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

Markus Hilty, Daniel Wüthrich, Susannah J. Salter, Hansjürg Engel, Samuel Campbell, Raquel Sá-Leão, Hermínia De Lencastre, Peter Hermans, Ewa Sadowy, Paul Turner, Claire Chewapreecha, Mathew Diggle, Gerd Pluschke, Lesley McGee, Özgen Köseoʇlu Eser, Donald E. Low, Heidi Smith-Vaughan, Andrea Endimiani, Marianne Kü Ffer, Mélanie DupasquierEmmanuel Beaudoing, Johann Weber, Rémy Bruggmann, William P. Hanage, Julian Parkhill, Lucy J. Hathaway, Kathrin Mü Hlemann, Stephen D. Bentley

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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 S. 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 nonsusceptiblity 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 multilocus sequences types (STs) ST344 (n = 39) and ST448 (n = 40). All ST344 and nine ST448 isolates had high nonsusceptiblity 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 PCV, non-Ec-Sp may become more prevalent.

Original languageEnglish
Pages (from-to)3281-3294
Number of pages14
JournalGenome Biology and Evolution
Volume6
Issue number12
DOIs
Publication statusPublished - 2014

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    Hilty, M., Wüthrich, D., Salter, S. J., Engel, H., Campbell, S., Sá-Leão, R., De Lencastre, H., Hermans, P., Sadowy, E., Turner, P., Chewapreecha, C., Diggle, M., Pluschke, G., McGee, L., Eser, Ö. K., Low, D. E., Smith-Vaughan, H., Endimiani, A., Ffer, M. K., ... Bentley, S. D. (2014). Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages. Genome Biology and Evolution, 6(12), 3281-3294. https://doi.org/10.1093/gbe/evu263