Abstract
SummaryThe evolution of parasitism is a recurrent event in the history of life and a core problem in evolutionary biology. Trypanosomatids are important parasites and include the human pathogens Trypanosoma brucei, Trypanosoma cruzi, and Leishmania spp., which in humans cause African trypanosomiasis, Chagas disease, and leishmaniasis, respectively. Genome comparison between trypanosomatids reveals that these parasites have evolved specialized cell-surface protein families, overlaid on a well-conserved cell template. Understanding how these features evolved and which ones are specifically associated with parasitism requires comparison with related non-parasites. We have produced genome sequences for Bodo saltans, the closest known non-parasitic relative of trypanosomatids, and a second bodonid, Trypanoplasma borreli. Here we show how genomic reduction and innovation contributed to the character of trypanosomatid genomes. We show that gene loss has “streamlined” trypanosomatid genomes, particularly with respect to macromolecular degradation and ion transport, but consistent with a widespread loss of functional redundancy, while adaptive radiations of gene families involved in membrane function provide the principal innovations in trypanosomatid evolution. Gene gain and loss continued during trypanosomatid diversification, resulting in the asymmetric assortment of ancestral characters such as peptidases between Trypanosoma and Leishmania, genomic differences that were subsequently amplified by lineage-specific innovations after divergence. Finally, we show how species-specific, cell-surface gene families (DGF-1 and PSA) with no apparent structural similarity are independent derivations of a common ancestral form, which we call “bodonin.” This new evidence defines the parasitic innovations of trypanosomatid genomes, revealing how a free-living phagotroph became adapted to exploiting hostile host environments.
Highlights
The history of life is punctuated by the transition from free-living to parasitic organisms, a process often accompanied by profound phenotypic transformation
We aim to identify the principal genomic changes associated with the ancestral trypanosomatid and so uncover the relative contributions of genomic reduction and innovation to the origin of parasitism
The genome sequences of B. saltans and model trypanosomatids are compared in Table 1; based on CEGMA score [13], the B. saltans sequence displays a comparable degree of completeness to the reference genomes
Summary
The history of life is punctuated by the transition from free-living to parasitic organisms, a process often accompanied by profound phenotypic transformation. Parasites are a substantial component of biodiversity, and their origins coincide with major eukaryotic lineages such as Trypanosomatidae, Apicomplexa, Microsporidia, and Neodermata. Phylogenomics provides an opportunity to revisit the engrained view that parasitism is coupled with loss of biological complexity, specialization, and reduced evolutionary capacity [3]. Celebrated cases such as obligate, intracellular pathogens like Mycoplasma [4] and Microsporidia [5] do have much reduced genomes and minimized physiology, most parasite genomes are, broadly comparable to those of nonparasitic model eukaryotes in size and content. All parasite genomes show evidence for innovation and increases in functional complexity.
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