Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes

Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S....
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Gespeichert in:

Autor*in:	Hannah N. Agnew [verfasserIn] Erin B. Brazel [verfasserIn] Alexandra Tikhomirova [verfasserIn] Mark van der Linden [verfasserIn] Kimberley T. McLean [verfasserIn] James C. Paton [verfasserIn] Claudia Trappetti [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2022

Schlagwörter:	Streptococcus pneumoniae virulence raffinose clinical isolates carbohydrate metabolism meningitis

Übergeordnetes Werk:	In: Frontiers in Cellular and Infection Microbiology - Frontiers Media S.A., 2016, 12(2022)
Übergeordnetes Werk:	volume:12 ; year:2022

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.3389/fcimb.2022.866259

Katalog-ID:	DOAJ046719849

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520			\|a Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis.
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allfields	10.3389/fcimb.2022.866259 doi (DE-627)DOAJ046719849 (DE-599)DOAJ4cc47e2da4fb452bbcb8af1819fdaad2 DE-627 ger DE-627 rakwb eng QR1-502 Hannah N. Agnew verfasserin aut Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis. Streptococcus pneumoniae virulence raffinose clinical isolates carbohydrate metabolism meningitis Microbiology Erin B. Brazel verfasserin aut Alexandra Tikhomirova verfasserin aut Mark van der Linden verfasserin aut Kimberley T. McLean verfasserin aut James C. Paton verfasserin aut Claudia Trappetti verfasserin aut In Frontiers in Cellular and Infection Microbiology Frontiers Media S.A., 2016 12(2022) (DE-627)664968554 (DE-600)2619676-1 22352988 nnns volume:12 year:2022 https://doi.org/10.3389/fcimb.2022.866259 kostenfrei https://doaj.org/article/4cc47e2da4fb452bbcb8af1819fdaad2 kostenfrei https://www.frontiersin.org/articles/10.3389/fcimb.2022.866259/full kostenfrei https://doaj.org/toc/2235-2988 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_60 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_206 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 12 2022
spelling	10.3389/fcimb.2022.866259 doi (DE-627)DOAJ046719849 (DE-599)DOAJ4cc47e2da4fb452bbcb8af1819fdaad2 DE-627 ger DE-627 rakwb eng QR1-502 Hannah N. Agnew verfasserin aut Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis. Streptococcus pneumoniae virulence raffinose clinical isolates carbohydrate metabolism meningitis Microbiology Erin B. Brazel verfasserin aut Alexandra Tikhomirova verfasserin aut Mark van der Linden verfasserin aut Kimberley T. McLean verfasserin aut James C. Paton verfasserin aut Claudia Trappetti verfasserin aut In Frontiers in Cellular and Infection Microbiology Frontiers Media S.A., 2016 12(2022) (DE-627)664968554 (DE-600)2619676-1 22352988 nnns volume:12 year:2022 https://doi.org/10.3389/fcimb.2022.866259 kostenfrei https://doaj.org/article/4cc47e2da4fb452bbcb8af1819fdaad2 kostenfrei https://www.frontiersin.org/articles/10.3389/fcimb.2022.866259/full kostenfrei https://doaj.org/toc/2235-2988 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_60 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_206 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 12 2022
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allfieldsGer	10.3389/fcimb.2022.866259 doi (DE-627)DOAJ046719849 (DE-599)DOAJ4cc47e2da4fb452bbcb8af1819fdaad2 DE-627 ger DE-627 rakwb eng QR1-502 Hannah N. Agnew verfasserin aut Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis. Streptococcus pneumoniae virulence raffinose clinical isolates carbohydrate metabolism meningitis Microbiology Erin B. Brazel verfasserin aut Alexandra Tikhomirova verfasserin aut Mark van der Linden verfasserin aut Kimberley T. McLean verfasserin aut James C. Paton verfasserin aut Claudia Trappetti verfasserin aut In Frontiers in Cellular and Infection Microbiology Frontiers Media S.A., 2016 12(2022) (DE-627)664968554 (DE-600)2619676-1 22352988 nnns volume:12 year:2022 https://doi.org/10.3389/fcimb.2022.866259 kostenfrei https://doaj.org/article/4cc47e2da4fb452bbcb8af1819fdaad2 kostenfrei https://www.frontiersin.org/articles/10.3389/fcimb.2022.866259/full kostenfrei https://doaj.org/toc/2235-2988 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_60 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_206 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 12 2022
