Collodictyon—An Ancient Lineage in the Tree of Eukaryotes

The current consensus for the eukaryote tree of life consists of several large assemblages (supergroups) that are hypothesized to describe the existing diversity. Phylogenomic analyses have shed light on the evolutionary relationships within and between supergroups as well as placed newly sequenced enigmatic species close to known lineages. Yet, a few eukaryote species remain of unknown origin and could represent key evolutionary forms for inferring ancient genomic and cellular characteristics of eukaryotes. Here, we investigate the evolutionary origin of the poorly studied protist Collodictyon (subphylum Diphyllatia) by sequencing a cDNA library as well as the 18S and 28S ribosomal DNA (rDNA) genes. Phylogenomic trees inferred from 124 genes placed Collodictyon close to the bifurcation of the “unikont” and “bikont” groups, either alone or as sister to the potentially contentious excavate Malawimonas. Phylogenies based on rDNA genes confirmed that Collodictyon is closely related to another genus, Diphylleia, and revealed a very low diversity in environmental DNA samples. The early and distinct origin of Collodictyon suggests that it constitutes a new lineage in the global eukaryote phylogeny. Collodictyon shares cellular characteristics with Excavata and Amoebozoa, such as ventral feeding groove supported by microtubular structures and the ability to form thin and broad pseudopods. These may therefore be ancient morphological features among eukaryotes. Overall, this shows that Collodictyon is a key lineage to understand early eukaryote evolution.

[1]  B. Lang,et al.  Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. , 2010, Molecular biology and evolution.

[2]  Y. Inagaki,et al.  Palpitomonas bilix gen. et sp. nov.: A novel deep-branching heterotroph possibly related to Archaeplastida or Hacrobia. , 2010, Protist.

[3]  T. Cavalier-smith Kingdoms Protozoa and Chromista and the eozoan root of the eukaryotic tree , 2010, Biology Letters.

[4]  T. Cavalier-smith,et al.  Myosin domain evolution and the primary divergence of eukaryotes , 2005, Nature.

[5]  R. Guillard,et al.  YELLOW‐GREEN ALGAE WITH CHLOROPHYLLIDE C 1, 2 , 1972 .

[6]  T. Cavalier-smith,et al.  Kingdom protozoa and its 18 phyla. , 1993, Microbiological reviews.

[7]  Heather M. Wilcox,et al.  Newly identified and diverse plastid-bearing branch on the eukaryotic tree of life , 2011, Proceedings of the National Academy of Sciences.

[8]  Y. Inagaki,et al.  Large-Scale Phylogenomic Analyses Reveal That Two Enigmatic Protist Lineages, Telonemia and Centroheliozoa, Are Related to Photosynthetic Chromalveolates , 2009, Genome biology and evolution.

[9]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[10]  E. Koonin,et al.  Analysis of Rare Genomic Changes Does Not Support the Unikont–Bikont Phylogeny and Suggests Cyanobacterial Symbiosis as the Point of Primary Radiation of Eukaryotes , 2009, Genome biology and evolution.

[11]  J. Rougemont,et al.  A rapid bootstrap algorithm for the RAxML Web servers. , 2008, Systematic biology.

[12]  A. Simpson,et al.  Evolutionary relationships of apusomonads inferred from taxon-rich analyses of 6 nuclear encoded genes. , 2006, Molecular biology and evolution.

[13]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[14]  James R. Knight,et al.  Genome sequencing in microfabricated high-density picolitre reactors , 2005, Nature.

[15]  Fabien Burki,et al.  Phylogenomics reveals a new ‘megagroup’ including most photosynthetic eukaryotes , 2008, Biology Letters.

[16]  Surendra Kumar,et al.  AIR: A batch-oriented web program package for construction of supermatrices ready for phylogenomic analyses , 2009, BMC Bioinformatics.

[17]  Hidetoshi Shimodaira An approximately unbiased test of phylogenetic tree selection. , 2002, Systematic biology.

[18]  M. Fiers,et al.  Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists , 2010, BMC Evolutionary Biology.

[19]  Laura Wegener Parfrey,et al.  Evaluating Support for the Current Classification of Eukaryotic Diversity , 2006, PLoS genetics.

