Multiple major disease-associated clones of Legionella pneumophila have emerged recently and independently

  1. Carmen Buchrieser3,4
  1. 1Wellcome Trust Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA Cambridge, United Kingdom;
  2. 2Public Health England, NW9 5HT London, United Kingdom;
  3. 3Institut Pasteur, Biologie des Bactéries Intracellulaires, 75015, Paris, France;
  4. 4CNRS UMR 3525, 75724, Paris, France;
  5. 5Hub de Bio-informatique et Biostatistiques, Centre de Bio-informatique, Biostatistique et Biologie Intégrative (C3BI), Institut Pasteur, 75724, Paris, France;
  6. 6National Reference Centre for Legionella, Hospice Civil de Lyon, International Center for Infection Research, Legionella pathogenesis Team, 69364, Lyon, France;
  7. 7Institut Pasteur, Evolution et Ecologie de la Resistance aux Antibiotiques, 75724, Paris, France;
  8. 8Institut Pasteur, Plate-Forme Génomique, 75724, Paris, France
  1. Corresponding authors: cbuch{at}pasteur.fr, parkhill{at}sanger.ac.uk
  1. 9 These authors are joint first authors and contributed equally to this work.

Abstract

Legionella pneumophila is an environmental bacterium and the leading cause of Legionnaires’ disease. Just five sequence types (ST), from more than 2000 currently described, cause nearly half of disease cases in northwest Europe. Here, we report the sequence and analyses of 364 L. pneumophila genomes, including 337 from the five disease-associated STs and 27 representative of the species diversity. Phylogenetic analyses revealed that the five STs have independent origins within a highly diverse species. The number of de novo mutations is extremely low with maximum pairwise single-nucleotide polymorphisms (SNPs) ranging from 19 (ST47) to 127 (ST1), which suggests emergences within the last century. Isolates sampled geographically far apart differ by only a few SNPs, demonstrating rapid dissemination. These five STs have been recombining recently, leading to a shared pool of allelic variants potentially contributing to their increased disease propensity. The oldest clone, ST1, has spread globally; between 1940 and 2000, four new clones have emerged in Europe, which show long-distance, rapid dispersal. That a large proportion of clinical cases is caused by recently emerged and internationally dispersed clones, linked by convergent evolution, is surprising for an environmental bacterium traditionally considered to be an opportunistic pathogen. To simultaneously explain recent emergence, rapid spread and increased disease association, we hypothesize that these STs have adapted to new man-made environmental niches, which may be linked by human infection and transmission.

Footnotes

  • [Supplemental material is available for this article.]

  • Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.209536.116.

  • Freely available online through the Genome Research Open Access option.

  • Received May 8, 2016.
  • Accepted September 16, 2016.

This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.

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