Genome-Wide Identification of Genes Essential for the Survival of Streptococcus pneumoniae in Human Saliva
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{"title"=>"Genome-wide identification of genes essential for the survival of Streptococcus pneumoniae in human saliva", "type"=>"journal", "authors"=>[{"first_name"=>"Lilly M.", "last_name"=>"Verhagen", "scopus_author_id"=>"36467443400"}, {"first_name"=>"Marien I.", "last_name"=>"De Jonge", "scopus_author_id"=>"55734436600"}, {"first_name"=>"Peter", "last_name"=>"Burghout", "scopus_author_id"=>"16041680200"}, {"first_name"=>"Kiki", "last_name"=>"Schraa", "scopus_author_id"=>"56067394600"}, {"first_name"=>"Lorenza", "last_name"=>"Spagnuolo", "scopus_author_id"=>"56067344300"}, {"first_name"=>"Svenja", "last_name"=>"Mennens", "scopus_author_id"=>"55632478300"}, {"first_name"=>"Marc J.", "last_name"=>"Eleveld", "scopus_author_id"=>"6603635740"}, {"first_name"=>"Christa E.", "last_name"=>"Van Der Gaast-de Jongh", "scopus_author_id"=>"37059920800"}, {"first_name"=>"Aldert", "last_name"=>"Zomer", "scopus_author_id"=>"57199358873"}, {"first_name"=>"Peter W.M.", "last_name"=>"Hermans", "scopus_author_id"=>"7101909804"}, {"first_name"=>"Hester J.", "last_name"=>"Bootsma", "scopus_author_id"=>"7003601080"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"372599252", "sgr"=>"84896094532", "pmid"=>"24586856", "scopus"=>"2-s2.0-84896094532", "doi"=>"10.1371/journal.pone.0089541", "issn"=>"19326203"}, "id"=>"94bd5cf4-5ca2-3120-8046-613ac6a53765", "abstract"=>"Since Streptococcus pneumoniae transmits through droplet spread, this respiratory tract pathogen may be able to survive in saliva. Here, we show that saliva supports survival of clinically relevant S. pneumoniae strains for more than 24 h in a capsule-independent manner. Moreover, saliva induced growth of S. pneumoniae in growth-permissive conditions, suggesting that S. pneumoniae is well adapted for uptake of nutrients from this bodily fluid. By using Tn-seq, a method for genome-wide negative selection screening, we identified 147 genes potentially required for growth and survival of S. pneumoniae in saliva, among which genes predicted to be involved in cell envelope biosynthesis, cell transport, amino acid metabolism, and stress response predominated. The Tn-seq findings were validated by testing a panel of directed gene deletion mutants for their ability to survive in saliva under two testing conditions: at room temperature without CO2, representing transmission, and at 37 °C with CO2, representing in-host carriage. These validation experiments confirmed that the plsX gene and the amiACDEF and aroDEBC operons, involved in respectively fatty acid metabolism, oligopeptide transport, and biosynthesis of aromatic amino acids play an important role in the growth and survival of S. pneumoniae in saliva at 37 °C. In conclusion, this study shows that S. pneumoniae is well-adapted for growth and survival in human saliva and provides a genome-wide list of genes potentially involved in adaptation. This notion supports earlier evidence that S. pneumoniae can use human saliva as a vector for transmission.", "link"=>"http://www.mendeley.com/research/genomewide-identification-genes-essential-survival-streptococcus-pneumoniae-human-saliva", "reader_count"=>25, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Student > Master"=>9, "Other"=>2, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>4, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>6, "Student > Postgraduate"=>1, "Student > Master"=>9, "Other"=>2, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>2, "Mathematics"=>1, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>2, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1398326/Figure_1.tif"], "description"=>"<p>A. Growth and survival of <i>S. pneumoniae</i> in saliva varies with varying concentrations of saliva. Different dilutions of human saliva in PBS were inoculated with 10<sup>4</sup> CFU ml<sup>−1 </sup><i>S. pneumoniae</i> Spain<sup>9V</sup>-3 at RT without CO<sub>2</sub> (left) or at 37°C with CO<sub>2</sub> (right). After 24 hours of incubation, viable bacterial counts of <i>S. pneumoniae</i> were determined and presented as the percentage of the viable bacterial counts detected at t = 0 h. Each point represents a separate replicate. Horizontal lines indicate geometric means. Saliva concentrations for which CFU ml<sup>−1</sup> significantly differed from 0% saliva by ANOVA and Tukey post-hoc tests are marked with an asterisk (*). Percentages of saliva for which CFU ml<sup>−1</sup> significantly differed from 100% saliva by ANOVA and Tukey post-hoc tests are marked with a black box (▪). B. Effect of bacterial inoculum size on survival and growth of <i>S. pneumoniae</i> Spain<sup>9V</sup>-3 in saliva. Different number of starting CFU were incubated in 100% saliva at RT without CO<sub>2</sub> (left) or at 37°C with CO<sub>2</sub> (right) for indicated periods. Data points represent the geometric mean of three replicate experiments. Vertical lines represent the standard deviations of log10 transformed values.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome analysis tools", "Genetic screens", "genetics", "Functional genomics", "microbiology", "Bacterial pathogens", "streptococci", "Host-pathogen interaction", "Microbial pathogens", "Anatomy and physiology", "Fluid physiology"], "article_id"=>944411, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Lilly M. Verhagen", "Marien I. de Jonge", "Peter Burghout", "Kiki Schraa", "Lorenza Spagnuolo", "Svenja Mennens", "Marc J. Eleveld", "Christa E. van der Gaast-de Jongh", "Aldert Zomer", "Peter W. M. Hermans", "Hester J. Bootsma"], "doi"=>["http://dx.doi.org/10.1371/journal.pone.0089541.