Re-examining Alveolate Evolution Using Multiple Protein Molecular Phylogenies

Abstract Alveolates are a diverse group of protists that includes three major lineages: ciliates, apicomplexa, and dinoflagellates. Among these three, it is thought that the apicomplexa and dinoflagellates are more closely related to one another than to ciliates. However, this conclusion is based almost entirely on results from ribosomal RNA phylogeny because very few morphological characters address this issue and scant molecular data are available from dinoflagellates. To better examine the relationships between the three major alveolate groups, we have sequenced six genes from the non-photosynthetic dinoflagellate, Crypthecodinium cohnii: actin, beta-tubulin, hsp70, BiP, hsp90, and mitochondrial hsp10. Beta-tubulin, hsp70, BiP, and hsp90 were found to be useful for intra-alveolate phylogeny, and trees were inferred from these genes individually and in combination. Trees inferred from individual genes generally supported the apicomplexa-dinoflagellate grouping, as did a combined analysis of all four genes. However, it was also found that the outgroup had a significant effect on the topology within alveolates when using certain methods of phylogenetic reconstruction, and an alternative topology clustering dinoflagellates and ciliates could not be rejected by the combined data. Altogether, these results support the sisterhood of apicomplexa and dinoflagellates, but point out that the relationship is not as strong as is often assumed.

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

[2]  A. Grossman,et al.  The gene family encoding the fucoxanthin chlorophyll proteins from the brown alga Macrocystis pyrifera , 1995, Molecular and General Genetics MGG.

[3]  A. Tartar,et al.  Phylogenetic analysis identifies the invertebrate pathogen Helicosporidium sp. as a green alga (Chlorophyta). , 2002, International journal of systematic and evolutionary microbiology.

[4]  T. Cavalier-smith,et al.  Dinoflagellate Nuclear SSU rRNA Phylogeny Suggests Multiple Plastid Losses and Replacements , 2001, Journal of Molecular Evolution.

[5]  P. Keeling.  Foraminifera and Cercozoa are related in actin phylogeny: two orphans find a home? , 2001, Molecular biology and evolution.

[6]  Satoru Miyano,et al.  Views: Fundamental Building Blocks in the Process of Knowledge Discovery , 2001, FLAIRS.

[7]  D. Roos,et al.  Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. , 2001, Molecular biology and evolution.

[8]  W. Ford Doolittle,et al.  An Updated and Comprehensive rRNA Phylogeny of (Crown) Eukaryotes Based on Rate-Calibrated Evolutionary Distances , 2000, Journal of Molecular Evolution.

[9]  A. Rodrigo,et al.  Likelihood-based tests of topologies in phylogenetics. , 2000, Systematic biology.

[10]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[11]  T. Cavalier-smith,et al.  Phylogeny of Ultra-Rapidly Evolving Dinoflagellate Chloroplast Genes: A Possible Common Origin for Sporozoan and Dinoflagellate Plastids , 2000, Journal of Molecular Evolution.

[12]  A. Halpern,et al.  Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. , 2000, Molecular biology and evolution.

[13]  G. McFadden,et al.  The secondary endosymbiont of the cryptomonad Guillardia theta contains alpha-, beta-, and gamma-tubulin genes. , 1999, Molecular biology and evolution.

[14]  Hidetoshi Shimodaira,et al.  Multiple Comparisons of Log-Likelihoods with Applications to Phylogenetic Inference , 1999, Molecular Biology and Evolution.

[15]  T. Cavalier-smith,et al.  Single gene circles in dinoflagellate chloroplast genomes , 1999, Nature.

[16]  F. Taylor.  MORPHOLOGY (TABULATION) AND MOLECULAR EVIDENCE FOR DINOFLAGELLATE PHYLOGENY REINFORCE EACH OTHER , 1999 .

[17]  D. Morse,et al.  The Phylogeny of Glyceraldehyde-3-Phosphate Dehydrogenase Indicates Lateral Gene Transfer from Cryptomonads to Dinoflagellates , 1998, Journal of Molecular Evolution.

[18]  H. Philippe,et al.  How good are deep phylogenetic trees? , 1998, Current opinion in genetics & development.

[19]  D. Roos,et al.  Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  G. McFadden,et al.  The Phylogenetic Position of Alpha‐ and Beta‐Tubulins from the Chlorarachnion Host and Cercomonas (Cercozoa) , 1998, The Journal of eukaryotic microbiology.

[21]  Yves Van de Peer,et al.  Evolutionary Relationships Among the Eukaryotic Crown Taxa Taking into Account Site-to-Site Rate Variation in 18S rRNA , 1997, Journal of Molecular Evolution.

[22]  J. Ajioka,et al.  The protozoan phylum Apicomplexa. , 1997, Methods.

[23]  T. Ohama,et al.  Algae or Protozoa: Phylogenetic Position of Euglenophytes and Dinoflagellates as Inferred from Mitochondrial Sequences , 1997, Journal of Molecular Evolution.

[24]  The cytochrome oxidase subunit 1 gene (cox1) from the dinoflagellate, Crypthecodinium cohnii , 1997, FEBS letters.

[25]  J. Graves,et al.  ‘Total evidence’ refutes the inclusion of Perkinsus species in the phylum Apicomplexa , 1997, Parasitology.

[26]  J. Graves,et al.  Phylogenetic analysis of Perkinsus based on actin gene sequences. , 1997, The Journal of parasitology.

[27]  O Gascuel,et al.  BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. , 1997, Molecular biology and evolution.

[28]  J. Palmer,et al.  A Plastid of Probable Green Algal Origin in Apicomplexan Parasites , 1997, Science.

[29]  R. Lévesque,et al.  Secondary structures and features of the 18S, 5.8S and 26S ribosomal RNAs from the Apicomplexan parasite Toxoplasma gondii. , 1996, Gene.

[30]  K. Strimmer,et al.  Quartet Puzzling: A Quartet Maximum-Likelihood Method for Reconstructing Tree Topologies , 1996 .

[31]  M. Strath,et al.  Complete gene map of the plastid-like DNA of the malaria parasite Plasmodium falciparum. , 1996, Journal of molecular biology.

[32]  Geoffrey I. McFadden,et al.  Plastid in human parasites , 1996, Nature.

[33]  Y Van de Peer,et al.  The evolution of stramenopiles and alveolates as derived by "substitution rate calibration" of small ribosomal subunit RNA. , 1996, Journal of molecular evolution.

[34]  Smith Rf,et al.  Pattern-induced multi-sequence alignment (PIMA) algorithm employing secondary structure-dependent gap penalties for use in comparative protein modelling. , 1992 .

[35]  R. F. Smith,et al.  Pattern-induced multi-sequence alignment (PIMA) algorithm employing secondary structure-dependent gap penalties for use in comparative protein modelling. , 1992, Protein engineering.

[36]  M. Sogin,et al.  Ribosomal RNA sequences of Sarcocystis muris, Theileria annulata and Crypthecodinium cohnii reveal evolutionary relationships among apicomplexans, dinoflagellates, and ciliates. , 1991, Molecular and biochemical parasitology.

[37]  J. Wolters,et al.  The troublesome parasites--molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. , 1991, Bio Systems.

[38]  F. Tailor.  The biology of Dinoflagellates , 1987 .

[39]  John J. Lee,et al.  An illustrated guide to the protozoa , 1985 .

[40]  F. Taylor,et al.  Flagellate Phylogeny: A Study in Conflicts* , 1976 .