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

Author:

Easton Alice12ORCID,Gao Shenghan34,Lawton Scott P5ORCID,Bennuru Sasisekhar1ORCID,Khan Asis6,Dahlstrom Eric7ORCID,Oliveira Rita G2,Kepha Stella8,Porcella Stephen F7,Webster Joanne29,Anderson Roy2,Grigg Michael E6,Davis Richard E3ORCID,Wang Jianbin310ORCID,Nutman Thomas B1ORCID

Affiliation:

1. Helminth Immunology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United States

2. Department of Infectious Disease Epidemiology, Imperial College London, London, United Kingdom

3. Department of Biochemistry and Molecular Genetics, RNA Bioscience Initiative, University of Colorado School of Medicine, Aurora, United States

4. Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China

5. Epidemiology Research Unit (ERU) Department of Veterinary and Animal Sciences, Northern Faculty, Scotland’s Rural College (SRUC), Inverness, United Kingdom

6. Molecular Parasitology Section, Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Disease, National Institutes of Health, Bethesda, United States

7. Genomics Unit, Research Technologies Branch, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, United States

8. London School of Tropical Medicine and Hygiene, London, United Kingdom

9. Royal Veterinary College, University of London, Department of Pathobiology and Population Sciences, Hertfordshire, United Kingdom

10. Department of Biochemistry and Cellular and Molecular Biology, University of Tennessee, Knoxville, United States

Abstract

Human ascariasis is a major neglected tropical disease caused by the nematodeAscaris lumbricoides. We report a 296 megabase (Mb) reference-quality genome comprised of 17,902 protein-coding genes derived from a single, representativeAscarisworm. 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 parasiteAscaris suumthan toA. 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 eitherA. suum-like orA. lumbricoides-like inheritance patterns supporting a highly interbredAscarisspecies 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.

Funder

National Institutes of Health

Bill and Melinda Gates Foundation

Wellcome Trust

London Centre for Neglected Tropical Disease Research

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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