An enigmatic GAPDH gene in the symbiotic dinoflagellate genus Symbiodinium and its related species (the order Suessiales): possible lateral gene transfer between two eukaryotic algae, dinoflagellate and euglenophyte.

A group of unicellular eukaryotic algae, the dinoflagellates, are known to possess two types of gene for glyceraldehyde-3-phosphate dehydrogenase (GAPDH). An enzyme encoded by one type of gene possibly plays a key role in the glycolytic pathway of the cytosol and the other in the Calvin cycle of plastids. In the present study, an additional type of GAPDH gene (GapC3) was found in the symbiotic dinoflagellates, Symbiodinium spp. and their related species, Gymnodinium simplex and Polarella glacialis, all of which belong to the order Suessiales. Since no intracellular translocation signal is found at both amino- and carboxy-termini of its deduced amino acid sequence, the protein is predicted to function in the cytosol. However, it may not be involved in glycolysis due to the presence of an amino acid signature that allows binding for NADP+. It is likely that dinoflagellate species, other than Suessiales investigated in this study, lack this type of GAPDH. Phylogenetic analysis placed GapC3 from the Suessialean species firmly in the clade composed of GAPDH from spirochetes, euglenophytes (cytosolic type) and kinetoplastids (glycosomal type). Specifically, this enigmatic GAPDH gene in dinoflagellates was closely related to its cytosolic counterpart in euglenophytes. It has been previously reported that plastid-targeted (Calvin cycle) GAPDH genes of the dinoflagellates Pyrocystis spp. and that of the euglenophyte Euglena gracilis also seem to share a common ancestor. It appears highly likely that at least two genes (cytosolic and plastid-targeted GAPDH genes) have been laterally transferred between these two eukaryotic algal groups.

[1]  Debashish Bhattacharya,et al.  A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[2]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[3]  W. Martin,et al.  A nuclear gene of eubacterial origin in Euglena gracilis reflects cryptic endosymbioses during protist evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Kawachi,et al.  PHYLOGENETIC POSITION OF SYMBIODINIUM (DINOPHYCEAE) ISOLATES FROM TRIDACNIDS (BIVALVIA), CARDIIDS (BIVALVIA), A SPONGE (PORIFERA), A SOFT CORAL (ANTHOZOA), AND A FREE‐LIVING STRAIN , 1999 .

[5]  C. Valentin,et al.  The evolutionary origin of red algae as deduced from the nuclear genes encoding cytosolic and chloroplast glyceraldehyde-3-phosphate dehydrogenases from Chondrus crispus , 1994, Journal of Molecular Evolution.

[6]  M. Fraunholz,et al.  Evidence for nucleomorph to host nucleus gene transfer: light-harvesting complex proteins from cryptomonads and chlorarachniophytes. , 2000, Protist.

[7]  T. Fagan,et al.  Phylogenetic analysis indicates multiple origins of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes in dinoflagellates. , 2002, Molecular biology and evolution.

[8]  W. Martin,et al.  Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. , 2000, Molecular biology and evolution.

[9]  B. Green,et al.  Second- and third-hand chloroplasts in dinoflagellates: Phylogeny of oxygen-evolving enhancer 1 (PsbO) protein reveals replacement of a nuclear-encoded plastid gene by that of a haptophyte tertiary endosymbiont , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  E. Viscogliosi,et al.  Phylogenetic Relationships of the Glycolytic Enzyme, Glyceraldehyde-3-Phosphate Dehydrogenase, from Parabasalid Flagellates , 1998, Journal of Molecular Evolution.

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

[12]  T. Maruyama,et al.  CONSPECIFICITY AND INDO‐PACIFIC DISTRIBUTION OF SYMBIODINIUM GENOTYPES (DINOPHYCEAE) FROM GIANT CLAMS , 2000 .

[13]  P. Keeling,et al.  Diplonemid glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and prokaryote-to-eukaryote lateral gene transfer. , 2001, Protist.

[14]  J. Palmer,et al.  Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A. Uchida,et al.  Molecular cloning and nucleotide sequence analysis of psbA from the dinoflagellates: Origin of the dinoflagellate plastid , 1999 .

[16]  Martin Vingron,et al.  TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing , 2002, Bioinform..

[17]  H. Brinkmann,et al.  Cloning and sequence analysis of cDNAs encoding the cytosolic precursors of subunits GapA and GapB of chloroplast glyceraldehyde-3-phosphate dehydrogenase from pea and spinach , 2004, Plant Molecular Biology.

[18]  S. Whelan,et al.  A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. , 2001, Molecular biology and evolution.

[19]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[20]  F. Opperdoes,et al.  The cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase from Trypanosoma brucei. Kinetic properties and comparison with homologous enzymes. , 1991, European journal of biochemistry.

[21]  L. Katz,et al.  Lateral gene transfers and the evolution of eukaryotes: theories and data. , 2002, International journal of systematic and evolutionary microbiology.

[22]  G. Procaccini,et al.  POLARELLA GLACIALIS, GEN. NOV., SP. NOV. (DINOPHYCEAE): SUESSIACEAE ARE STILL ALIVE! , 1999 .

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

[24]  James A. Lake,et al.  Mix and Match in the Tree of Life , 1999, Science.

[25]  H. Brinkmann,et al.  Glyceraldehyde-3-phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra- and inter-kingdom gene transfer. , 1999, Molecular biology and evolution.

[26]  Y. Mély,et al.  Determinants of coenzyme specificity in glyceraldehyde-3-phosphate dehydrogenase: role of the acidic residue in the fingerprint region of the nucleotide binding fold. , 1993, Biochemistry.

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

[28]  P. Keeling,et al.  Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[29]  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.

[30]  R. Figge,et al.  GAPDH gene diversity in spirochetes: a paradigm for genetic promiscuity. , 2001, Molecular biology and evolution.

[31]  Doolittle Wf.  Phylogenetic Classification and the Universal Tree , 1999 .

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

[33]  T. Maruyama,et al.  Comparison of phylogenies based on nuclear-encoded SSU rDNA and plastid-encoded psbA in the symbiotic dinoflagellate genus Symbiodinium , 2003 .

[34]  W. Martin,et al.  Evidence for a chimeric nature of nuclear genomes: eubacterial origin of eukaryotic glyceraldehyde-3-phosphate dehydrogenase genes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[35]  T. L. Smith.  Disparate evolution of yeasts and filamentous fungi indicated by phylogenetic analysis of glyceraldehyde-3-phosphate dehydrogenase genes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Ø. Moestrup,et al.  Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates , 2000 .

[37]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.