Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages.

Genome Biol Evol. 2014 Dec 4. pii: evu263. [Epub ahead of print]

Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages.

Hilty M1, Wüthrich D2, Salter SJ3, Engel H4, Campbell S4, Sá-Leão R5, de Lencastre H6, Hermans P7, Sadowy E8, Turner P9, Chewapreecha C10, Diggle M11, Pluschke G12, McGee L13, Eser OK14, Low DE15, Smith-Vaughan H16, Endimiani A4, Küffer M4, Dupasquier M17, Beaudoing E17, Weber J17, Bruggmann R2, Hanage WP18, Parkhill J3, Hathaway LJ4, Mühlemann K19, Bentley SD20.

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Abstract

The surrounding capsule of Streptococcus pneumoniae has been identified as a major virulence factor and is targeted by pneumococcal conjugate vaccines (PCV). However, nonencapsulated Streptococcus pneumoniae (Non-Ec-Sp) have also been isolated globally, mainly in carriage studies. It is unknown if Non-Ec-Sp evolve sporadically, if they have high antibiotic non-susceptiblity rates and a unique, specific gene content. Here, whole genome sequencing of 131 Non-Ec-Sp isolates sourced from 17 different locations around the world was performed. Results revealed a deep-branching classic lineage that is distinct from multiple sporadic lineages. The sporadic lineages clustered with a previously sequenced, global collection of encapsulated S. pneumoniae (Ec-Sp) isolates while the classic lineage is comprised mainly of the frequently identified multi-locus sequences types ST344 (n=39) and ST448 (n=40). All ST344 and nine ST448 isolates had high non-susceptiblity rates to β-lactams and other antimicrobials. Analysis of the accessory genome reveals that the classic Non-Ec-Sp contained an increased number of mobile elements, than Ec-Sp and sporadic Non-Ec-Sp. Performing adherence assays to human epithelial cells for selected classic and sporadic Non-Ec-Sp revealed that the presence of a integrative conjugative element (ICE) results in increased adherence to human epithelial cells (P=0.005). In contrast, sporadic Non-Ec-Sp lacking the ICE had greater growth in vitro possibly resulting in improved fitness. In conclusion, Non-Ec-Sp isolates from the classic lineage have evolved separately. They have spread globally, are well adapted to nasopharyngeal carriage and are able to coexist with Ec-Sp. Due to continued use of pneumococcal conjugate vaccines, Non-Ec-Sp may become more prevalent.

© The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

KEYWORDS:

Pneumococcal isolates; antibiotic non-susceptibility; comparative genomics; integrative conjugative elements (ICEs); whole genome sequencing

PMID: 25480686 [PubMed - as supplied by publisher]