Genetic characterization of nodular worm infections in Asian Apes

Abstract Parasitic nematodes of Oesophagostomum spp., commonly known, as 'nodular worms' are emerging as the most widely distributed and prevalent zoonotic nematodes. Oesophagostomum infections are well documented in African non-human primates; however, the taxonomy, distribution and trans...

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Main Authors: Erhan Yalcindag, Peter Stuart, Hideo Hasegawa, Adrian Streit, Jana Doležalová, Helen Morrogh-Bernard, Susan M. Cheyne, Wisnu Nurcahyo, Ivona Foitová
Format: Article
Language:English
Published: Nature Publishing Group 2021-03-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-86518-2
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spelling doaj-cf81327c70f847dc87b643297c7030ca2021-04-04T11:30:53ZengNature Publishing GroupScientific Reports2045-23222021-03-0111111110.1038/s41598-021-86518-2Genetic characterization of nodular worm infections in Asian ApesErhan Yalcindag0Peter Stuart1Hideo Hasegawa2Adrian Streit3Jana Doležalová4Helen Morrogh-Bernard5Susan M. Cheyne6Wisnu Nurcahyo7Ivona Foitová8Department of Botany and Zoology, Faculty of Science, Masaryk UniversityDepartment of Botany and Zoology, Faculty of Science, Masaryk UniversityDepartment of Biomedicine, Faculty of Medicine, Oita UniversityDepartment Evolutionary Biology, Max Planck Institute for Developmental BiologyDepartment of Physiology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, BrnoBorneo Nature FoundationDepartment of Humanities and Social Sciences, Oxford Brookes UniversityDepartment of Parasitology, Faculty of Veterinary Medicine, Gadjah Mada UniversityDepartment of Botany and Zoology, Faculty of Science, Masaryk UniversityAbstract Parasitic nematodes of Oesophagostomum spp., commonly known, as 'nodular worms' are emerging as the most widely distributed and prevalent zoonotic nematodes. Oesophagostomum infections are well documented in African non-human primates; however, the taxonomy, distribution and transmission of Oesophagostomum in Asian non-human primates are not adequately studied. To better understand which Oesophagostomum species infect Asian non-human primates and determine their phylogeny we analysed 55 faecal samples from 50 orangutan and 5 gibbon individuals from Borneo and Sumatra. Both microscopy and molecular results revealed that semi-wild animals had higher Oesophagostomum infection prevalence than free ranging animals. Based on sequence genotyping analysis targeting the Internal transcribed spacer 2 of rDNA, we report for the first time the presence of O. aculeatum in Sumatran apes. Population genetic analysis shows that there is significant genetic differentiation between Bornean and Sumatran O. aculeatum populations. Our results clearly reveal that O. aculeatum in free-ranging animals have a higher genetic variation than those in semi-wild animals, demonstrating that O. aculeatum is circulating naturally in wildlife and zoonotic transmission is possible. Further studies should be conducted to better understand the epidemiology and dynamics of Oesophagostomum transmission between humans, non-human primates and other wild species and livestock in Southeast Asia.https://doi.org/10.1038/s41598-021-86518-2
collection DOAJ
language English
format Article
sources DOAJ
author Erhan Yalcindag
Peter Stuart
Hideo Hasegawa
Adrian Streit
Jana Doležalová
Helen Morrogh-Bernard
Susan M. Cheyne
Wisnu Nurcahyo
Ivona Foitová
spellingShingle Erhan Yalcindag
Peter Stuart
Hideo Hasegawa
Adrian Streit
Jana Doležalová
Helen Morrogh-Bernard
Susan M. Cheyne
Wisnu Nurcahyo
Ivona Foitová
Genetic characterization of nodular worm infections in Asian Apes
Scientific Reports
author_facet Erhan Yalcindag
Peter Stuart
Hideo Hasegawa
Adrian Streit
Jana Doležalová
Helen Morrogh-Bernard
Susan M. Cheyne
Wisnu Nurcahyo
Ivona Foitová
author_sort Erhan Yalcindag
title Genetic characterization of nodular worm infections in Asian Apes
title_short Genetic characterization of nodular worm infections in Asian Apes
title_full Genetic characterization of nodular worm infections in Asian Apes
title_fullStr Genetic characterization of nodular worm infections in Asian Apes
title_full_unstemmed Genetic characterization of nodular worm infections in Asian Apes
title_sort genetic characterization of nodular worm infections in asian apes
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-03-01
description Abstract Parasitic nematodes of Oesophagostomum spp., commonly known, as 'nodular worms' are emerging as the most widely distributed and prevalent zoonotic nematodes. Oesophagostomum infections are well documented in African non-human primates; however, the taxonomy, distribution and transmission of Oesophagostomum in Asian non-human primates are not adequately studied. To better understand which Oesophagostomum species infect Asian non-human primates and determine their phylogeny we analysed 55 faecal samples from 50 orangutan and 5 gibbon individuals from Borneo and Sumatra. Both microscopy and molecular results revealed that semi-wild animals had higher Oesophagostomum infection prevalence than free ranging animals. Based on sequence genotyping analysis targeting the Internal transcribed spacer 2 of rDNA, we report for the first time the presence of O. aculeatum in Sumatran apes. Population genetic analysis shows that there is significant genetic differentiation between Bornean and Sumatran O. aculeatum populations. Our results clearly reveal that O. aculeatum in free-ranging animals have a higher genetic variation than those in semi-wild animals, demonstrating that O. aculeatum is circulating naturally in wildlife and zoonotic transmission is possible. Further studies should be conducted to better understand the epidemiology and dynamics of Oesophagostomum transmission between humans, non-human primates and other wild species and livestock in Southeast Asia.
url https://doi.org/10.1038/s41598-021-86518-2
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