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.

Origin and Distribution of Calvin Cycle Fructose and Sedoheptulose Bisphosphatases in Plantae and Complex Algae: A Single Secondary Origin of Complex Red Plastids and Subsequent Propagation via Tertiary Endosymbioses

“…2), and thus favor a red algal origin of the apicoplast in the long-standing dispute about its endosymbiotic ancestry (Funes et al 2002(Funes et al , 2003Rogers and Keeling 2004;Waller et al 2003). The trypanosomal SBP was previously proposed to be a relict of a common photosynthetic ancestor of all Euglenozoa (Hannaert et al 2003). However, our analyses strongly indicate that the SBP of Euglena is of green algal endosymbiotic origin (Fig.…”

“…Several phylogenetic analyses of SBP and FBP sequences have shown that they are homologous and demonstrated the highly distinct nature of the monophyletic SBP subtree (Hannaert et al 2003;Martin et al 1996;Rogers and Keeling 2004). Figure 2 shows the maximum likelihood tree (PhyML) of 37 eukaryotic SBP sequences based on 197 aa positions.…”

“…Thus, SBP may represent a promising test system for open questions of eukaryotic evolution including the examination of the relationships of complex algae that originated via eukaryote-toeukaryote endosymbioses (see above). Given its presumably specific function within the Calvin cycle, the presence of a SBP gene in the agent of sleeping sickness, Trypanosoma brucei, has been regarded as a strong argument for a photosynthetic ancestry of the Euglenozoa (Hannaert et al 2003;Martin and Borst 2003;Rogers and Keeling 2004).…”

A trypanothione-dependent glyoxalase I with a prokaryotic ancestry in Leishmania major

“…Thus, the unambiguous demonstration of the requirement of the L. major GLO1 for nickel, but not zinc, by metal analysis and reconstitution is important in confirming the unique relationship of these eukaryotic glyoxalases to the E. coli enzyme. Importantly, the similarity in sequence to cyanobacterial enzymes suggests that the presence of these genes in the trypanosomatids may be the result of gene transfer from an ancestral endosymbiont (33). It is interesting that a rice GLO1 that is of bacterial origin and belongs to a group of plant glyoxalases with strong sequence similarity to the bacterial enzymes has been identified (34).…”

Gene transfer in the evolution of parasite nucleotide biosynthesis

“…This evidence, combined with the presence of the bifunctional enzyme dihydrofolate reductase-thymidylate synthase, DHFR, in C. parvum (33) and other apicomplexans provides an additional phylogenetic link between the Apicomplexa and plants. Whether the presence of both fused genes in these lineages indicates monophyly (21, 22) or multiple independent gene transfers (34) remains to be determined. Our discovery of a TK gene of ␣-or ␥-proteobacterial ancestry in C. parvum represents a second, and probably distinct eubacterial horizontal gene transfer because IMPDH was acquired from an -proteobacterium (9).…”