Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>

ABSTRACT Streptococcus pseudopneumoniae is a close relative of the major human pathogen S. pneumoniae. It is increasingly associated with lower-respiratory-tract infections (LRTI) and a high prevalence of antimicrobial resistance (AMR). S. pseudopneumoniae is difficult to identify using traditional...

Full description

Bibliographic Details
Main Authors: Geneviève Garriss, Priyanka Nannapaneni, Alexandra S. Simões, Sarah Browall, Karthik Subramanian, Raquel Sá-Leão, Herman Goossens, Herminia de Lencastre, Birgitta Henriques-Normark
Format: Article
Language:English
Published: American Society for Microbiology 2019-06-01
Series:mBio
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/mBio.01286-19
_version_ 1819004401203806208
author Geneviève Garriss
Priyanka Nannapaneni
Alexandra S. Simões
Sarah Browall
Karthik Subramanian
Raquel Sá-Leão
Herman Goossens
Herminia de Lencastre
Birgitta Henriques-Normark
author_facet Geneviève Garriss
Priyanka Nannapaneni
Alexandra S. Simões
Sarah Browall
Karthik Subramanian
Raquel Sá-Leão
Herman Goossens
Herminia de Lencastre
Birgitta Henriques-Normark
author_sort Geneviève Garriss
collection DOAJ
description ABSTRACT Streptococcus pseudopneumoniae is a close relative of the major human pathogen S. pneumoniae. It is increasingly associated with lower-respiratory-tract infections (LRTI) and a high prevalence of antimicrobial resistance (AMR). S. pseudopneumoniae is difficult to identify using traditional typing methods due to similarities with S. pneumoniae and other members of the mitis group (SMG). Using whole-genome sequencing of LRTI isolates and a comparative genomic approach, we found that a large number of pneumococcal virulence and colonization genes are present in the core S. pseudopneumoniae genome. We also reveal an impressive number of novel surface-exposed proteins encoded by the genome of this species. In addition, we propose a new and entirely specific molecular marker useful for the identification of S. pseudopneumoniae. Phylogenetic analyses of S. pseudopneumoniae show that specific clades are associated with allelic variants of core proteins. Resistance to tetracycline and macrolides, the two most common types of resistance, were found to be encoded by Tn916-like integrating conjugative elements and Mega-2. Overall, we found a tight association of genotypic determinants of AMR and phenotypic AMR with a specific lineage of S. pseudopneumoniae. Taken together, our results shed light on the distribution in S. pseudopneumoniae of genes known to be important during invasive disease and colonization and provide insight into features that could contribute to virulence, colonization, and adaptation. IMPORTANCE S. pseudopneumoniae is an overlooked pathogen emerging as the causative agent of lower-respiratory-tract infections and associated with chronic obstructive pulmonary disease (COPD) and exacerbation of COPD. However, much remains unknown on its clinical importance and epidemiology, mainly due to the lack of specific markers to distinguish it from S. pneumoniae. Here, we provide a new molecular marker entirely specific for S. pseudopneumoniae and offer a comprehensive view of the virulence and colonization genes found in this species. Finally, our results pave the way for further studies aiming at understanding the pathogenesis and epidemiology of S. pseudopneumoniae.
first_indexed 2024-12-20T23:36:18Z
format Article
id doaj.art-0bc1f1ef40f84d038a186ac45502dafb
institution Directory Open Access Journal
issn 2150-7511
language English
last_indexed 2024-12-20T23:36:18Z
publishDate 2019-06-01
publisher American Society for Microbiology
record_format Article
series mBio
spelling doaj.art-0bc1f1ef40f84d038a186ac45502dafb2022-12-21T19:23:11ZengAmerican Society for MicrobiologymBio2150-75112019-06-0110310.1128/mBio.01286-19Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>Geneviève Garriss0Priyanka Nannapaneni1Alexandra S. Simões2Sarah Browall3Karthik Subramanian4Raquel Sá-Leão5Herman Goossens6Herminia de Lencastre7Birgitta Henriques-Normark8Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, SwedenDepartment of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, SwedenLaboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica Antonio Xavier, Universidade Nova de Lisboa, Oeiras, PortugalDepartment of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, SwedenDepartment of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, SwedenLaboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica Antonio Xavier, Universidade