Abstract

BackgroundTrypanosomatid parasites such as Trypanosoma spp. and Leishmania spp. are a major source of infectious disease in humans and domestic animals worldwide. Fundamental to the host-parasite interactions of these potent pathogens are their cell surfaces, which are highly decorated with glycosylated proteins and other macromolecules. Trypanosomatid genomes contain large multi-copy gene families encoding UDP-dependent glycosyltransferases (UGTs), the primary role of which is cell-surface decoration. Here we report a phylogenetic analysis of UGTs from diverse trypanosomatid genomes, the aim of which was to understand the origin and evolution of their diversity.ResultsBy combining phylogenetics with analyses of recombination, and selection, we compared UGT repertoire, genomic context and sequence evolution across 19 trypanosomatids. We identified a UGT lineage present in stercorarian trypanosomes and a free-living kinetoplastid Bodo saltans that likely represents the ancestral state of this gene family. The phylogeny of parasite-specific genes shows that UGTs repertoire in Leishmaniinae and salivarian trypanosomes has expanded independently and with distinct evolutionary dynamics. In the former, the ancestral UGT repertoire was organised in a tandem array from which sporadic transpositions to telomeric regions occurred, allowing expansion most likely through telomeric exchange. In the latter, the ancestral UGT repertoire was comprised of seven subtelomeric lineages, two of which have greatly expanded potentially by gene transposition between these dynamic regions of the genome.ConclusionsThe phylogeny of UGTs confirms that they represent a substantial parasite-specific innovation, which has diversified independently in the distinct trypanosomatid lineages. Nonetheless, developmental regulation has been a strong driver of UGTs diversification in both African trypanosomes and Leishmania.

Highlights

  • Trypanosomatid parasites such as Trypanosoma spp. and Leishmania spp. are a major source of infectious disease in humans and domestic animals worldwide

  • We aim to identify monophyletic free-living (B. saltans) and parasitic UDP-dependent glycosyltransferases (UGTs) to understand more about their ancestral form and the origin of family expansion

  • Data collection and nomenclature Annotated UGT sequences were obtained from genome sequences of Trypanosoma cruzi CL Brenner Esmeraldo-like, T. rangeli SC58, T. grayi ANR4, T. brucei TREU927, T. congolense IL3000, T. vivax Y486, Leishmania major Friedlin, L. infantum JPCM5, L. mexicana MHOM/GT/2001/U1103, L. tarantolae Parrot-Tarll, L. enriettii LEM3045, L. braziliensis MHOM/BR/75/M2904, Leptomonas pyrrhocoris H10, and Crithidia fasciculata Cf-Cl hosted by TritrypDB v.28 [46]; Bodo saltans hosted by the GeneDB website [47]; and Angomonas deanei and Strigomonas culicis hosted by Ensembl Protists v

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Summary

Introduction

Trypanosomatid parasites such as Trypanosoma spp. and Leishmania spp. are a major source of infectious disease in humans and domestic animals worldwide. Trypanosomatids include Leishmania spp., which cause various kinds of leishmaniasis; stercorarian trypanosomes such as Trypanosoma cruzi, the cause of Chagas disease in central and south America; and salivarian trypanosomes such as Trypanosoma brucei, the cause of African trypanosomiasis in humans and animals, (as well as T. vivax and T. congolense that cause disease exclusively in animals). These vector-borne diseases have a significant impact on human and animal health, and are a profound constraint on the socio-economic development of low and middle-income countries.

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