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The impact of antimicrobials on gonococcal evolution

Nature Microbiology volume 4, pages 1941–1950 (2019)Cite this article

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Abstract

The sexually transmitted pathogen Neisseria gonorrhoeae is regarded as being on the way to becoming an untreatable superbug. Despite its clinical importance, little is known about its emergence and evolution, and how this corresponds with the introduction of antimicrobials. We present a genome-based phylogeographical analysis of 419 gonococcal isolates from across the globe. Results indicate that modern gonococci originated in Europe or Africa, possibly as late as the sixteenth century and subsequently disseminated globally. We provide evidence that the modern gonococcal population has been shaped by antimicrobial treatment of sexually transmitted infections as well as other infections, leading to the emergence of two major lineages with different evolutionary strategies. The well-described multidrug-resistant lineage is associated with high rates of homologous recombination and infection in high-risk sexual networks. A second, multisusceptible lineage is more associated with heterosexual networks, with potential implications for infection control.

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Fig. 1: Geographical and phylogenetic distribution of N. gonorrhoeae isolates.
Fig. 2: Global phylogeographical analysis.
Fig. 3: Evolution of AMR genetic determinants in N. gonorrhoeae.
Fig. 4: Characterization of the lineages of N. gonorrhoeae.

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Data availability

All genomic data have been deposited in the European Nucleotide Archive (ENA) under project number PRJEB4024. Accession numbers for the particular strains are indicated in Supplementary Table 1. All other data supporting the findings of this study are available within the paper and its Supplementary Information files.

Code availability

The custom Perl script to convert xmfa to fasta files (xmfa2fas.pl) is available from https://gist.github.com/leosanbu/.

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Acknowledgements

We thank H. To and O. Gascuel for their help with the LSD software, and the Pathogen Informatics group at the Wellcome Sanger Institute for informatics support. We also thank S. Szreter, T. Bayliss-Smith and P. Mitchell from the University of Cambridge, Cambridge, UK, for interesting discussions on the historical evidence of gonorrhoea infection. The Japanese isolates were kindly provided by Y. Watanabe and T. Kuroki, Department of Microbiology, Kanagawa Prefectural Institute of Public Health, Kanagawa, Japan. This work was funded by the Wellcome grant number 098051 and the Foundation for Medical Research at Örebro University Hospital, Örebro, Sweden. J.C. was funded by the ERC grant number 745258. Y.H.G. is supported by The Smith Family Foundation and the NIH/NIAID grant 1R01AI132606-01.

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Authors and Affiliations

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

    Leonor Sánchez-Busó, Jukka Corander, Julian Parkhill, Stephen D. Bentley & Simon R. Harris

  2. WHO Collaborating Centre for Gonorrhoea and other Sexually Transmitted Infections, National Reference Laboratory for Sexually Transmitted Infections, Department of Laboratory Medicine, Clinical Microbiology, Faculty of Medicine and Health, Örebro University, Örebro, Sweden

    Daniel Golparian & Magnus Unemo

  3. Helsinki Institute for Information Technology, Department of Mathematics and Statistics, University of Helsinki, Helsinki, Finland

    Jukka Corander

  4. Department of Biostatistics, University of Oslo, Oslo, Norway

    Jukka Corander

  5. Department of Immunology and Infectious Diseases, Harvard TH Chan School of Public Health, Boston, MA, USA

    Yonatan H. Grad

  6. Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA, USA

    Yonatan H. Grad

  7. Department of Bacteriology I, National Institute of Infectious Diseases, Tokyo, Japan

    Makoto Ohnishi

  8. Antimicrobial Resistance Research Center, National Institute of Infectious Diseases, Tokyo, Japan

    Makoto Ohnishi

  9. Faculty of Classics, University of Cambridge, Cambridge, UK

    Rebecca Flemming

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  1. Leonor Sánchez-Busó
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Contributions

S.R.H., M.U., S.D.B. and J.P. conceived and managed the study. L.S.B. and S.R.H. analysed the data and drafted the manuscript. D.G., M.U. and M.O. cultured isolates and extracted DNA. L.S.B., S.R.H., M.U. and Y.H.G. interpreted the data. J.C. provided statistical analysis. R.F. advised on historical interpretation. All authors contributed to the writing of the manuscript.

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Correspondence to Simon R. Harris.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–10, Supplementary Tables 2 and 3, Supplementary Tables 5–7 and Supplementary Notes.

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Supplementary Table 1

Additional strain information.

Supplementary Table 4

Prior and posterior continent assignments.

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Sánchez-Busó, L., Golparian, D., Corander, J. et al. The impact of antimicrobials on gonococcal evolution. Nat Microbiol 4, 1941–1950 (2019). https://doi.org/10.1038/s41564-019-0501-y

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