Kinetoplastid Phylogenomics Reveals the Evolutionary Innovations Associated with the Origins of Parasitism

摘要

class="head no_bottom_margin" id="sec1title">IntroductionThe 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. Parasites affect the fitness of practically every other organism [], and they have influenced the form and function of all organisms from the earliest times [].Phylogenomics provides an opportunity to revisit the engrained view that parasitism is coupled with loss of biological complexity, specialization, and reduced evolutionary capacity []. Although celebrated cases such as obligate, intracellular pathogens like Mycoplasma [] and Microsporidia [] do have much reduced genomes and minimized physiology, most parasite genomes are, in fact, broadly comparable to those of non-parasitic model eukaryotes in size and content. Moreover, all parasite genomes show evidence for innovation and increases in functional complexity. Accurate analysis of the relative contributions of reduction and innovation to parasite evolution requires comparison of parasites not with model organisms, but with closely related non-parasites []. Yet, genomes for such free-living relatives are currently uncommon.Trypanosomatids are a major parasitic lineage with diverse hosts and include the human parasites Trypanosoma brucei, Trypanosoma cruzi, and Leishmania spp. Bodo saltans is a free-living Kinetoplastid and the closest known free-living relative of the trypanosomatid parasites []. Comparison of the T. brucei, T. cruzi, and L. major genome sequences [, , ] revealed their species-specific features, conspicuous against a background of widespread structural conservation [, ]. Many of their shared features could conceivably relate to a parasitic life strategy, such the absence of biosynthetic pathways for haem, purines, and aromatic amino acids. However, without a free-living outgroup for such comparisons, it has been impossible to define shared features that are parasite specific, and therefore plausibly adaptive, and to distinguish these from features shared by kinetoplastids generally.The absence of a free-living comparator has also impeded an explanation of species-specific features, most obviously the gene families that encode the enigmatic cell-surface proteins specific to each lineage [], such as the variant surface glycoprotein (VSG) in T. brucei, trans-sialidase (TS) and dispersed gene family 1 (DGF-1) in T. cruzi, and promastigote surface antigen (PSA) and δ-amastin in Leishmania spp. It is unknown whether free-living kinetoplastids possess homologs of these genes and, if so, how they were modified for their prominent role in parasites.Here we report the Bodo saltans genome sequence in comparison with trypanosomatids. 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. We show that although trypanosomatid genomes have become “streamlined,” gene families crucial for nutrient scavenging and host interactions have been elaborated, and we demonstrate that the enigmatic cell-surface gene families of different parasites originated through radical reorganization of common ancestral structures.