Revisiting the Phylogenetic History of Helminths Through Genomics, the Case of the New Echinococcus oligarthrus Genome

Abstract

The first parasitic helminth genome sequence was published in 2007; since then, only ∼200 genomes have become available, most of them being draft assemblies. Nevertheless, despite the medical and economical global impact of helminthic infections, parasite genomes in public databases are underrepresented. Recently, through an integrative approach involving morphological, genetic, and ecological aspects, we have demonstrated that the complete life cycle of <i>Echinococcus oligarthrus</i> (Cestoda: Taeniidae) is present in South America. The neotropical <i>E. oligarthrus</i> parasite is capable of developing in any felid species and producing human infections. Neotropical echinococcosis is poorly understood yet and requires a complex medical examination to provide the appropriate intervention. Only a few cases of echinococcosis have been unequivocally identified and reported as a consequence of <i>E. oligarthrus</i> infections. Regarding phylogenetics, the analyses of mitogenomes and nuclear datasets have resulted in discordant topologies, and there is no unequivocal taxonomic classification of <i>Echinococcus</i> species so far. In this work, we sequenced and assembled the genome of <i>E. oligarthrus</i> that was isolated from agoutis (<i>Dasyprocta azarae</i>) naturally infected and performed the first comparative genomic study of a neotropical <i>Echinococcus</i> species. The <i>E. oligarthrus</i> genome assembly consisted of 86.22 Mb which showed ∼90% identity and 76.3% coverage with <i>Echinococcus multilocularis</i> and contained the 85.0% of the total expected genes. Genetic variants analysis of whole genome revealed a higher rate of intraspecific genetic variability (23,301 SNPs; 0.22 SNPs/kb) rather than for the genomes of <i>E. multilocularis</i> and <i>Echinococcus canadensis</i> G7 but lower with respect to <i>Echinococcus granulosus</i> G1. Comparative genomics against <i>E. multilocularis</i>, <i>E. granulosus</i> G1, and <i>E. canadensis</i> G7 revealed 38,762, 125,147, and 170,049 homozygous polymorphic sites, respectively, indicating a higher genetic distance between <i>E. oligarthrus</i> and <i>E. granulosus sensu lato</i> species. The SNP distribution in chromosomes revealed a higher SNP density in the longest chromosomes. Phylogenetic analysis using whole-genome SNPs demonstrated that <i>E. oligarthrus</i> is one of the basal species of the genus <i>Echinococcus</i> and is phylogenetically closer to <i>E. multilocularis</i>. This work sheds light on the <i>Echinococcus</i> phylogeny and settles the basis to study sylvatic <i>Echinococcus</i> species and their developmental evolutionary features.