[20]  Ramón Doallo,et al.  ProtTest 3: fast selection of best-fit models of protein evolution , 2011, Bioinform..

[21]  H. Philippe,et al.  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. , 2002, Protist.

[22]  Masami Hasegawa,et al.  CONSEL: for assessing the confidence of phylogenetic tree selection , 2001, Bioinform..

[23]  B. Lang,et al.  Toward Resolving the Eukaryotic Tree: The Phylogenetic Positions of Jakobids and Cercozoans , 2007, Current Biology.

[24]  T. Embley,et al.  Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I , 2004, Nature.

[25]  T. Cavalier-smith,et al.  Evolutionary position of breviate amoebae and the primary eukaryote divergence , 2009, Proceedings of the Royal Society B: Biological Sciences.

[26]  A. Simpson,et al.  The real ‘kingdoms’ of eukaryotes , 2004, Current Biology.

[27]  D. Vaulot,et al.  Telonemia, a new protist phylum with affinity to chromist lineages , 2006, Proceedings of the Royal Society B: Biological Sciences.

[28]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

[29]  H. Philippe,et al.  A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. , 2004, Molecular biology and evolution.

[30]  Kamran Shalchian-Tabrizi,et al.  Multigene Phylogeny of Choanozoa and the Origin of Animals , 2008, PloS one.

[31]  K. Jakobsen,et al.  Diversification of unicellular eukaryotes: cryptomonad colonizations of marine and fresh waters inferred from revised 18S rRNA phylogeny. , 2008, Environmental microbiology.

[32]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[33]  L. Hug,et al.  Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups” , 2009, Proceedings of the National Academy of Sciences.

[34]  Kamran Shalchian-Tabrizi,et al.  Phylogenomics Reshuffles the Eukaryotic Supergroups , 2007, PloS one.

[35]  R. Stepanauskas,et al.  Single-Cell Genomics Reveals Organismal Interactions in Uncultivated Marine Protists , 2011, Science.

[36]  Y. Inagaki,et al.  Multiple Gene Phylogenies Support the Monophyly of Cryptomonad and Haptophyte Host Lineages , 2007, Current Biology.

[37]  T. Cavalier-smith,et al.  Rooting the Eukaryote Tree by Using a Derived Gene Fusion , 2002, Science.

[38]  D. Patterson,et al.  The Diversity of Eukaryotes , 1999, The American Naturalist.

[39]  H. J. Carter XXXII.—On the fresh- and salt-water Rhizopoda of England and India , 1865 .

[40]  Edward Susko,et al.  PROCOV: maximum likelihood estimation of protein phylogeny under covarion models and site-specific covarion pattern analysis , 2009, BMC Evolutionary Biology.

[41]  H. Philippe,et al.  Archaea sister group of Bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. , 1999, Molecular biology and evolution.

[42]  A. Simpson,et al.  Evolution: Revisiting the Root of the Eukaryote Tree , 2009, Current Biology.

[43]  L. Katz,et al.  Broadly sampled multigene analyses yield a well-resolved eukaryotic tree of life. , 2010, Systematic biology.

[44]  Aleš Horák,et al.  Molecular Phylogeny and Description of the Novel Katablepharid Roombia truncata gen. et sp. nov., and Establishment of the Hacrobia Taxon nov , 2009, PloS one.

[45]  B. Hoffman,et al.  A simple and very efficient method for generating cDNA libraries. , 1983, Gene.

[46]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[47]  A. Simpson,et al.  Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). , 2003, International journal of systematic and evolutionary microbiology.

[48]  B. Lang,et al.  Rooting the eukaryotic tree with mitochondrial and bacterial proteins. , 2012, Molecular biology and evolution.

[49]  T. Cavalier-smith,et al.  The excavate protozoan phyla Metamonada Grassé emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. , 2003, International journal of systematic and evolutionary microbiology.

[50]  M. P. Cummings PHYLIP (Phylogeny Inference Package) , 2004 .

[51]  L. Katz,et al.  BMC Evolutionary Biology BioMed Central Research article Broadly sampled multigene trees of eukaryotes , 2008 .