allfieldsSound	10.3389/fcimb.2022.866259 doi (DE-627)DOAJ046719849 (DE-599)DOAJ4cc47e2da4fb452bbcb8af1819fdaad2 DE-627 ger DE-627 rakwb eng QR1-502 Hannah N. Agnew verfasserin aut Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes 2022 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis. Streptococcus pneumoniae virulence raffinose clinical isolates carbohydrate metabolism meningitis Microbiology Erin B. Brazel verfasserin aut Alexandra Tikhomirova verfasserin aut Mark van der Linden verfasserin aut Kimberley T. McLean verfasserin aut James C. Paton verfasserin aut Claudia Trappetti verfasserin aut In Frontiers in Cellular and Infection Microbiology Frontiers Media S.A., 2016 12(2022) (DE-627)664968554 (DE-600)2619676-1 22352988 nnns volume:12 year:2022 https://doi.org/10.3389/fcimb.2022.866259 kostenfrei https://doaj.org/article/4cc47e2da4fb452bbcb8af1819fdaad2 kostenfrei https://www.frontiersin.org/articles/10.3389/fcimb.2022.866259/full kostenfrei https://doaj.org/toc/2235-2988 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_11 GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_60 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_206 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2003 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 12 2022
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callnumber-first	Q - Science
author	Hannah N. Agnew
spellingShingle	Hannah N. Agnew misc QR1-502 misc Streptococcus pneumoniae misc virulence misc raffinose misc clinical isolates misc carbohydrate metabolism misc meningitis misc Microbiology Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes
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topic_title	QR1-502 Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes Streptococcus pneumoniae virulence raffinose clinical isolates carbohydrate metabolism meningitis
topic	misc QR1-502 misc Streptococcus pneumoniae misc virulence misc raffinose misc clinical isolates misc carbohydrate metabolism misc meningitis misc Microbiology
topic_unstemmed	misc QR1-502 misc Streptococcus pneumoniae misc virulence misc raffinose misc clinical isolates misc carbohydrate metabolism misc meningitis misc Microbiology
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title	Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes
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title_full	Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes
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title_sort	streptococcus pneumoniae strains isolated from a single pediatric patient display distinct phenotypes
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title_auth	Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes
abstract	Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis.
abstractGer	Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis.
abstract_unstemmed	Streptococcus pneumoniae is the leading cause of bacterial paediatric meningitis after the neonatal period worldwide, but the bacterial factors and pathophysiology that drive pneumococcal meningitis are not fully understood. In this work, we have identified differences in raffinose utilization by S. pneumoniae isolates of identical serotype and sequence type from the blood and cerebrospinal fluid (CSF) of a single pediatric patient with meningitis. The blood isolate displayed defective raffinose metabolism, reduced transcription of the raffinose utilization pathway genes, and an inability to grow in vitro when raffinose was the sole carbon source. The fitness of these strains was then assessed using a murine intranasal infection model. Compared with the CSF isolate, mice infected with the blood isolate displayed higher bacterial numbers in the nose, but this strain was unable to invade the ears of infected mice. A premature stop codon was identified in the aga gene in the raffinose locus, suggesting that this protein likely displays impaired alpha-galactosidase activity. These closely related strains were assessed by Illumina sequencing, which did not identify any single nucleotide polymorphisms (SNPs) between the two strains. However, these wider genomic analyses identified the presence of an alternative alpha-galactosidase gene that appeared to display altered sequence coverage between the strains, which may account for the observed differences in raffinose metabolic capacity. Together, these studies support previous findings that raffinose utilization capacity contributes to disease progression, and provide insight into a possible alternative means by which perturbation of this pathway may influence the behavior of pneumococci in the host environment, particularly in meningitis.
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title_short	Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes
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up_date	2024-07-03T22:12:16.866Z
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Streptococcus pneumoniae Strains Isolated From a Single Pediatric Patient Display Distinct Phenotypes

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