Extensive hybridization between pig and humanAscarisidentifies a highly interbred species complex infecting humans

Abstract

48Human ascariasis is a major neglected tropical disease caused by the nematode Ascaris 49 lumbricoides. We report a 296 megabase (Mb) reference quality genome comprised of 17902 50 protein-coding genes derived from a single, representative Ascaris worm collected from 60 human 51 hosts in Kenyan villages where pig husbandry is rare. Notably, the majority of human isolates 52 (63/68) possessed mitochondrial genomes that clustered closer to the pig parasite Ascaris suum 53 than to A. lumbricoides. Comparative phylogenomic analyses identified over 11 million nuclear-54 encoded SNPs but just two distinct genetic types that had recombined across the genomes analysed. 55The nuclear genomes had extensive heterozygosity and all samples existed as genetic mosaics with 56 either A. suum-like or A. lumbricoides-like inheritance patterns supporting a highly interbred 57Ascaris species genetic complex. As no barriers appear to exist for anthroponotic transmission of 58 these "hybrid" worms, a one-health approach to control the spread of human ascariasis will be 59 necessary. 60 61 the genetic differences between Ascaris worms collected from human populations in different parts 87 5 of the world 11,21 are the result of geographic reproductive isolation. Previous studies using Ascaris 88 mitochondrial genomes or genes suggest there are A. lumbricoides-type (human-associated) and A. 89 suum-type (pig-associated) clades 8,22,23 . Other work suggests multiple clades of worms, only one of 90 which is unique to pigs 24 . 91In the current study, we constructed a reference-quality Ascaris genome (ALV5) based on 92 sequences from a single female worm collected from a single person in Kenya. This person was 93 presumed to be infected with A. lumbricoides as there is a lack of local pig husbandry. Draft A. 94 suum genomes have previously been constructed from worms obtained from pigs in Australia 25 95 and in the United States 26,27 . The Ascaris genome ALV5 was found to be highly similar (99% 96 identity) to the A. suum genome from worms collected from pigs in the United States 28 . Our 97 mitochondrial and whole-genome analyses from an additional 68 individual worms indicate that A. 98 suum and A. lumbricoides form a genetic complex that is capable of interbreeding. Our data support 99 a model for a recent worldwide, multi-species Ascaris population expansion caused by the 100 movement of humans and/or livestock globally. Ascaris isolates from both pigs and humans may be 101 important in human disease, necessitating a one-health approach to control the spread of human 102 ascariasis. 103 104 Results: 105

Comprehensive Chromosome End Remodeling during Programmed DNA Elimination

“…Although this genome assembly is not gap free, we have essentially anchored all sequences into the 24 chromosomes, identified the locations for the 34 large 120 bp repeat clusters, and characterized the organization of the 120 bp repeats as well as the subtelomeric repeats. This complete genome assembly provides a significant new resource for an important parasite infecting upward of 800 million people [29,30] and enables a chromosomal view of programmed DNA elimination.…”

Detangling the Crosstalk Between Ascaris, Trichuris and Gut Microbiota: What´s Next?

“…Factors such as the highly resistant nature of the eggs in moist soil, long standing patency, high rate of reinfections despite effective anti-helminth therapy and the unavailability of vaccines, have all been associated with a high dispersal of Ascaris and Trichuris , not only in human hosts but also in other vertebrate hosts ( Schüle et al., 2014 ; Easton et al., 2019 ; Cools et al., 2021 ). In addition to the human parasite A. lumbricoides , ascariasis infection of swine by the highly prevalent species Ascaris suum is also known for its pathogenic effects in domestic pigs and its impact in livestock productivity ( Dold and Holland, 2011 ; Velasco et al., 2011 ; Cooper and Figuieredo, 2013 ; Miller et al., 2015 ; Katakam et al., 2016 ; Williams et al., 2017 ; Midha et al., 2018 ; Hansen et al., 2019 ; Arora et al., 2020 ; Easton et al., 2020 ).…”