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T. Cavalier-Smith et al./Molecular Phylogenetics and Evolution 81 (2014) 71–85

Multigene eukaryote phylogeny reveals the likely protozoan ancestors of opisthokonts (animals, fungi, choanozoans) and Amoebozoa

Thomas Cavalier-Smith[1], Ema E. Chao, Elizabeth A. Snell, Cédric Berney[2], Anna Maria Fiore-Donno[3], Rhodri Lewis

Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

ARTICLE INFO ABSTRACT
Article history:

Received 24 January 2014
Revised 2 August 2014
Accepted 11 August 2014
Available online 23 August 2014

Animals and fungi independently evolved from the protozoan phylum Choanozoa, these three groups constituting a major branch of the eukaryotic evolutionary tree known as opisthokonts. Opisthokonts and the protozoan phylum Amoebozoa (amoebae plus slime moulds) were previously argued to have evolved independently from the little-studied, largely flagellate, protozoan phyl| Animals and fungi independently evolved from the protozoan phylum Choanozoa, these three groups constituting a major branch of the eukaryotic evolutionary tree known as opisthokonts. Opisthokonts and the protozoan phylum Amoebozoa (amoebae plus slime moulds) were previously argued to have evolved independently from the little-studied, largely flagellate, protozoan phylum, Sulcozoa. Sulcozoa are a likely evolutionary link between opisthokonts and the more primitive excavate flagellates that have ventral feeding grooves and the most primitive known mitochondria. To extend earlier sparse evidence for the ancestral (paraphyletic) nature of Sulcozoa, we sequenced transcriptomes from six gliding flagellates (two apusomonads; three planomonads; Mantamonas). Phylogenetic analyses of 173–192 genes and 73–122 eukaryote-wide taxa show Sulcozoa as deeply paraphyletic, confirming that opisthokonts and Amoebozoa independently evolved from sulcozoans by losing their ancestral ventral groove and dorsal pellicle: Apusozoa (apusomonads plus anaerobic breviate amoebae) are robustly sisters to opisthokonts and probably paraphyletic, breviates diverging before apusomonads; Varisulca (planomonads, Mantamonas, and non-gliding flagellate Collodictyon) are sisters to opisthokonts plus Apusozoa and Amoebozoa, and possibly holophyletic; Glissodiscea (planomonads, Mantamonas) may be holophyletic, but Mantamonas sometimes groups with Collodictyon instead. Taxon and gene sampling slightly affects tree topology; for the closest branches in Sulcozoa and opisthokonts, proportionally reducing missing data eliminates conflicts between homogeneous-model maximum-likelihood trees and evolutionarily more realistic site-heterogeneous trees. Sulcozoa, opisthokonts, and Amoebozoa constitute an often-pseudopodial 'podiate' clade, one of only three eukaryotic 'supergroups'. Our trees indicate that evolution of sulcozoan dorsal pellicle, ventral pseudopodia, and ciliary gliding (probably simultaneously) generated podiate eukaryotes from Malawimonas-like excavate flagellates.

© 2014 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/)

Keywords:

Cell evolution
Eukaryote phylogeny
Podiates
Protozoa
Transcriptome sequencing
Sulcozoa


1. Introduction


Phylogenetically, all eukaryotes have been assigned to just three supergroups: podiates, corticates (kingdoms Plantae and Chromista), and Eozoa (excavates and Euglenozoa)[4]. The entirely heterotrophic podiates, the focus of this paper, include Animalia, Fungi, and four protozoan phyla (Sulcozoa, Amoebozoa, Choanozoa Microsporidia); they are so called because of the general presence of pseudopodia except in the derived Fungi that lost them[4]. Originally 'excavates' excluded Euglenozoa[5], but later these distinctive flagellates were included despite not sharing excavate morphology[6][7][8] under the influence of a probably erroneous assumption about the location of the eukaryotic root; here we follow[9][4] in excluding Euglenozoa from excavates. Multigene trees usually show corticates as a clade, but are contradictory concerning the boundary between the excavate Eozoa and the putatively basal podiate phylum Sulcozoa. The problem lies in the uncertain phylogenetic position of the excavate flagellate Malawimonas[10][11][12][13][14]). Some multigene trees show podiates as a clade with Malawimonas one node deeper (e.g.[10]); others place Malawimonas within podiates, typically as sister to the sulcozoan flagellate Collodictyon (e.g.

http://dx.doi.org/10.1016/j.ympev.2014.08.012
1055-7903/© 2014 The Authors. Published by Elsevier Inc.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).

  1. ↑ Corresponding author.
    E-mail address: tom.cavalier-smith@zoo.ox.ac.uk (T. Cavalier-Smith).
  2. ↑ Present address: Station Biologique de Roscoff, UMR7144/Groupe Evolution et10 PaléOcéans, CNRS/Université Paris VI, Roscoff, France.
  3. ↑ Present address: Zoology Institute, Terrestrial Ecology Group, Faculty of Mathematics and Natural Sciences, University of Cologne, Biozentrum Köln, Zülpicher Str. 47b, D-50674 Köln, Germany.
  4. ↑ 4.0 4.1 4.2 Cavalier-Smith, T., 2013a. Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa. Eur. J. Protistol. 49, 115–178.
  5. ↑ Simpson, A.G.B., Patterson, D.J., 1999. The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the excavate hypothesis. Eur. J. Protistol. 35, 353–370.
  6. ↑ Cavalier-Smith, T., 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297–354.
  7. ↑ Cavalier-Smith, T., 2003. The excavate protozoan phyla Metamonada Grassé emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. Int. J. Syst. Evol. Microbiol. 53, 1741–1758.
  8. ↑ Simpson, A.G.B., 2003. Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). Int. J. Syst. Evol. Microbiol. 53, 1759–1777.
  9. ↑ Cavalier-Smith, T., 2010a. Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree. Biol. Lett. 6, 342–345.
  10. ↑ 10.0 10.1 Brown, M.W., Sharpe, S.C., Silberman, J.D., Heiss, A.A., Lang, F.B., Simpson, A.G.B., Roger, A.J., 2013. Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads. Proc. R. Soc. B 280, 20131755.
  11. ↑ Derelle, R., Lang, F.B., 2012. Rooting the eukaryotic tree with mitochondrial and bacterial proteins. Mol. Biol. Evol. 29, 1277–1289.
  12. ↑ Hampl, V., Hug, L., Leigh, J.W., Dacks, J.B., Lang, F.B., Simpson, A.G.B., Roger, A.J., 2009. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Proc. Natl. Acad. Sci. USA 106, 3859–3864.
  13. ↑ Zhao, S., Burki, F., Bråte, J., Keeling, P.J., Klaveness, D., Shalchian-Tabrizi, K., 2012. Collodictyon – an ancient lineage in the tree of eukaryotes. Mol. Biol. Evol. 29, 1557–1568.
  14. ↑ Zhao, S., Shalchian-Tabrizi, K., Klaveness, D., 2013. Sulcozoa revealed as a paraphyletic group in mitochondrial phylogenomics. Mol. Phylogenet. Evol. 69, 462–468.
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