Abstract
Many high-quality genomes are available for dixenous (two hosts) trypanosomatid species of the genera Trypanosoma, Leishmania, and Phytomonas, but only fragmentary information is available for monoxenous (single-host) trypanosomatids. In trypanosomatids, monoxeny is ancestral to dixeny, thus it is anticipated that the genome sequences of the key monoxenous parasites will be instrumental for both understanding the origin of parasitism and the evolution of dixeny. Here, we present a high-quality genome for Leptomonas pyrrhocoris, which is closely related to the dixenous genus Leishmania. The L. pyrrhocoris genome (30.4 Mbp in 60 scaffolds) encodes 10,148 genes. Using the L. pyrrhocoris genome, we pinpointed genes gained in Leishmania. Among those genes, 20 genes with unknown function had expression patterns in the Leishmania mexicana life cycle suggesting their involvement in virulence. By combining differential expression data for L. mexicana, L. major and Leptomonas seymouri, we have identified several additional proteins potentially involved in virulence, including SpoU methylase and U3 small nucleolar ribonucleoprotein IMP3. The population genetics of L. pyrrhocoris was also addressed by sequencing thirteen strains of different geographic origin, allowing the identification of 1,318 genes under positive selection. This set of genes was significantly enriched in components of the cytoskeleton and the flagellum.
Highlights
The trypanosomatids are a group of protists distinguished by a highly specialized mitochondrion and a prominent mitochondrial genome, the kinetoplast
We investigated gene family gains and losses in a phylogeny including dixenous species with published genomes and five monoxenous species (L. pyrrhocoris, L. seymouri, C. fasciculata, Blechomonas ayalai, Paratrypanosoma confusum), with a focus on genes gained in Leishmania and Leishmaniinae
Its current annotation contains 10,148 genes, of which 9,878 are protein-coding. This number falls within the range of previously annotated genomes of Leishmania and Trypanosoma (8,400 protein-coding genes for L. major Friedlin and 11,567 for T. brucei TREU927, TriTrypDB, release 25)[24] and is significantly higher than that of the streamlined genomes of two plant-infecting Phytomonas spp., with 6,381 and 6,451 protein-coding genes[39]
Summary
The trypanosomatids (family Trypanosomatidae, class Kinetoplastea) are a group of protists distinguished by a highly specialized mitochondrion and a prominent mitochondrial genome, the kinetoplast. It has been proposed recently that some monoxenous species are facultatively dixenous if conditions permit and favor such an alteration of their life cycle[9,10] One such requirement is the absence of an efficient immunological mechanism for clearing the parasite from the potential host. The model organism for the current study is Leptomonas pyrrhocoris (Zotta 1912) This species was isolated from the midgut of the firebug Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae), but the range of suitable hosts is known to embrace several species of the hemipterid family Pyrrhocoridae, including Pyrrhocoris apterus, P. marginatus and Scantius aegyptius in Europe and the Mediterranean, Dysdercus poecilius in China, and several Dysdercus spp. in the Neotropics and Africa. This is one a few truly globally distributed monoxenous trypanosomatids, the dissemination of which is facilitated by the omnipresence of its Pyrrhocoridae hosts in all regions studied far[2]
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