Genomics of an endemic cystic fibrosis Burkholderia multivorans strain reveals low within-patient evolution but high between-patient diversity

Cédric Lood, Charlotte Peeters, Quentin Lamy-Besnier, Jeroen Wagemans, Daniel De Vos, Marijke Proesmans, Jean-Paul Pirnay, Fedoua Echahidi, Denis Piérard, Matthieu Thimmesch, Anca Boeras, Katrien Lagrou, Evelien De Canck, Elke De Wachter, Vera van Noort, Rob Lavigne, Peter Vandamme

Research output: Contribution to journalArticle

Abstract

Burkholderia multivorans is a member of the Burkholderia cepacia complex (Bcc), notorious for its pathogenicity in persons with cystic fibrosis. Epidemiological surveillance suggests that patients predominantly acquire B. multivorans from environmental sources, with rare cases of patient-to-patient transmission. Here we report on the genomic analysis of thirteen isolates from an endemic B. multivorans strain infecting four cystic fibrosis patients treated in different pediatric cystic fibrosis centers in Belgium, with no evidence of cross-infection. All isolates share an identical sequence type (ST-742) but whole genome analysis shows that they exhibit peculiar patterns of genomic diversity between patients. By combining short and long reads sequencing technologies, we highlight key differences in terms of small nucleotide polymorphisms indicative of low rates of adaptive evolution within patient, and well-defined, hundred Kbps-long segments of high enrichment in mutations between patients. In addition, we observed large structural genomic variations amongst the isolates which revealed different plasmid contents, active roles for transposase IS3 and IS5 in the deactivation of genes, and mobile prophage elements. Our study shows limited within-patient B. multivorans evolution and high between-patient strain diversity, indicating that an environmental microdiverse reservoir must be present for this endemic strain, in which active diversification is taking place. Furthermore, our analysis also reveals a set of 30 parallel adaptations across multiple patients, indicating that the specific genomic background of a given strain may dictate the route of adaptation within the cystic fibrosis lung.

Original languageEnglish
Article numbere1009418
Number of pages23
JournalPLoS Pathogens
Volume17
Issue number3
Early online date2021
DOIs
Publication statusPublished - Mar 2021

Keywords

  • cystic fibrosis
  • Burkholderia multivorans
  • Burkholderia cepacia complex

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