Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans

Human ascariasis is a major neglected tropical disease caused by the nematode Ascaris lumbricoides. We report a 296 megabase (Mb) reference-quality genome comprised of 17,902 protein-coding genes derived from a single, representative Ascaris worm. An additional 68 worms were collected from 60 human...

Full description

Bibliographic Details
Main Authors: Alice Easton, Shenghan Gao, Scott P Lawton, Sasisekhar Bennuru, Asis Khan, Eric Dahlstrom, Rita G Oliveira, Stella Kepha, Stephen F Porcella, Joanne Webster, Roy Anderson, Michael E Grigg, Richard E Davis, Jianbin Wang, Thomas B Nutman
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/61562
id doaj-9b8812e5f2d5494187a78b77e4e2b000
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Alice Easton
Shenghan Gao
Scott P Lawton
Sasisekhar Bennuru
Asis Khan
Eric Dahlstrom
Rita G Oliveira
Stella Kepha
Stephen F Porcella
Joanne Webster
Roy Anderson
Michael E Grigg
Richard E Davis
Jianbin Wang
Thomas B Nutman
spellingShingle Alice Easton
Shenghan Gao
Scott P Lawton
Sasisekhar Bennuru
Asis Khan
Eric Dahlstrom
Rita G Oliveira
Stella Kepha
Stephen F Porcella
Joanne Webster
Roy Anderson
Michael E Grigg
Richard E Davis
Jianbin Wang
Thomas B Nutman
Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
eLife
Ascaris lumbricoides
Ascaris suum
reference genome
Phylogenetics
species complex
zoonoses
author_facet Alice Easton
Shenghan Gao
Scott P Lawton
Sasisekhar Bennuru
Asis Khan
Eric Dahlstrom
Rita G Oliveira
Stella Kepha
Stephen F Porcella
Joanne Webster
Roy Anderson
Michael E Grigg
Richard E Davis
Jianbin Wang
Thomas B Nutman
author_sort Alice Easton
title Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
title_short Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
title_full Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
title_fullStr Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
title_full_unstemmed Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
title_sort molecular evidence of hybridization between pig and human ascaris indicates an interbred species complex infecting humans
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2020-11-01
description Human ascariasis is a major neglected tropical disease caused by the nematode Ascaris lumbricoides. We report a 296 megabase (Mb) reference-quality genome comprised of 17,902 protein-coding genes derived from a single, representative Ascaris worm. An additional 68 worms were collected from 60 human hosts in Kenyan villages where pig husbandry is rare. Notably, the majority of these worms (63/68) possessed mitochondrial genomes that clustered closer to the pig parasite Ascaris suum than to A. lumbricoides. Comparative phylogenomic analyses identified over 11 million nuclear-encoded SNPs but just two distinct genetic types that had recombined across the genomes analyzed. The nuclear genomes had extensive heterozygosity, and all samples existed as genetic mosaics with either A. suum-like or A. lumbricoides-like inheritance patterns supporting a highly interbred Ascaris species genetic complex. As no barriers appear to exist for anthroponotic transmission of these ‘hybrid’ worms, a one-health approach to control the spread of human ascariasis will be necessary.
topic Ascaris lumbricoides
Ascaris suum
reference genome
Phylogenetics
species complex
zoonoses
url https://elifesciences.org/articles/61562
work_keys_str_mv AT aliceeaston molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT shenghangao molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT scottplawton molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT sasisekharbennuru molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT asiskhan molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT ericdahlstrom molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT ritagoliveira molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT stellakepha molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT stephenfporcella molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT joannewebster molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT royanderson molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT michaelegrigg molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT richardedavis molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT jianbinwang molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
AT thomasbnutman molecularevidenceofhybridizationbetweenpigandhumanascarisindicatesaninterbredspeciescomplexinfectinghumans
_version_ 1721457896533786624
spelling doaj-9b8812e5f2d5494187a78b77e4e2b0002021-05-05T21:41:24ZengeLife Sciences Publications LtdeLife2050-084X2020-11-01910.7554/eLife.61562Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humansAlice Easton0https://orcid.org/0000-0002-4476-9415Shenghan Gao1Scott P Lawton2https://orcid.org/0000-0003-4055-6524Sasisekhar Bennuru3https://orcid.org/0000-0002-6117-742XAsis Khan4Eric Dahlstrom5https://orcid.org/0000-0002-9333-3060Rita G Oliveira6Stella Kepha7Stephen F Porcella8Joanne Webster9Roy Anderson10Michael E Grigg11Richard E Davis12https://orcid.org/0000-0003-2242-3234Jianbin Wang13https://orcid.org/0000-0003-3155-894XThomas B Nutman14https://orcid.org/0000-0001-6887-4941Helminth Immunology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United States; Department of Infectious Disease Epidemiology, Imperial College London, London, United KingdomDepartment of Biochemistry and Molecular Genetics, RNA Bioscience Initiative, University of Colorado School of Medicine, Aurora, United States; Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, ChinaEpidemiology Research Unit (ERU) Department of Veterinary and Animal Sciences, Northern Faculty, Scotland’s Rural College (SRUC), Inverness, United KingdomHelminth Immunology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United StatesMolecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United StatesGenomics Unit, Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, United StatesDepartment of Infectious Disease Epidemiology, Imperial College London, London, United KingdomLondon School of Tropical Medicine and Hygiene, London, United KingdomGenomics Unit, Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, United StatesDepartment of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom; Royal Veterinary College, University of London, Department of Pathobiology and Population Sciences, Hertfordshire, United KingdomDepartment of Infectious Disease Epidemiology, Imperial College London, London, United KingdomMolecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United StatesDepartment of Biochemistry and Molecular Genetics, RNA Bioscience Initiative, University of Colorado School of Medicine, Aurora, United StatesDepartment of Biochemistry and Molecular Genetics, RNA Bioscience Initiative, University of Colorado School of Medicine, Aurora, United States; Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, United StatesHelminth Immunology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United StatesHuman ascariasis is a major neglected tropical disease caused by the nematode Ascaris lumbricoides. We report a 296 megabase (Mb) reference-quality genome comprised of 17,902 protein-coding genes derived from a single, representative Ascaris worm. An additional 68 worms were collected from 60 human hosts in Kenyan villages where pig husbandry is rare. Notably, the majority of these worms (63/68) possessed mitochondrial genomes that clustered closer to the pig parasite Ascaris suum than to A. lumbricoides. Comparative phylogenomic analyses identified over 11 million nuclear-encoded SNPs but just two distinct genetic types that had recombined across the genomes analyzed. The nuclear genomes had extensive heterozygosity, and all samples existed as genetic mosaics with either A. suum-like or A. lumbricoides-like inheritance patterns supporting a highly interbred Ascaris species genetic complex. As no barriers appear to exist for anthroponotic transmission of these ‘hybrid’ worms, a one-health approach to control the spread of human ascariasis will be necessary.https://elifesciences.org/articles/61562Ascaris lumbricoidesAscaris suumreference genomePhylogeneticsspecies complexzoonoses