiae Ciliatae as Infusoria Flagellata: or observations on the structure, animality, and relationship of Leucosolenia botryoides, Bowerbank. Memoirs Boston Soc Nat Hist 1:305–340 plus plates 9, 10Google Scholar
  79. Karpov SA (2000) Ultrastructure of the aloricate bicosoecid Pseudobodo tremulans, with revision of the order Bicosoecida. Protistology 1:101–109Google Scholar
  80. Karpov SA (2001) Protist cell structure. Tessa, St PetersburgGoogle Scholar
  81. Karpov SA, Fokin SA (1995) The structural diversity of the flagellar transition zone in heterotrophic flagellates and other protists. Cytology 37:1038–1052Google Scholar
  82. Karpov SA, Kersanach R, Williams DM (1998) Ultrastructure and 18S rRNA gene sequence of a small heterqtrophic flagellate Siluania monomastiga gen. et sp. nov. (Bicosoecida). Eur J Protistol 34:414–425Google Scholar
  83. Karpov SA, Sogin M, Silberman JD (2001) Rootlet homology, taxononmy, and phytogeny of bicosoecids based on 18S rRNA gene sequences. Protistology 2:34–47Google Scholar
  84. Kawachi M, Inouye I, Honda D, O’Kelly CI, Bailey JC, Bidgare RR, Andersen RA (2002a) The Pinguiophyceae classis nova, a new class of photosynthetic stramenopiles whose members produce large amounts of omega-3 fatty acids. Phycol Res 50:31–47Google Scholar
  85. Kawachi M, Noël MH, Andersen RA (2002b) Re-examination of the marine ‘chrysophyte’ Polypodiochrysis teissieri (Pinguiophyceae). Phycol Res 50:91–100Google Scholar
  86. Kawai H, Maeba S, Sasaki H, Okuda K, Henry EC (2003) Schizoclaclia ischiensis: a new filamentous marine chromophyte belonging to a new class, Schizocladiophyceae. Protist 154:211–228PubMedCrossRefGoogle Scholar
  87. Kent WS (1880–1882) A manual of the Infusoria. Bogue, LondonGoogle Scholar
  88. Kostka M, Hampl V, Cepicka I, Flegr J (2004) Phylogenetic position of Rnoopalina intestinalis based on SSU rRNA gene sequence. Mol Phylogenet Evol 33:220–224PubMedGoogle Scholar
  89. Kuehn S, Medlin LK, Eller G (2004) Phylogettetic position of the parasitoid nanoflagellate Pirsonia inferred from nuclear-encoded smallsubunit ribosomal DNAand redescription of Pseudopirsonia mucosa (Drebes) comb. nov. Protist 155:143–156Google Scholar
  90. Lankester ER (1890) Zoological articles contributed to the “Encyclopedia Brittanica”. Adam and Charles Black, LondonGoogle Scholar
  91. Larsen J, Pattemon DJ (1990) Some flagellates (Protista) from tropical marine sediments, J Nat Hist 24:801–937Google Scholar
  92. Leander CA, Porter D, (2001) The Labyrinthulomycota is comprised of three distinct lineages. Mycologia 93:459–464Google Scholar
  93. Leedale G (1974) How many are the kingdoms of organisms? Taxon 23:261–270Google Scholar
  94. Leipe DD, Tong SM, Goggin CL, Slemenda SB, Pienizek NJ, Sogin ML (1996) 16S-like rDNA sequences from Developayella elegans, Labyrinthuloides haliotidis, and Proteromonas lacertae confirm that the stramenopiles are a primarily heterotrophic group. Eur J Protistol 32:449–458Google Scholar
  95. Luther A, (1899) Ueber Chlorosaccus, eine neue Gattung der Süsswasseralgen, Bihang till Kongliga Svenska Vetenkaps Akademiens Handlingar 24, III:1–22Google Scholar
  96. Manton I, Clarke B (1950) Electron microscope observations on the spemiatozoid of Fucus. Nature 166:973–974PubMedGoogle Scholar
  97. Margulis L (1970) Origin of eukaryotic cells, Yale University Press, New HavenGoogle Scholar
  98. McCutchan TF, de la Cruz VF, Lal AA, Gunderson JH, Elwood HJ, Sogin ML (1988) Primary sequences of two small subunit ribosomal RNA genes from Plasmodium falciparum. Mol Biochem Parasitol 28:63–68PubMedCrossRefGoogle Scholar
  99. Medlin L, Kooistra WHCF, Potter D, Saunders GW, Andersen RA (1997) Phylogenetic relationships of the ‘golden algae’ (haptophytes, heterokont chromophytes) and their plastids. PI Syst Evol Suppl 11:187–219Google Scholar
