Plant-like traits associated with metabolism of Trypanosoma parasites

Abstract

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.

Figure 1

Alignment of the T. brucei FBPase (F16P_TRYBB) and SBPase (S17P_TRYBB) sequences with three representative FBPases and all of the other SBPases in the SWISS-PROT database. Bold letters mark positions entirely conserved in a full alignment of all of the SWISS-PROT database entries containing the FBPase/SBPase family PROSITE signature. Red, green, and blue shading mark residues interacting with the 1-phosphate, sugar, and 6/7-phosphate moieties of substrate, respectively, as observed by crystallographic analysis of pig liver FBPase (40). Both T. brucei sequences carry a PTS1 (C-terminal -SKL), and the FBPase carries a potential PTS2 (residues 6–13, RVxxxxxQF).

Figure 2

Neighbor-joining tree of SBPases and FBPases. The T. brucei SBPase and FBPase sequences were compared with the complete SWISS-PROT database for homologous sequences by using the BLASTP algorithm. The best scoring 43 homologous protein sequences were aligned by using the program clustalw (14). The alignment, after removal of all regions with insertions and deletions, was used for the creation of a neighbor-joining tree. A maximum-likelihood tree was created by using the program treepuzzle (16) with 1,000 puzzle steps and the JTT correction as an evolutionary model (17). Bootstrap values (1,000 samplings) obtained by the neighbor-joining method are indicated above the branches, while the puzzle frequencies (1,000 puzzle steps) are indicated below the branches. The horizontal bar represents the equivalent of 10 substitutions per 100 residues.

Figure 3

Phylogenetic tree of FBPase aldolases. The T. brucei FBPase aldolase sequence was compared with the complete SWISS-PROT database for homologous sequences using the blastp algorithm. The best scoring 37 protein sequences were aligned by using the program clustalw (14). Neighbor-joining and maximum-likelihood trees were prepared as described in the legend to Fig. 1. Neighbor-joining bootstrap values are indicated above the branches, and puzzle frequencies (1,000 puzzle steps) are indicated below the branches. The horizontal bar represents the equivalent of 10 substitutions per 100 residues.