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Genome Biol Evol. 2014 Dec 4;6(12):3281-94. doi: 10.1093/gbe/evu263.

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

Author information

1
Institute for Infectious Diseases, University of Bern, Switzerland Department of Infectious Diseases, Inselspital, Bern University Hospital and University of Bern, Switzerland markus.hilty@ifik.unibe.ch.
2
Interfaculty Bioinformatics Unit, University of Bern, Switzerland Swiss Institute of Bioinformatics, Lausanne, Switzerland.
3
Wellcome Trust Sanger Institute, Hinxton, United Kingdom.
4
Institute for Infectious Diseases, University of Bern, Switzerland.
5
Instituto de Tecnologia Química e Biológica, University of Lisbon, Portugal.
6
Instituto de Tecnologia Química e Biológica, University of Lisbon, Portugal Laboratory of Microbiology and Infectious Diseases, The Rockefeller University.
7
Laboratory of Pediatric Infectious Diseases, Radboud University Medical Centre, Nijmegen, The Netherlands.
8
National Medicines Institute, Warsaw, Poland.
9
Shoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand Centre for Tropical Medicine, Nuffield Department of Medicine, University of Oxford, United Kingdom.
10
Wellcome Trust Sanger Institute, Hinxton, United Kingdom Shoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand.
11
Clinical Microbiology Department, Queens Medical Centre, Nottingham, United Kingdom.
12
Swiss Tropical and Public Health Institute, University of Basel, Switzerland.
13
Respiratory Diseases Branch, Centers for Disease Control and Prevention, Georgia, Atlanta.
14
Department of Microbiology, Medical Faculty, Hacettepe University, Ankara, Turkey.
15
Mt Sinai Hospital & Public Health Laboratories, Toronto, Ontario, Canada.
16
Menzies School of Health Research, Charles Darwin University, Australia.
17
Centre for Integrative Genomics, University of Lausanne, Switzerland.
18
Department of Epidemiology, Center for Communicable Disease Dynamics, Harvard School of Public Health.
19
Institute for Infectious Diseases, University of Bern, Switzerland Department of Infectious Diseases, Inselspital, Bern University Hospital and University of Bern, Switzerland.
20
Wellcome Trust Sanger Institute, Hinxton, United Kingdom Department of Medicine, Addenbrookes Hospital, University of Cambridge, United Kingdom.

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.

KEYWORDS:

antibiotic nonsusceptibility; comparative genomics; integrative conjugative elements; pneumococcal isolates; whole-genome sequencing

PMID:
25480686
PMCID:
PMC4986459
DOI:
10.1093/gbe/evu263
[Indexed for MEDLINE]
Free PMC Article

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