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Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing

Nature Genetics volume 44, pages 413–419 (2012)Cite this article

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Abstract

Chlamydia trachomatis is responsible for both trachoma and sexually transmitted infections, causing substantial morbidity and economic cost globally. Despite this, our knowledge of its population and evolutionary genetics is limited. Here we present a detailed phylogeny based on whole-genome sequencing of representative strains of C. trachomatis from both trachoma and lymphogranuloma venereum (LGV) biovars from temporally and geographically diverse sources. Our analysis shows that predicting phylogenetic structure using ompA, which is traditionally used to classify Chlamydia, is misleading because extensive recombination in this region masks any true relationships present. We show that in many instances, ompA is a chimera that can be exchanged in part or as a whole both within and between biovars. We also provide evidence for exchange of, and recombination within, the cryptic plasmid, which is another key diagnostic target. We used our phylogenetic framework to show how genetic exchange has manifested itself in ocular, urogenital and LGV C. trachomatis strains, including the epidemic LGV serotype L2b.

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Figure 1: Maximum likelihood reconstruction of the phylogeny of C. trachomatis with recombinations removed.
Figure 2: Reconstruction of recombination events on the species phylogeny of C. trachomatis.
Figure 3: Distribution of SNPs in ompA of C. trachomatis.

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Acknowledgements

We thank the core informatics, library-making and sequencing teams at the Wellcome Trust Sanger Institute. S.R.H. is grateful for the opportunity to discuss this project at the Permafrost conference. This work was funded by the Wellcome Trust grant numbers 098051 and 080348. B.G.S. was funded by the Wellcome Trust.

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Authors and Affiliations

  1. Pathogen Genomics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK

    Simon R Harris, Helena M B Seth-Smith, Julian Parkhill & Nicholas R Thomson

  2. Molecular Microbiology Group, University Medical School, Southampton General Hospital, Southampton, UK

    Ian N Clarke, Lesley T Cutcliffe & Rachel J Skilton

  3. Department of Clinical Research, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK

    Anthony W Solomon, Martin J Holland, David Mabey, Rosanna W Peeling & David A Lewis

  4. Health Protection Agency, Public Health Laboratory Southampton, Southampton General Hospital, Southampton, UK

    Peter Marsh

  5. Sexually Transmitted Infections Reference Centre, National Institute for Communicable Diseases, National Health Laboratory Service, Johannesburg, South Africa

    David A Lewis

  6. Department of Internal Medicine, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa

    David A Lewis

  7. Department of Infectious Disease Epidemiology, Imperial College, St. Mary's Hospital Campus, London, UK

    Brian G Spratt

  8. Department of Laboratory Medicine and Clinical Microbiology, National Reference Laboratory for Pathogenic Neisseria, Örebro University Hospital, Örebro, Sweden

    Magnus Unemo

  9. Department of Laboratory Medicine, Clinical Microbiology, Malmö University Hospital, Malmö, Sweden

    Kenneth Persson

  10. Department of Obstetrics and Gynecology, Institute of Clinical Sciences, Malmö University Hospital, Malmö, Sweden

    Carina Bjartling

  11. British Columbia Centre for Disease Control, Vancouver, British Columbia, Canada

    Robert Brunham

  12. Department of Dermatology, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands

    Henry J C de Vries

  13. Sexually Transmitted Infections Outpatient Clinic, Infectious Diseases Cluster, Public Health Service Amsterdam, Amsterdam, The Netherlands

    Henry J C de Vries

  14. Centre for Infection and Immunity Amsterdam, Academic Medical Centre, University of Amsterdam, Amsterdam, The Netherlands

    Henry J C de Vries

  15. Department of Medical Microbiology of Infection Prevention, Laboratory of Immunogenetics, VU University Medical Center, Amsterdam, The Netherlands

    Servaas A Morré

  16. Department of Genetics and Cell Biology, Institute of Public Health Genomics, School for Public Health and Primary Care and School for Oncology & Developmental Biology, Faculty of Health, Medicine & Life Sciences, University of Maastricht, Maastricht, The Netherlands

    Servaas A Morré

  17. Geneeskundige en Gezondheidsdienst Amsterdam (GGD; Health Service Amsterdam), Amsterdam, The Netherlands

    Arjen Speksnijder

  18. Université de Bordeaux, Unité Sous Contrat (USC) Mycoplasmal and Chlamydial Infections in Humans, French National Reference Center for Chlamydial Infections, Bordeaux, France

    Cécile M Bébéar, Maïté Clerc & Bertille de Barbeyrac

  19. Institut National de la Recherche Agronomique, USC Mycoplasmal and Chlamydial Infections in Humans, French National Reference Center for Chlamydial Infections, Bordeaux, France

    Cécile M Bébéar, Maïté Clerc & Bertille de Barbeyrac

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Contributions

S.R.H. assembled, aligned and analyzed the data and wrote the paper. I.N.C. jointly conceived of the project with N.R.T. and provided samples. H.M.B.S.-S. performed experiments, carried out analyses of the data and helped write the paper. L.T.C., P.M., R.J.S., M.J.H., D.M., R.W.P., D.A.L., M.U., K.P., C.B., R.B., H.J.C.d.V., S.A.M., A.W.S., C.M.B., A.S., M.C. and B.d.B. collected and cultured samples. B.G.S. and J.P. helped interpret the data and write the paper. N.R.T. conceived of and ran the project and wrote the paper.

Corresponding author

Correspondence to Simon R Harris.

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The authors declare no competing financial interests.

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Harris, S., Clarke, I., Seth-Smith, H. et al. Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat Genet 44, 413–419 (2012). https://doi.org/10.1038/ng.2214

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