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...

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Published in:eLife Vol. 9
Main Authors: Easton, Alice, Gao, Shenghan, Lawton, Scott P, Bennuru, Sasisekhar, Khan, Asis, Dahlstrom, Eric, Oliveira, Rita G, Kepha, Stella, Porcella, Stephen F, Webster, Joanne, Anderson, Roy, Grigg, Michael E, Davis, Richard E, Wang, Jianbin, Nutman, Thomas B
Format: Journal Article
Language:English
Published: England eLife Science Publications, Ltd 06.11.2020
eLife Sciences Publications, Ltd
eLife Sciences Publications Ltd
Subjects:
Analysis
Animals
Ascariasis - parasitology
Ascariasis - veterinary
Ascaris lumbricoides
Ascaris lumbricoides - genetics
Ascaris lumbricoides - pathogenicity
Ascaris suum
Ascaris suum - genetics
Ascaris suum - pathogenicity
Cyclooxygenase 1 - genetics
Epidemiology and Global Health
Female
Genes
Genetics and Genomics
Genome, Helminth - genetics
Genome, Mitochondrial - genetics
Genomes
Genomics
Heterozygote
Humans
Hybridization, Genetic - genetics
Kenya
Male
Phylogenetics
Phylogeny
Polymorphism, Single Nucleotide - genetics
Proteome - genetics
reference genome
Roundworms
species complex
Swine
Swine Diseases - parasitology
zoonoses
Kenya
global health
Ascaris lumbricoides
epidemiology
genetics
species complex
Ascaris suum
Phylogenetics
genomics
reference genome
zoonoses
human
ISSN:2050-084X, 2050-084X
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Abstract 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.
AbstractList 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.
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.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.
Human ascariasis is a major neglected tropical disease caused by the nematode . We report a 296 megabase (Mb) reference-quality genome comprised of 17,902 protein-coding genes derived from a single, representative 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 than to . 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 -like or -like inheritance patterns supporting a highly interbred 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.
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.
Audience Academic
Author Oliveira, Rita G
Nutman, Thomas B
Bennuru, Sasisekhar
Gao, Shenghan
Wang, Jianbin
Khan, Asis
Porcella, Stephen F
Dahlstrom, Eric
Anderson, Roy
Easton, Alice
Lawton, Scott P
Webster, Joanne
Kepha, Stella
Davis, Richard E
Grigg, Michael E
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  organization: Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom
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  surname: Webster
  fullname: Webster, Joanne
  organization: Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom, Royal Veterinary College, University of London, Department of Pathobiology and Population Sciences, Hertfordshire, United Kingdom
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  organization: Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom
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  organization: Molecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United States
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  orcidid: 0000-0003-2242-3234
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  orcidid: 0000-0003-3155-894X
  surname: Wang
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  organization: Department 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 States
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  surname: Nutman
  fullname: Nutman, Thomas B
  organization: Helminth Immunology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United States
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Keywords global health
Ascaris lumbricoides
epidemiology
genetics
species complex
Ascaris suum
Phylogenetics
genomics
reference genome
zoonoses
human
Language English
License This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
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content type line 23
These authors contributed equally to this work.
Institute of Microbiology, Chinese Academy of Sciences, Beijing, China.
ORCID 0000-0002-9333-3060
0000-0002-4476-9415
0000-0001-6887-4941
0000-0003-4055-6524
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PublicationDate 2020-11-06
PublicationDateYYYYMMDD 2020-11-06
PublicationDate_xml – month: 11
  year: 2020
  text: 2020-11-06
  day: 06
PublicationDecade 2020
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PublicationTitle eLife
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Publisher eLife Science Publications, Ltd
eLife Sciences Publications, Ltd
eLife Sciences Publications Ltd
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– name: eLife Sciences Publications, Ltd
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Snippet Human ascariasis is a major neglected tropical disease caused by the nematode Ascaris lumbricoides . We report a 296 megabase (Mb) reference-quality genome...
Human ascariasis is a major neglected tropical disease caused by the nematode . We report a 296 megabase (Mb) reference-quality genome comprised of 17,902...
Human ascariasis is a major neglected tropical disease caused by the nematode Ascaris lumbricoides. We report a 296 megabase (Mb) reference-quality genome...
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SubjectTerms Analysis
Animals
Ascariasis - parasitology
Ascariasis - veterinary
Ascaris lumbricoides
Ascaris lumbricoides - genetics
Ascaris lumbricoides - pathogenicity
Ascaris suum
Ascaris suum - genetics
Ascaris suum - pathogenicity
Cyclooxygenase 1 - genetics
Epidemiology and Global Health
Female
Genes
Genetics and Genomics
Genome, Helminth - genetics
Genome, Mitochondrial - genetics
Genomes
Genomics
Heterozygote
Humans
Hybridization, Genetic - genetics
Kenya
Male
Phylogenetics
Phylogeny
Polymorphism, Single Nucleotide - genetics
Proteome - genetics
reference genome
Roundworms
species complex
Swine
Swine Diseases - parasitology
zoonoses
Title Molecular evidence of hybridization between pig and human Ascaris indicates an interbred species complex infecting humans
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https://pubmed.ncbi.nlm.nih.gov/PMC7647404
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Volume 9
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