Within-host microevolution of Streptococcus pneumoniae is rapid and adaptive during natural colonisation

Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae , an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate wi...

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Veröffentlicht in:	Nature communications Jg. 11; H. 1; S. 3442 - 14
Hauptverfasser:	Chaguza, Chrispin, Senghore, Madikay, Bojang, Ebrima, Gladstone, Rebecca A., Lo, Stephanie W., Tientcheu, Peggy-Estelle, Bancroft, Rowan E., Worwui, Archibald, Foster-Nyarko, Ebenezer, Ceesay, Fatima, Okoi, Catherine, McGee, Lesley, Klugman, Keith P., Breiman, Robert F., Barer, Michael R., Adegbola, Richard A., Antonio, Martin, Bentley, Stephen D., Kwambana-Adams, Brenda A.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 10.07.2020 Nature Publishing Group Nature Portfolio
Schlagworte:	13 45 45/23 631/208/212/2304 631/208/325/2482 631/326/107 692/308/3187 Antibiotic resistance Antibiotics Colonization Divergence Drug resistance Evolution Evolution, Molecular Evolutionary genetics Gene sequencing Genetic diversity Genetics Genome, Bacterial - genetics Genomes Genomics Homologous recombination Homology Humanities and Social Sciences Humans Infants multidisciplinary Nucleotides Opportunist infection Pathogenesis Pathogens Pneumococcal Infections - genetics Science Science (multidisciplinary) Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - genetics Substitutes Whole Genome Sequencing
ISSN:	2041-1723, 2041-1723
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Abstract	Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae , an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation. Streptococcus pneumoniae is an opportunistic pathogen and asymptomatic colonization is a precursor for invasive disease. Here the authors show rapid within-host evolution of naturally acquired pneumococci in ninety-eight infants driven by high nucleotide substitution rates and intra-host homologous recombination.
AbstractList	Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae , an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation. Streptococcus pneumoniae is an opportunistic pathogen and asymptomatic colonization is a precursor for invasive disease. Here the authors show rapid within-host evolution of naturally acquired pneumococci in ninety-eight infants driven by high nucleotide substitution rates and intra-host homologous recombination. Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae, an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation.Streptococcus pneumoniae is an opportunistic pathogen and asymptomatic colonization is a precursor for invasive disease. Here the authors show rapid within-host evolution of naturally acquired pneumococci in ninety-eight infants driven by high nucleotide substitution rates and intra-host homologous recombination. Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae , an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation. Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae, an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation.Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae, an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation. Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae, an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal carriage. However, little is known about genomic changes during natural colonisation. Here, we use whole-genome sequencing to investigate within-host microevolution of naturally carried pneumococci in ninety-eight infants intensively sampled sequentially from birth until twelve months in a high-carriage African setting. We show that neutral evolution and nucleotide substitution rates up to forty-fold faster than observed over longer timescales in S. pneumoniae and other bacteria drives high within-host pneumococcal genetic diversity. Highly divergent co-existing strain variants emerge during colonisation episodes through real-time intra-host homologous recombination while the rest are co-transmitted or acquired independently during multiple colonisation episodes. Genic and intergenic parallel evolution occur particularly in antibiotic resistance, immune evasion and epithelial adhesion genes. Our findings suggest that within-host microevolution is rapid and adaptive during natural colonisation. Streptococcus pneumoniae is an opportunistic pathogen and asymptomatic colonization is a precursor for invasive disease. Here the authors show rapid within-host evolution of naturally acquired pneumococci in ninety-eight infants driven by high nucleotide substitution rates and intra-host homologous recombination.
ArticleNumber	3442
Author	Barer, Michael R. Worwui, Archibald Bojang, Ebrima Senghore, Madikay Okoi, Catherine Tientcheu, Peggy-Estelle Bancroft, Rowan E. Chaguza, Chrispin Gladstone, Rebecca A. Kwambana-Adams, Brenda A. Breiman, Robert F. Ceesay, Fatima McGee, Lesley Adegbola, Richard A. Bentley, Stephen D. Antonio, Martin Lo, Stephanie W. Foster-Nyarko, Ebenezer Klugman, Keith P.
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/32651390$$D View this record in MEDLINE/PubMed
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Snippet	Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae , an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal... Genomic evolution, transmission and pathogenesis of Streptococcus pneumoniae, an opportunistic human-adapted pathogen, is driven principally by nasopharyngeal... Streptococcus pneumoniae is an opportunistic pathogen and asymptomatic colonization is a precursor for invasive disease. Here the authors show rapid...
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SubjectTerms	13 45 45/23 631/208/212/2304 631/208/325/2482 631/326/107 692/308/3187 Antibiotic resistance Antibiotics Colonization Divergence Drug resistance Evolution Evolution, Molecular Evolutionary genetics Gene sequencing Genetic diversity Genetics Genome, Bacterial - genetics Genomes Genomics Homologous recombination Homology Humanities and Social Sciences Humans Infants multidisciplinary Nucleotides Opportunist infection Pathogenesis Pathogens Pneumococcal Infections - genetics Science Science (multidisciplinary) Streptococcus infections Streptococcus pneumoniae Streptococcus pneumoniae - genetics Substitutes Whole Genome Sequencing
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Title	Within-host microevolution of Streptococcus pneumoniae is rapid and adaptive during natural colonisation
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