Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient

ABSTRACT Streptococcus pneumoniae isolates of serotype 23F with intermediate penicillin resistance were recovered on seven occasions over a period of 37 months from a cystic fibrosis patient in Berlin. All isolates expressed the same multilocus sequence type (ST), ST10523. The genome sequences of th...

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Autores principales:	Martin Rieger, Harald Mauch, Regine Hakenbeck
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	23F clone Streptococcus pneumoniae cystic fibrosis hyaluronidase penicillin-binding proteins persistence Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/27d34f637c114b318419dc1a241bdb12
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spelling	oai:doaj.org-article:27d34f637c114b318419dc1a241bdb122021-11-15T15:21:46ZLong Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient10.1128/mSphere.00201-172379-5042https://doaj.org/article/27d34f637c114b318419dc1a241bdb122017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00201-17https://doaj.org/toc/2379-5042ABSTRACT Streptococcus pneumoniae isolates of serotype 23F with intermediate penicillin resistance were recovered on seven occasions over a period of 37 months from a cystic fibrosis patient in Berlin. All isolates expressed the same multilocus sequence type (ST), ST10523. The genome sequences of the first and last isolates, D122 and D141, revealed the absence of two phage-related gene clusters compared to the genome of another ST10523 strain, D219, isolated earlier at a different place in Germany. Genomes of all three strains carried the same novel mosaic penicillin-binding protein (PBP) genes, pbp2x, pbp2b, and pbp1a; these genes were distinct from those of other penicillin-resistant S. pneumoniae strains except for pbp1a of a Romanian S. pneumoniae isolate. All PBPs contained mutations that have been associated with the penicillin resistance phenotype. Most interestingly, a mosaic block identical to an internal pbp2x sequence of ST10523 was present in pbp2x of Streptococcus mitis strain B93-4, which was isolated from the same patient. This suggests interspecies gene transfer from S. pneumoniae to S. mitis within the host. Nearly all genes expressing surface proteins, which represent major virulence factors of S. pneumoniae and are typical for this species, were present in the genome of ST10523. One exception was the hyaluronidase gene hlyA, which contained a 12-nucleotide deletion within the promoter region and an internal stop codon. The lack of a functional hyaluronidase might contribute to the ability to persist in the host for an unusually long period of time. IMPORTANCE Streptococcus pneumoniae is a common resident in the human nasopharynx. However, carriage can result in severe diseases due to a unique repertoire of pathogenicity factors that are rare in closely related commensal streptococci. We investigated a penicillin-resistant S. pneumoniae clone of serotype 23F isolated from a cystic fibrosis patient on multiple occasions over an unusually long period of over 3 years that was present without causing disease. Genome comparisons revealed an apparent nonfunctional pneumococcus-specific gene encoding a hyaluronidase, supporting the view that this enzyme adds to the virulence potential of the bacterium. The 23F clone harbored unique mosaic genes encoding penicillin resistance determinants, the product of horizontal gene transfer involving the commensal S. mitis as donor species. Sequences identical to one such mosaic gene were identified in an S. mitis strain from the same patient, suggesting that in this case S. pneumoniae played the role of donor.Martin RiegerHarald MauchRegine HakenbeckAmerican Society for Microbiologyarticle23F cloneStreptococcus pneumoniaecystic fibrosishyaluronidasepenicillin-binding proteinspersistenceMicrobiologyQR1-502ENmSphere, Vol 2, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	23F clone Streptococcus pneumoniae cystic fibrosis hyaluronidase penicillin-binding proteins persistence Microbiology QR1-502
spellingShingle	23F clone Streptococcus pneumoniae cystic fibrosis hyaluronidase penicillin-binding proteins persistence Microbiology QR1-502 Martin Rieger Harald Mauch Regine Hakenbeck Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient
description	ABSTRACT Streptococcus pneumoniae isolates of serotype 23F with intermediate penicillin resistance were recovered on seven occasions over a period of 37 months from a cystic fibrosis patient in Berlin. All isolates expressed the same multilocus sequence type (ST), ST10523. The genome sequences of the first and last isolates, D122 and D141, revealed the absence of two phage-related gene clusters compared to the genome of another ST10523 strain, D219, isolated earlier at a different place in Germany. Genomes of all three strains carried the same novel mosaic penicillin-binding protein (PBP) genes, pbp2x, pbp2b, and pbp1a; these genes were distinct from those of other penicillin-resistant S. pneumoniae strains except for pbp1a of a Romanian S. pneumoniae isolate. All PBPs contained mutations that have been associated with the penicillin resistance phenotype. Most interestingly, a mosaic block identical to an internal pbp2x sequence of ST10523 was present in pbp2x of Streptococcus mitis strain B93-4, which was isolated from the same patient. This suggests interspecies gene transfer from S. pneumoniae to S. mitis within the host. Nearly all genes expressing surface proteins, which represent major virulence factors of S. pneumoniae and are typical for this species, were present in the genome of ST10523. One exception was the hyaluronidase gene hlyA, which contained a 12-nucleotide deletion within the promoter region and an internal stop codon. The lack of a functional hyaluronidase might contribute to the ability to persist in the host for an unusually long period of time. IMPORTANCE Streptococcus pneumoniae is a common resident in the human nasopharynx. However, carriage can result in severe diseases due to a unique repertoire of pathogenicity factors that are rare in closely related commensal streptococci. We investigated a penicillin-resistant S. pneumoniae clone of serotype 23F isolated from a cystic fibrosis patient on multiple occasions over an unusually long period of over 3 years that was present without causing disease. Genome comparisons revealed an apparent nonfunctional pneumococcus-specific gene encoding a hyaluronidase, supporting the view that this enzyme adds to the virulence potential of the bacterium. The 23F clone harbored unique mosaic genes encoding penicillin resistance determinants, the product of horizontal gene transfer involving the commensal S. mitis as donor species. Sequences identical to one such mosaic gene were identified in an S. mitis strain from the same patient, suggesting that in this case S. pneumoniae played the role of donor.
format	article
author	Martin Rieger Harald Mauch Regine Hakenbeck
author_facet	Martin Rieger Harald Mauch Regine Hakenbeck
author_sort	Martin Rieger
title	Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient
title_short	Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient
title_full	Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient
title_fullStr	Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient
title_full_unstemmed	Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient
title_sort	long persistence of a <named-content content-type="genus-species">streptococcus pneumoniae</named-content> 23f clone in a cystic fibrosis patient
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/27d34f637c114b318419dc1a241bdb12
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Long Persistence of a <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> 23F Clone in a Cystic Fibrosis Patient

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