title: Kinetoplastid Phylogenomics Reveals the Evolutionary Innovations Associated with the Origins of Parasitism.
abstract: The 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.
authors.affiliation: Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool Science Park Ic2, 146 Brownlow Hill, Liverpool L3 5RF, UK. Electronic address: a.p.jackson@liv.ac.uk.
authors.forename: Andrew P
authors.initials: AP
authors.lastname: Jackson
authors.affiliation: Pathogen Genomics Group, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Thomas D
authors.initials: TD
authors.lastname: Otto
authors.affiliation: Pathogen Genomics Group, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Martin
authors.initials: M
authors.lastname: Aslett
authors.affiliation: Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool Science Park Ic2, 146 Brownlow Hill, Liverpool L3 5RF, UK.
authors.forename: Stuart D
authors.initials: SD
authors.lastname: Armstrong
authors.affiliation: Centre de Résonance Magnétique des Systèmes Biologiques (RMSB), UMR 5536 CNRS, Zone Nord, Bâtiment 4A, Université Bordeaux Segalen, 146, Rue Léo Saignat, 33076 Bordeaux Cedex, France.
authors.forename: Frederic
authors.initials: F
authors.lastname: Bringaud
authors.affiliation: Department of Cell Biology, University of Alberta, Edmonton, AB T6G 2H7, Canada.
authors.forename: Alexander
authors.initials: A
authors.lastname: Schlacht
authors.affiliation: Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool Science Park Ic2, 146 Brownlow Hill, Liverpool L3 5RF, UK.
authors.forename: Catherine
authors.initials: C
authors.lastname: Hartley
authors.affiliation: Pathogen Genomics Group, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Mandy
authors.initials: M
authors.lastname: Sanders
authors.affiliation: Faculty of Natural Sciences, University of Keele, Keele ST5 5BG, UK; NIHR HPRU in Emerging and Zoonotic Infections, Institute of Infection and Global Health, University of Liverpool, 1-5 Brownlow Street, Liverpool L69 3GL, UK.
authors.forename: Jonathan M
authors.initials: JM
authors.lastname: Wastling
authors.affiliation: Department of Cell Biology, University of Alberta, Edmonton, AB T6G 2H7, Canada.
authors.forename: Joel B
authors.initials: JB
authors.lastname: Dacks
authors.affiliation: Department of Parasitology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool L3 5QA, UK.
authors.forename: Alvaro
authors.initials: A
authors.lastname: Acosta-Serrano
authors.affiliation: Division of Biological Chemistry and Drug Discovery, College of Life Sciences, University of Dundee, Dow Street, Dundee DD1 5EH, UK.
authors.forename: Mark C
authors.initials: MC
authors.lastname: Field
authors.affiliation: Division of Biomedical and Life Sciences, Lancaster University, Lancaster LA1 4YG, UK.
authors.forename: Michael L
authors.initials: ML
authors.lastname: Ginger
authors.affiliation: Pathogen Genomics Group, Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
authors.forename: Matthew
authors.initials: M
authors.lastname: Berriman
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D054627:Genome, Plastid; D018503:Genome, Protozoan; D006801:Humans; D010802:Phylogeny; D018087:Plastids / Q000378:metabolism*; D012987:Soil
chemical_list: D012987:Soil