X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes

The sequence diversity of natural and laboratory populations of Brugia pahangi and Brugia malayi was assessed with Illumina resequencing followed by mapping in order to identify single nucleotide variants and insertions/deletions. In natural and laboratory Brugia populations, there is a lack of sequ...

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Autores principales: John Mattick, Silvia Libro, Robin Bromley, Wanpen Chaicumpa, Matthew Chung, Darren Cook, Mohammad Behram Khan, Nikhil Kumar, Yee-Ling Lau, Shailja Misra-Bhattacharya, Ramakrishna Rao, Lisa Sadzewicz, Atiporn Saeung, Mohd Shahab, Benjamin C. Sparklin, Andrew Steven, Joseph D. Turner, Luke J. Tallon, Mark J. Taylor, Andrew R. Moorhead, Michelle Michalski, Jeremy M. Foster, Julie C. Dunning Hotopp
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Publicado: Public Library of Science (PLoS) 2021
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spelling oai:doaj.org-article:5ef3bd723d724620a2d7851b385d70452021-11-18T09:11:35ZX-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes1935-27271935-2735https://doaj.org/article/5ef3bd723d724620a2d7851b385d70452021-10-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8575316/?tool=EBIhttps://doaj.org/toc/1935-2727https://doaj.org/toc/1935-2735The sequence diversity of natural and laboratory populations of Brugia pahangi and Brugia malayi was assessed with Illumina resequencing followed by mapping in order to identify single nucleotide variants and insertions/deletions. In natural and laboratory Brugia populations, there is a lack of sequence diversity on chromosome X relative to the autosomes (πX/πA = 0.2), which is lower than the expected (πX/πA = 0.75). A reduction in diversity is also observed in other filarial nematodes with neo-X chromosome fusions in the genera Onchocerca and Wuchereria, but not those without neo-X chromosome fusions in the genera Loa and Dirofilaria. In the species with neo-X chromosome fusions, chromosome X is abnormally large, containing a third of the genetic material such that a sizable portion of the genome is lacking sequence diversity. Such profound differences in genetic diversity can be consequential, having been associated with drug resistance and adaptability, with the potential to affect filarial eradication. Author summary Almost a billion people receive >7.7 billion doses of treatment aimed at eliminating lymphatic filariasis, which is caused by three filarial nematodes: Wuchereria bancrofti, Brugia malayi, and Brugia timori. Drug resistance and adaptation are both associated with pathogen success as well as higher levels of genetic diversity. In an examination of genetic diversity in Brugia malayi and Brugia pahangi, we observed a lack of genetic diversity over a third of the genome that is found on chromosome X. These species have neo-X chromosomes where a chromosome X fused with an autosome. Using publicly-available published data, the other filarial nematodes of greatest human significance are also found to have a similar lack of genetic diversity on their neo-X chromosomes. The two filarial nematodes with publicly-available data that lack neo-X chromosomes did not have this lack of genetic diversity. This lack of sequence diversity in B. malayi, W. bancrofti, and O. volvulus could have profound effects on all traits encoded on chromosome X.John MattickSilvia LibroRobin BromleyWanpen ChaicumpaMatthew ChungDarren CookMohammad Behram KhanNikhil KumarYee-Ling LauShailja Misra-BhattacharyaRamakrishna RaoLisa SadzewiczAtiporn SaeungMohd ShahabBenjamin C. SparklinAndrew StevenJoseph D. TurnerLuke J. TallonMark J. TaylorAndrew R. MoorheadMichelle MichalskiJeremy M. FosterJulie C. Dunning HotoppPublic Library of Science (PLoS)articleArctic medicine. Tropical medicineRC955-962Public aspects of medicineRA1-1270ENPLoS Neglected Tropical Diseases, Vol 15, Iss 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
spellingShingle Arctic medicine. Tropical medicine