  100. Mikrjukov KA, Patterson DJ (2001) Taxonomy and phylogeny of Heliozoa. III. Actinophryids, Acta Protozoologica 40:3–25Google Scholar
  101. Moestrup Ø (2000) The flagellate cytoskeleton; introduction of a general terminology for microtubular roots in protists. In: Leadbeater BS, Green JC (eds) The flagellates: unity, diversity and evolution, Taylor & Francis, London, pp 69–94Google Scholar
  102. Moestrup Ø (2002) Order Bicosoecida Grassé 1926. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the Protozoa. Society of Protozoologists, Lawrence, Kansas, pp 690–693Google Scholar
  103. Moriya M, Nakayama T, Inouye I (2000) Ultrastructure and 18S rDNA sequence analysis of Wobblia lunata gen. et sp. nov., a new heterotrophic flagellate (stramenopiles, incertae sedis), Protist 151:41–55PubMedCrossRefGoogle Scholar
  104. Moriya M, Nakayama T, Inouye I (2002) A new class of the stramenopiles, Placididea classis nova: description of Placidia cafeteriopsis gen. et sp. nov. Protist 153:143–156PubMedCrossRefGoogle Scholar
  105. Müller DG, Küpper FC, Küpper H (1999) Infection experiments reveal feoad host ranges of Eurychasma dicksonii (Oomycota) and Chytridium polysiphoniae (Chytridicmyaejta), two eukaryotic parasites in marine brown algae (Phaeophyceae). Phycol Res 47:217–223Google Scholar
  106. Nikolaev SI, Berney C, Fahrni JF, Bolivar I, Polet S, Mylnikov AP, Aleshin VV, Petrov NB, Pawlowski J (2004) The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Prop Natl Acad Sci USA 101:8066–8071PubMedCrossRefGoogle Scholar
  107. Nishi A, Ishida K, Endoh H (2005) Reevaluation of the evolutionary position of opalinids based on β-tubulin and 18S rDNA phylogenies. J Mol Evol 60:695–705PubMedCrossRefGoogle Scholar
  108. O’Kelly CJ (1989) The evolutionary origin of the brown algae: information from studies of motile cell ultrastructure. In: Green JC, Leadbeater BSC, Diver WL (eds) The chromophyte algae: problems and perspectives. Clarendon Press, Oxford, pp 255–278Google Scholar
  109. O’Kelly CJ (2002) Glossomastix chrysoplasta n. gen., n. sp. (Pinguiophyceae), attew coccoidal, colony-forming golden alga from southern Australia. Phycol Res 50:67–74Google Scholar
  110. O’Kelly C, Nerad T (1998) Kinetid architecture and bicosoecid affinities of me marine heterotrophic nanoflagellate Cqecitellus parvulus (Griessmann 1913) Patterson et al. 1993. Eur J Protistol 34:306–375Google Scholar
  111. Patron NJ, Rogers MB, Keeling PJ (2004) Gene replacement of fructose- 1,6-bisphosphate aldolase bie hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot Cell 3:1169–1175PubMedCrossRefGoogle Scholar
  112. Patterson DJ (1989) Stramenopiles: chromophytes from a protistan perspective. In: Green JC, Leadbeater BS, Diver WL (eds) The chromophyte algae. Clarendon Press, Oxford, pp 357–379Google Scholar
  113. Patterson DJ (2002 dated 2000) Residual heterotrophic stramenopiles. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the Protozoa. Society of Protozoologists, Lawrence, Kansas, pp 751–754Google Scholar
  114. Patterson DJ, Lee WJ (2000) Geographic distribution and diversity of free-living heterotrophic flagpllates. In: Leadbeater BSC, Green JC (eds) The flagellates: unity, diversity and evolution, Taylor and Francis, London, pp 267–287Google Scholar
  115. Patterson DJ, Simpson AGB (1996) Heterotrophic flagellates from coastal marine aiid hypersaline sediments in Western Australia. Eur J Protistol 32:423–448Google Scholar
  116. Patterson DJ, Simpson AGB, Rogerson A (2002a, dated 2000) Amoebae of uncertain affinities. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the Protozoa. Society of Protozoologists, Lawrence, Kansas, pp 804–827Google Scholar
