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Genomic diversity in Onchocerca volvulus and its Wolbachia endosymbiont

Nature Microbiology volume 2, Article number: 16207 (2017) Cite this article

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Abstract

Ongoing elimination efforts have altered the global distribution of Onchocerca volvulus, the agent of river blindness, and further population restructuring is expected as efforts continue. Therefore, a better understanding of population genetic processes and their effect on biogeography is needed to support elimination goals. We describe O. volvulus genome variation in 27 isolates from the early 1990s (before widespread mass treatment) from four distinct locales: Ecuador, Uganda, the West African forest and the West African savanna. We observed genetic substructuring between Ecuador and West Africa and between the West African forest and savanna bioclimes, with evidence of unidirectional gene flow from savanna to forest strains. We identified forest:savanna-discriminatory genomic regions and report a set of ancestry informative loci that can be used to differentiate between forest, savanna and admixed isolates, which has not previously been possible. We observed mito-nuclear discordance possibly stemming from incomplete lineage sorting. The catalogue of the nuclear, mitochondrial and endosymbiont DNA variants generated in this study will support future basic and translational onchocerciasis research, with particular relevance for ongoing control programmes, and boost efforts to characterize drug, vaccine and diagnostic targets.

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Figure 1: Geographical and genomic relationship between O. volvulus isolates.
Figure 2: Sequence variation in the nuclear genome of O. volvulus.
Figure 3: Ancestry-informative markers (AIMs) that exhibit substantially different allele frequencies between the West African forest and savanna populations were used to assign individual isolates to source populations and identify genetic admixture.
Figure 4: Haplotype characterization and relative abundance of Wolbachia and mitochondria in O. volvulus.

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  • 14 July 2017

    In the PDF version of this article previously published, the year of publication provided in the footer of each page and in the 'How to cite' section was erroneously given as 2017, it should have been 2016. This error has now been corrected. The HTML version of the article was not affected.

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Acknowledgements

The sequencing work was funded by NIH–NHGRI (U54HG003079) and the genetic variation analysis was funded by NIH–NIAID (R01AI081803) and the Bill & Melinda Gates Foundation (OPP GH 1083853). The study was also funded, in part, by the Division of Intramural Research, National Institute of Allergy and Infectious Diseases. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The findings and conclusions contained within are those of the authors and do not necessarily reflect positions or policies of the Bill & Melinda Gates Foundation. The authors thank the faculty and staff of the McDonnell Genome Institute who contributed to this study, and thank the physicians and fieldworkers in the endemic countries for their extensive help in collecting the parasite material. The unpublished RNAseq data used in this study were produced by the parasite genomics group at the Wellcome Trust Sanger Institute in collaboration with the laboratories of T. B. Nutman and S. Lustigman.

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  1. Young-Jun Choi and Rahul Tyagi: These authors contributed equally to this work.

Authors and Affiliations

  1. McDonnell Genome Institute, Washington University in St Louis, St Louis, 63108, Missouri, USA

    Young-Jun Choi, Rahul Tyagi, Samantha N. McNulty, Bruce A. Rosa, Philip Ozersky, John Martin, Kymberlie Hallsworth-Pepin & Makedonka Mitreva

  2. Department of Global Health, Global Health Infectious Disease Research Program, University of South Florida, Tampa, 33612, Florida, USA

    Thomas R. Unnasch

  3. Laboratory of Parasitic Diseases, National Institute of Allergy and Infectious Diseases, Bethesda, 20892, Maryland, USA

    Carmelle T. Norice & Thomas B. Nutman

  4. Division of Infectious Diseases, Department of Medicine Washington University School of Medicine, Washington University School of Medicine, St Louis, 63110, Missouri, USA

    Gary J. Weil, Peter U. Fischer & Makedonka Mitreva

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Contributions

Y.-J.C. and R.T. contributed equally to this work. M.M., P.U.F. and G.J.W. conceived and planned the project. M.M. led the project, and carried out analysis and manuscript preparation. T.R.U., C.T.N., T.B.N. and P.U.F. provided material. K.H.-P., P.O. and J.M. carried out sequence data production, annotation and submission. Y.C., R.T., B.A.R. and S.M.N.M performed genome-based variant studies. M.M., R.T., Y.C., S.N.M. and B.A.R. drafted, edited and wrote the manuscript.

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Correspondence to Makedonka Mitreva.

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Supplementary information

Supplementary Information

Legends for Supplementary Tables 1-9, Supplementary Figures 1-10 (PDF 1252 kb)

Supplementary Table 1

Classifications, sources and read mapping data for each of the samples utilized (XLSX 48 kb)

Supplementary Table 2

SnpEff annotations and allele frequency data per SNP position (XLSX 11775 kb)

Supplementary Table 3

Summary of results from the FST sliding window analysis (XLSX 34 kb)

Supplementary Table 4

FST genome scan sliding window positions, summary statistics, and overlapping genes (XLSX 5074 kb)

Supplementary Table 5

Detailed functional annotation and SNP annotation per gene (XLSX 4685 kb)

Supplementary Table 6

ABBA-BABA analysis results for gene flow (XLSX 76 kb)

Supplementary Table 7

Ancestry Informative Markers for distinguishing savanna from forest O. volvulus isolates (XLSX 47 kb)

Supplementary Table 8

Variants ranked by FST (FOR:SAV comparison, minimum value 0.5) (XLSX 944 kb)

Supplementary Table 9

Sources, dates, and processing procedures for each of the whole genome shotgun libraries in each of the samples (XLSX 51 kb)

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Choi, YJ., Tyagi, R., McNulty, S. et al. Genomic diversity in Onchocerca volvulus and its Wolbachia endosymbiont. Nat Microbiol 2, 16207 (2017). https://doi.org/10.1038/nmicrobiol.2016.207

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