RC955-962
Public aspects of medicine
RA1-1270
John Mattick
Silvia Libro
Robin Bromley
Wanpen Chaicumpa
Matthew Chung
Darren Cook
Mohammad Behram Khan
Nikhil Kumar
Yee-Ling Lau
Shailja Misra-Bhattacharya
Ramakrishna Rao
Lisa Sadzewicz
Atiporn Saeung
Mohd Shahab
Benjamin C. Sparklin
Andrew Steven
Joseph D. Turner
Luke J. Tallon
Mark J. Taylor
Andrew R. Moorhead
Michelle Michalski
Jeremy M. Foster
Julie C. Dunning Hotopp
X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes
description The sequence diversity of natural and laboratory populations of Brugia pahangi and Brugia malayi was assessed with Illumina resequencing followed by mapping in order to identify single nucleotide variants and insertions/deletions. In natural and laboratory Brugia populations, there is a lack of sequence diversity on chromosome X relative to the autosomes (πX/πA = 0.2), which is lower than the expected (πX/πA = 0.75). A reduction in diversity is also observed in other filarial nematodes with neo-X chromosome fusions in the genera Onchocerca and Wuchereria, but not those without neo-X chromosome fusions in the genera Loa and Dirofilaria. In the species with neo-X chromosome fusions, chromosome X is abnormally large, containing a third of the genetic material such that a sizable portion of the genome is lacking sequence diversity. Such profound differences in genetic diversity can be consequential, having been associated with drug resistance and adaptability, with the potential to affect filarial eradication. Author summary Almost a billion people receive >7.7 billion doses of treatment aimed at eliminating lymphatic filariasis, which is caused by three filarial nematodes: Wuchereria bancrofti, Brugia malayi, and Brugia timori. Drug resistance and adaptation are both associated with pathogen success as well as higher levels of genetic diversity. In an examination of genetic diversity in Brugia malayi and Brugia pahangi, we observed a lack of genetic diversity over a third of the genome that is found on chromosome X. These species have neo-X chromosomes where a chromosome X fused with an autosome. Using publicly-available published data, the other filarial nematodes of greatest human significance are also found to have a similar lack of genetic diversity on their neo-X chromosomes. The two filarial nematodes with publicly-available data that lack neo-X chromosomes did not have this lack of genetic diversity. This lack of sequence diversity in B. malayi, W. bancrofti, and O. volvulus could have profound effects on all traits encoded on chromosome X.
format article
author John Mattick
Silvia Libro
Robin Bromley
Wanpen Chaicumpa
Matthew Chung
Darren Cook
Mohammad Behram Khan
Nikhil Kumar
Yee-Ling Lau
Shailja Misra-Bhattacharya
Ramakrishna Rao
Lisa Sadzewicz
Atiporn Saeung
Mohd Shahab
Benjamin C. Sparklin
Andrew Steven
Joseph D. Turner
Luke J. Tallon
Mark J. Taylor
Andrew R. Moorhead
Michelle Michalski
Jeremy M. Foster
Julie C. Dunning Hotopp
author_facet John Mattick
Silvia Libro
Robin Bromley
Wanpen Chaicumpa
Matthew Chung
Darren Cook
Mohammad Behram Khan
Nikhil Kumar
Yee-Ling Lau
Shailja Misra-Bhattacharya
Ramakrishna Rao
Lisa Sadzewicz
Atiporn Saeung
Mohd Shahab
Benjamin C. Sparklin
Andrew Steven
Joseph D. Turner
Luke J. Tallon
Mark J. Taylor
Andrew R. Moorhead
Michelle Michalski
Jeremy M. Foster
Julie C. Dunning Hotopp
author_sort John Mattick
title X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes
title_short X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes
title_full X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes
title_fullStr X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes
title_full_unstemmed X-treme loss of sequence diversity linked to neo-X chromosomes in filarial nematodes
title_sort x-treme loss of sequence diversity linked to neo-x chromosomes in filarial nematodes
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/5ef3bd723d724620a2d7851b385d7045
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