  117. Patterson DJ, Vørs N, Simpson AG, O’Kelly C (2002b, dated 2000) Residual free-living and predatory heterotrophic flagellates. In: Lee JJ, Leedale GF, Bradbury P (eds). An illustrated guide to the Protozoa. Society of Protozoologists, Lawrence, Kansas, pp 1302–1328Google Scholar
  118. Patterson DJ, Zölfell M (1991) Heterotrophic flagellates of uncertain taxonomic position. In: Patterson DJ, Larsen J (eds) The biology of free-living heterotrophic flagellates. Clarendon Press, Oxford, pp 427–476Google Scholar
  119. Pollock DD, Zwicjd DJ, McGuire JA, Hillis DM (2002) Increased taxon sampling is advantageous for phylogenetic inference. Syst Biol 51:664–671PubMedCrossRefGoogle Scholar
  120. Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution, Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  121. Potter D, Saunders GW, Andersen RA (1997) Phylogenetic relationships of the Raphidophyceae and Xanthonhyeeae as inferred from nucleotide sequences of the 18S ribosomal RNA gene. Am J Bot 84:962–972Google Scholar
  122. Preisig H, Andersen RA (2002, dated 2000) Chrysomonada (class Chrysophyceae Pascher, 1914). In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the Protozoa, Society of Protozoologists, pp 693–730Google Scholar
  123. Preisig H, Vørs N, Hällfors G (1991) Diversity of heterotrophic heterokont flagellates. In: Patterson DJ, Larsen J (eds) The biology of free-living heterotrophic flagellates. Clarendon Press, Oxford, pp 361–399Google Scholar
  124. Preparata RM, Beam CA, Himes M, Nanney DL, Meyer EB, Simon EM (1992) Crypthecodinium and Tetrahymena: an exercise in comparative evolution. J Mol Evol 34:209–218PubMedCrossRefGoogle Scholar
  125. Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436:1113–1118PubMedCrossRefGoogle Scholar
  126. Ruinen J, (1938) Notizen der Salzflagellaten: II. Über die Verbreitung der Salzflagellaten, Archiv Protistenk 90:210–218Google Scholar
  127. Ryall K, Harper JT, Keeling PJ (2003) Plastid-derived Type II fatty acid biosynthetic enzymes in chromists. Gene 313:139–148PubMedCrossRefGoogle Scholar
  128. Sáez AG, Probert I, Geisen M, Quinn P, Young JR, Medlin LK (2003) Pseudo-cryptic speciation in cocgolithophores. Proc Nat Acad Sci USA 100:7163–7168PubMedGoogle Scholar
  129. Saunders GW, Potter D, Andersen RA (1997) Phylogenetic affinities of the Sarcinochrysidales and Chrysomeridales (Heterokonta) based on analyses of molecular and combined data. J Phycol 33:310–318Google Scholar
  130. Saunders GW, Potter D, Paskind MP, Andersen RA (1995) Cladistic analysis of combined traditional and molecular data sets reveal an algal lineage. Proc Natl Acad Sci USA 92:244–248PubMedGoogle Scholar
  131. Scheckenbach F, Wylezich C, Weitere M, Hausmann K, Anidt H (2005) Molecular identity of strains of heterotrophic flagellates isolated from surface waters and deep-sea sediments of the South Atlantic based on SSU rDNA. Aquatic Microbial Ecol 38:239–247Google Scholar
  132. Schnepf E, Drebes G, Elbrächter M (1990) Pirsonia guinardiae, gen, et spec, nov.: a parasitic flagellate on the marine diatom Guinardia flaccida with an unusual mode of food uptake, Helgol Meeresunters 44:275–293Google Scholar
  133. Sekiguchi H, Moriya M, Nakayaina T, Inouye I (2002) Vestigial chloroplasts in heterotrophic stramenopiles Pteridomonas danica and Ciliophrys infusionum (Dictyochophyceae). Protist 153:157–167 PubMedCrossRefGoogle Scholar
  134. Silberman JD, Sogin ML, Leipe DD, Clark CG (1996) Human parasite finds taxonomic home. Nature380–398Google Scholar
  135. Skuja H (1956) Taxonomische und biologische Studien iiber das Phytoplankton schwedischer Binnengewässer. Nov Act Reg Soc Sci Uppsal Ser 4/16:1–404Google Scholar
  136. Patterson DJ (1986) An analysis of heliozoan interrelationships: an example of the potentials and limitations ultrastructural approaches to the study of protistan phytogeny, Proc R Soc Lond B 227:325–366Google Scholar
