Home Economics American Trypanosomiasis Chagas Disease, Second Edition: One Hundred Years of Research
Origin of trypanosomes and the relationship between T. cruzi and T brucei
Trypanosomes are kinetoplastids, which include both free-living and parasitic groups. There has been considerable interest in the transitional steps between the free-living ancestor and trypanosomes which are parasitic at all life cycle stages. Two groups of theories have dominated debate. Vertebrate-first theories proposed that the ancestral trypanosome evolved from a gut parasite of vertebrates,4 while invertebrate-first theories proposed that it evolved from a single-host (monogenetic) invertebrate parasite, similar to the trypanosomatids now found in insect guts.1,5,6
Resolving the relationships between trypanosomes, other trypanosomatids (family Trypanosomatidae) and bodonids is the key to understanding the origin of the genus. Bodonids are mostly free living. All trypanosomatids are parasitic at all stages of their lifecycles. Most trypanosomatid genera (e.g., Blastocrithidia, Crithidia, Herpetomonas, Leptomonas, Sergeia, Wallaceina) are single-host (monogenetic) parasites of insects. Recent studies using molecular methods have led to significant changes to the taxonomy of trypanosomatids and have revealed a large diversity among these insect parasites. Several new genera have been recently described by investigating less-studied insect host groups,32,33 including Sergeia from a biting midge,34 Blechomonas from fleas,35 and Paratrypanosoma from a mosquito.36 Nonetheless, Trypanosoma and Leishmania remain the only two-host (digenetic) vertebrate parasites. The existence of another digenetic vertebrate parasite, Endotrypanum, has not been verified using molecular techniques, as the isolates of this genus examined to date have turned out to be Leishmania.37,38 A few other trypanosomatid genera have been isolated from humans that are either immuno- compromised,39 or coinfected with Leishmania 40, but these are thought not to infect healthy vertebrates. Phytomonas (another digenetic genus) is a parasite of plants, which is also transmitted by insects.41,42
A central question that has been the source of considerable debate is whether trypanosomes are monophyletic. A monophyletic group is a collection of organisms, which form a single clade comprising an ancestor and all its descendants. Monophyly of trypanosomes would indicate that all described taxa within the genus had a single common origin and did not gave rise to other trypanosomatid groups, by for example losing dependence on the vertebrate lifecycle stage. If this had occurred we may expect some of the insect-only trypanosomatids would fall among trypanosomes in the evolutionary tree. The monophyly debate has also been central to resolving whether the two trypanosome groups that include the human pathogens T. brucei and T. cruzi evolved vertebrate parasitism independently.
In several early phylogenetic trees, based on comparisons of genes encoding ribosomal RNAs, trypanosomes appeared paraphyletic.43-45 Often the evolutionary trees obtained from these studies suggested that the clade including T. brucei and related parasites (the “T. brucei” clade) diverged early in trypanosomatid evolution and evolved vertebrate parasitism independently to the other trypanosomes that include T. cruzi. On the other hand, most later studies, also using ribosomal RNA genes, but with substantially increased taxon-sampling, supported monophyly of trypanosomes,8,10,28,46 although several supported paraphyly.9 The issue was resolved using taxon-rich trees based on protein-coding genes, which strongly supported monophyly of the genus,10,47-49 confirming earlier studies using protein-coding genes that had included fewer taxa.50-53 This question was subsequently addressed using whole-genome phylogenetic analyses including Trypanosoma brucei, Trypanosoma cruzi, Leishmania major, and two outgroup taxa, Euglena gracilis and Naegleria gruberi; almost all of the analyzed gene markers shared between the genomes of T. brucei, T. cruzi, and L. major supported the hypothesis that these trypanosomes form a monophyletic group.11 This analysis demonstrated the power of using whole genome sequences to resolve deep trypanosomatid relationships. Significantly, trypanosome monophyly indicates that trypanosome species might share some common, ancestral adaptations for survival in vertebrates. Understanding such ancestral adaptations could aid the rational design of therapeutics that target a broad range of pathogenic trypanosome species.
Recent phylogenetic studies suggest that trypanosomes and Leishmania evolved from different insect parasites, supporting the “invertebrate first” hypothesis.1,5,6 In support of this hypothesis, a newly described trypanosomatid genus, Paratrypanosoma, fell at the base of all trypanosomatids in a multigene phylogenetic analysis, suggesting that the first trypanosomatids were parasites of insects.36 Trypanosomes and all other trypanosomatids are sister groups in this tree, as is the case in most 18S rDNA trees (but differing from some gGAPDH gene trees), indicating that trypanosomes likely emerged relatively early in trypanosomatid evolution.10 Strong evidence that Leishmania acquired vertebrate parasitism independently from trypanosomes comes from the discovery of Leptomonas costaricensis, an insect-only trypanosomatid that is closely related to Leishmania,54 and studies that have resolved relationships between the genus and other insect trypanosomatids.32,36 Leishmania appears to have evolved considerably more recently than Trypanosoma, which may partially explain its comparatively narrow vertebrate (mammals, reptiles) and invertebrate (sandflies) host range. Thus, T. cruzi and other trypanosomes will not share common, ancestral adaptations to vertebrate parasitism with Leishmania spp.
The evolution of trypanosomes from a monogenetic insect parasite indicates that the first trypanosomes were insect-transmitted parasites of amphibious or terrestrial vertebrates. In this scenario, trypanosomes of fish that are transmitted by leeches must have evolved later. This hypothesis receives some support as, while the deepest split within genus Trypanosoma is between the Aquatic clade (that includes the fish trypanosomes) and the Terrestrial clade (Fig. 15.1A), both clades contain insect-transmitted parasites. The position of leech-transmitted trypanosomes of freshwater and marine fish in phylogenetic trees provides further support for this scenario7; they all fall in one of the two major subclades of the Aquatic clade,8 indicating that they were not the first to evolve, as had previously been hypothesized.55 Trypanosomes of marine fish form a monophyletic subclade within the fish clade, further indicating that these were not the first to evolve, as may have been expected if trypanosomes first evolved in early vertebrates (marine fish). It therefore appears that adaptation to transmission by aquatic leeches, perhaps by leeches feeding on infected amphibious vertebrates, enabled trypanosomes to colonize many aquatic vertebrates, including both freshwater and marine fish.
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