Plant-like traits associated with metabolism of Trypanosoma parasites

Trypanosomatid parasites cause serious diseases among humans, livestock, and plants. They belong to the order of the Kinetoplastida and form, together with the Euglenida, the phylum Euglenozoa. Euglenoid algae possess plastids capable of photosynthesis, but plastids are unknown in trypanosomatids. Here we present molecular evidence that trypanosomatids possessed a plastid at some point in their evolutionary history. Extant trypanosomatid parasites, such as Trypanosoma and Leishmania, contain several “plant-like” genes encoding homologs of proteins found in either chloroplasts or the cytosol of plants and algae. The data suggest that kinetoplastids and euglenoids acquired plastids by endosymbiosis before their divergence and that the former lineage subsequently lost the organelle but retained numerous genes. Several of the proteins encoded by these genes are now, in the parasites, found inside highly specialized peroxisomes, called glycosomes, absent from all other eukaryotes, including euglenoids.

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

[2]  T. Cavalier-smith,et al.  Membrane heredity and early chloroplast evolution. , 2000, Trends in plant science.

[3]  F. Opperdoes,et al.  The evolutionary origin of glycosomes. , 1991, Parasitology today.

[4]  H. Lichtenthaler,et al.  Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. , 1999, Science.

[5]  G. C. Hill,et al.  Cloning, sequencing, and functional activity of the Trypanosoma brucei brucei alternative oxidase. , 1996, Molecular and biochemical parasitology.

[6]  F. Opperdoes,et al.  Purification, localisation and characterisation of glucose-6-phosphate dehydrogenase of Trypanosoma brucei. , 1999, Molecular and biochemical parasitology.

[7]  F. Opperdoes,et al.  Molecular analysis of the cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase in Leishmania mexicana. , 1992, Molecular and biochemical parasitology.

[8]  C. Clayton,et al.  Protein trafficking in kinetoplastid protozoa. , 1995, Microbiological reviews.

[9]  J Van Roy,et al.  Molecular characterization of the first two enzymes of the pentose-phosphate pathway of Trypanosoma brucei. Glucose-6-phosphate dehydrogenase and 6-phosphogluconolactonase. , 2000, The Journal of biological chemistry.

[10]  W. Martin,et al.  Purification and cloning of chloroplast 6-phosphogluconate dehydrogenase from spinach. Cyanobacterial genes for chloroplast and cytosolic isoenzymes encoded in eukaryotic chromosomes. , 2001, European journal of biochemistry.

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

[12]  P. A. Rea,et al.  Vacuolar H(+) pyrophosphatases: from the evolutionary backwaters into the mainstream. , 2001, Trends in plant science.

[13]  W. Gross,et al.  Chloroplast class I and class II aldolases are bifunctional for fructose‐1,6‐biphosphate and sedoheptulose‐1,7‐biphosphate cleavage in the Calvin cycle , 1999, FEBS letters.

[14]  F. Opperdoes,et al.  Demonstration of glycosomes (microbodies) in the Bodonid flagellate Trypanoplasma borelli (Protozoa, Kinetoplastida). , 1988, Molecular and biochemical parasitology.

[15]  R. Ridley.  Planting the Seeds of New Antimalarial Drugs , 1999, Science.

[16]  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.

[17]  Andrew J. Roger,et al.  A Cyanobacterial Gene in Nonphotosynthetic Protists—An Early Chloroplast Acquisition in Eukaryotes? , 2002, Current Biology.

[18]  F. Opperdoes,et al.  Localization of nine glycolytic enzymes in a microbody‐like organelle in Trypanosoma brucei: The glycosome , 1977, FEBS letters.

[19]  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.

[20]  R. Wilson,et al.  Progress with parasite plastids. , 2002, Journal of molecular biology.

[21]  P. T. Englund,et al.  Specialized fatty acid synthesis in African trypanosomes: myristate for GPI anchors. , 2000, Science.

[22]  C. Greenblatt,et al.  Synthesis of ca-Linolenic Acid by Leishmania enriettii , 1963, Science.

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

[24]  P. T. Englund,et al.  Fatty acid synthesis in African trypanosomes: a solution to the myristate mystery. , 2001, Trends in parasitology.

[25]  William N. Lipscomb,et al.  Crystallographic studies of the catalytic mechanism of the neutral form of fructose-1,6-bisphosphatase. , 1993 .

[26]  F. Opperdoes,et al.  Molecular analysis of phosphoglycerate kinase in Trypanoplasma borreli and the evolution of this enzyme in kinetoplastida. , 1998, Gene.

[27]  F. Opperdoes.  Compartmentation of carbohydrate metabolism in trypanosomes. , 1987, Annual review of microbiology.

[28]  M. Barrett,et al.  A 6-phosphogluconate dehydrogenase gene from Trypanosoma brucei. , 1993, Molecular and biochemical parasitology.

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

[30]  F. Opperdoes,et al.  Cloning and characterization of the NAD-linked glycerol-3-phosphate dehydrogenases of Trypanosoma brucei brucei and Leishmania mexicana mexicana and expression of the trypanosome enzyme in Escherichia coli. , 1996, Molecular and biochemical parasitology.

[31]  W. Martin,et al.  Higher-plant chloroplast and cytosolic fructose-1,6-bisphophosphatase isoenzymes: origins via duplication rather than prokaryote-eukaryote divergence , 1996, Plant Molecular Biology.

[32]  F. Opperdoes,et al.  Characterization of the genes for fructose-bisphosphate aldolase in Trypanosoma brucei. , 1988, Molecular and biochemical parasitology.

[33]  F. Bringaud,et al.  Metabolic aspects of glycosomes in trypanosomatidae - new data and views. , 2000, Parasitology today.

[34]  W. Doolittle.  You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. , 1998, Trends in genetics : TIG.

[35]  J Van Roy,et al.  Trypanosoma brucei contains a 2,3-bisphosphoglycerate independent phosphoglycerate mutase. , 2000, European journal of biochemistry.

[36]  F R Opperdoes,et al.  Cloning and characterization of Leishmania mexicana fructose-1,6-bisphosphate aldolase. , 1999, Molecular and biochemical parasitology.

[37]  J. Cazzulo,et al.  The NAD-linked aromatic α-hydroxy acid dehydrogenase from Trypanosoma cruzi , 1999 .

[38]  F. Opperdoes,et al.  The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship. , 1991, European journal of biochemistry.

[39]  Marianne Grunberg-Manago,et al.  Evolutionary tinkering in gene expression , 1989, NATO ASI Series.