Nova de Lisboa, Oeiras, PortugalLaboratory of Medical Microbiology, Vaccine &amp; Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, BelgiumLaboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica Antonio Xavier, Universidade Nova de Lisboa, Oeiras, PortugalDepartment of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, SwedenABSTRACT Streptococcus pseudopneumoniae is a close relative of the major human pathogen S. pneumoniae. It is increasingly associated with lower-respiratory-tract infections (LRTI) and a high prevalence of antimicrobial resistance (AMR). S. pseudopneumoniae is difficult to identify using traditional typing methods due to similarities with S. pneumoniae and other members of the mitis group (SMG). Using whole-genome sequencing of LRTI isolates and a comparative genomic approach, we found that a large number of pneumococcal virulence and colonization genes are present in the core S. pseudopneumoniae genome. We also reveal an impressive number of novel surface-exposed proteins encoded by the genome of this species. In addition, we propose a new and entirely specific molecular marker useful for the identification of S. pseudopneumoniae. Phylogenetic analyses of S. pseudopneumoniae show that specific clades are associated with allelic variants of core proteins. Resistance to tetracycline and macrolides, the two most common types of resistance, were found to be encoded by Tn916-like integrating conjugative elements and Mega-2. Overall, we found a tight association of genotypic determinants of AMR and phenotypic AMR with a specific lineage of S. pseudopneumoniae. Taken together, our results shed light on the distribution in S. pseudopneumoniae of genes known to be important during invasive disease and colonization and provide insight into features that could contribute to virulence, colonization, and adaptation. IMPORTANCE S. pseudopneumoniae is an overlooked pathogen emerging as the causative agent of lower-respiratory-tract infections and associated with chronic obstructive pulmonary disease (COPD) and exacerbation of COPD. However, much remains unknown on its clinical importance and epidemiology, mainly due to the lack of specific markers to distinguish it from S. pneumoniae. Here, we provide a new molecular marker entirely specific for S. pseudopneumoniae and offer a comprehensive view of the virulence and colonization genes found in this species. Finally, our results pave the way for further studies aiming at understanding the pathogenesis and epidemiology of S. pseudopneumoniae.https://journals.asm.org/doi/10.1128/mBio.01286-19infectious diseaseStreptococcus pseudopneumoniaeStreptococcus pneumoniaebacterial diagnosticscomparative genomics
spellingShingle Geneviève Garriss
Priyanka Nannapaneni
Alexandra S. Simões
Sarah Browall
Karthik Subramanian
Raquel Sá-Leão
Herman Goossens
Herminia de Lencastre
Birgitta Henriques-Normark
Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>
mBio
infectious disease
Streptococcus pseudopneumoniae
Streptococcus pneumoniae
bacterial diagnostics
comparative genomics
title Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>
title_full Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>
title_fullStr Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>
title_full_unstemmed Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>
title_short Genomic Characterization of the Emerging Pathogen <named-content content-type="genus-species">Streptococcus pseudopneumoniae</named-content>
title_sort genomic characterization of the emerging pathogen named content content type genus species streptococcus pseudopneumoniae named content
topic infectious disease
Streptococcus pseudopneumoniae
Streptococcus pneumoniae
bacterial diagnostics
comparative genomics
url https://journals.asm.org/doi/10.1128/mBio.01286-19
work_keys_str_mv AT genevievegarriss genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT priyankanannapaneni genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT alexandrassimoes genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT sarahbrowall genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT karthiksubramanian genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT raquelsaleao genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT hermangoossens genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT herminiadelencastre genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent
AT birgittahenriquesnormark genomiccharacterizationoftheemergingpathogennamedcontentcontenttypegenusspeciesstreptococcuspseudopneumoniaenamedcontent