  137. Stechmann A, Cavalier-Smith T (2002) Rooting the eukaryote tree by using a derived gene fusion. Science 297:89–91PubMedCrossRefGoogle Scholar
  138. Stechmann A, Cavalier-Smith T (2003a) The root of the eukaryote tree pinpointed. Curr Biol 13:R665–R666CrossRefGoogle Scholar
  139. Stechmann A, Cavalier-Smith (2003b) Phylogenetic analysis of eukaryotes using heat-shock protein Hsp90. J Mol Evol 57:408–419CrossRefGoogle Scholar
  140. Stein FR (1878) Der Organismus der Infusionsthiere. III. Der Organismus der Flagellaten I. Engelmann, LeipzigGoogle Scholar
  141. Strüder-Kypke MC, Hausmann K (1998) Ultrastructure of the heterotrophic flagellates Cyathobodo sp., Rhipidodendron huxleyi Kent, 1880, Spongomonas saccculus Kent, 1880, and Spongomonas sp. Eur J Protistol 34:376–390Google Scholar
  142. Swofford DW (1999) PAUP* 4.0b10. Sinauer Sunderland, MSGoogle Scholar
  143. Thomsen HA, Larsen J (1993) The ultrastructure of Commation gen. nov. (stramenopiles incertae sedis), a genus of heterotrophic nanoplanktonic flagellates from Antarctic waters. Eur J Protistol 29:462–477Google Scholar
  144. Tong SM (1995) Developayella elegans nov. gen., spec., a new type of heterotrophic flagellate from marine plankton. Eur J Protistol 31:24–31Google Scholar
  145. Tong SM (1997) Heterotrophic flagellates and other protists from Southampton Water, UK. Ophelia 47:71–131Google Scholar
  146. van de Peer Y, Baldauf SL, Doolittle WF, Meyer A (2000) An updated and comprehensive rRNA phylogpv of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51:565–576PubMedGoogle Scholar
  147. Verhagen FJM, Zölffel M, Brugerolle G, Patterson DJ (1994) Adriamonas peritocrescems gen. nov., sp. nov., a new free-living soil flagellate (Protista, Pseudodendromonadidae incertae sedis). Eur J Protistol 30:295–308Google Scholar
  148. von der Heyden S, Chao EE, Cavalier-Smith T (2004a) Genetic diversity ofgoniGmonads: an ancient divergence between marine and freshwater species. Bur J Phycol 39:343–550Google Scholar
  149. von der Heyden S, Chao EE, Vickerman K, Cavalier-Smith T (2004b) Ribosomal RNA phylogew bodonid and diplonemid flagellates and the evolution of Euglenozoa. J Euk Microbiol 51:402–416Google Scholar
  150. von der Heyden S, Cavalier-Smith T (2005) Culturing and environmental DNA sequencing uncover hidden kinetoplastid biodiversity and a major marine clade within ancestrally freshwater Neobodo designis. Int J Syst Evol Microbiol 55:2605–2621PubMedGoogle Scholar
  151. Vørs N (1992) Heterotrophic amoebae, flagellates and heliozoa from the Tvärminne area, Gulf of Finland, in 1988–1990. Ophelia 36:1–109Google Scholar
  152. Wenderoth K, Marquardt J, Fraunholz M, Van de Peer Y, Wastl J, Maier U-G (1999) The taxonomic position of Chlamydomyxa labyrinthuloides. Europ J Phycol 34:97–108Google Scholar
  153. Wylezich C, Meisterfeld R, Meisterfeld S, Schlegel M (2002) Phylogenetic analyses of small subunit ribosomal RNA coding regions reveal a monophyktic lineage of euglyphid testate amoebae (Order Euglyphida). J Eukaryot Microbiol 49:108–118PubMedCrossRefGoogle Scholar
  154. Yoon HS, Hackett JD, Pinto G, Bhattacharya JD (2002) The single, ancient origin of chromist plastids, Proc Natl Acad Sci USA 99:15507–15512PubMedGoogle Scholar
  155. Zettler LAA, Nerad TA, O’Kelly CJ, Sogin ML (2001) The nueleariid amoebae: more protists at the animal-fungal boundary. J Eukaryot Microbiol 48:293–297PubMedCrossRefGoogle Scholar
  156. Zwickl DJ, Hillis DM (2002) Increased taxon sampling greatly reduces phylogenetic error. Syst Biol 51:588–598PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of OxfordOxfordUK

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