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Optimal_conditions_for_growth_and_survival_of_S_pneumoniae_in_saliva_/944411", "title"=>"Optimal conditions for growth and survival of <i>S. pneumoniae</i> in saliva.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-25 03:36:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1398327/Figure_2.tif"], "description"=>"<p>A. Growth characteristics of several <i>S. pneumoniae</i> strains in human saliva. Strains were incubated in 100% saliva at RT without CO<sub>2</sub> (left) or at 37°C with CO<sub>2</sub> (right) for 24 h. Viable bacterial counts are presented as the percentage of the viable bacterial counts detected at t = 0 h. Each point represents a single measurement. Horizontal lines indicate geometric means. B. Competitive growth between wild-type Spain<sup>9V</sup>-3 and its unencapsulated derivative Spain<sup>9V</sup>-3 Δ<i>cps</i>. A 1∶1 ratio of the wild-type and its unencapsulated mutant was inoculated in 100% saliva at 37°C with CO<sub>2</sub> and at RT without CO<sub>2</sub>. Competitive index scores (CI) were determined at t = 4 h and at t = 24 h. Experiments were performed in quadruplicate. Each point represents the log competitive index score of a single measurement. Horizontal lines represent the mean.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome analysis tools", "Genetic screens", "genetics", "Functional genomics", "microbiology", "Bacterial pathogens", "streptococci", "Host-pathogen interaction", "Microbial pathogens", "Anatomy and physiology", "Fluid physiology", "strains"], "article_id"=>944412, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Lilly M. Verhagen", "Marien I. de Jonge", "Peter Burghout", "Kiki Schraa", "Lorenza Spagnuolo", "Svenja Mennens", "Marc J. Eleveld", "Christa E. van der Gaast-de Jongh", "Aldert Zomer", "Peter W. M. Hermans", "Hester J. Bootsma"], "doi"=>["http://dx.doi.org/10.1371/journal.pone.0089541.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Single_and_competitive_growth_characteristics_of_S_pneumoniae_strains_in_human_saliva_/944412", "title"=>"Single and competitive growth characteristics of <i>S. pneumoniae</i> strains in human saliva.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-25 03:36:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1398328/Figure_3.tif"], "description"=>"<p>A. Overlap between genes identified by Tn-seq as important for survival of <i>S. pneumoniae</i> in saliva at RT without CO<sub>2</sub> or at 37°C with CO<sub>2</sub>. B. Biological properties and molecular functions of genes identified by the Tn-seq screen as essential for pneumococcal growth and/or survival in saliva. The numbers of genes within each category are indicated.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome analysis tools", "Genetic screens", "genetics", "Functional genomics", "microbiology", "Bacterial pathogens", "streptococci", "Host-pathogen interaction", "Microbial pathogens", "Anatomy and physiology", "Fluid physiology", "affecting"], "article_id"=>944413, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Lilly M. Verhagen", "Marien I. de Jonge", "Peter Burghout", "Kiki Schraa", "Lorenza Spagnuolo", "Svenja Mennens", "Marc J. Eleveld", "Christa E. van der Gaast-de Jongh", "Aldert Zomer", "Peter W. M. Hermans", "Hester J. Bootsma"], "doi"=>["http://dx.doi.org/10.1371/journal.pone.0089541.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Genes_affecting_survival_of_S_pneumoniae_in_human_saliva_/944413", "title"=>"Genes affecting survival of <i>S. pneumoniae</i> in human saliva.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-25 03:36:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1398329/Figure_4.tif"], "description"=>"<p>A. Single growth experiments. A starting concentration of 10<sup>6</sup> CFU ml<sup>−1</sup> wild-type or mutant bacteria was incubated with saliva at the two conditions. Median and interquartile range (IQR) of the CFU at each time point are displayed. After 24 h at 37°C with CO<sub>2</sub>, all mutant strains showed decreased survival, but this was only statistically significant for Δ<i>aroDEBC</i>. B. Competitive growth experiments. A 1∶1 ratio of the wild type strain and the mutant strain (5*10<sup>5</sup> CFU ml<sup>−1</sup> for each strain) was inoculated in saliva. Each black point represents the log competitive index score of an individual experiment. Values <0 indicate attenuation of the mutant strain. Horizontal lines represent the mean. After 24 h at 37°C with CO<sub>2</sub>, the wild-type strain outcompeted all mutant strains, but this was only statistically significant for Δ<i>amiACDEF</i> and Δ<i>plsX</i>.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome analysis tools", "Genetic screens", "genetics", "Functional genomics", "microbiology", "Bacterial pathogens", "streptococci", "Host-pathogen interaction", "Microbial pathogens", "Anatomy and physiology", "Fluid physiology", "directed", "deletion", "mutants"], "article_id"=>944414, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Lilly M. Verhagen", "Marien I. de Jonge", "Peter Burghout", "Kiki Schraa", "Lorenza Spagnuolo", "Svenja Mennens", "Marc J. Eleveld", "Christa E. van der Gaast-de Jongh", "Aldert Zomer", "Peter W. M. Hermans", "Hester J. Bootsma"], "doi"=>["http://dx.doi.org/10.1371/journal.pone.0089541.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Survival_of_directed_gene_deletion_mutants_in_human_saliva_/944414", "title"=>"Survival of directed gene deletion mutants in human saliva.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-25 03:36:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1398331/Table_1.xls"], "description"=>"a<p>Underlined sequences are complementary to primers used for amplification of antibiotic resistant cassettes.</p>b<p>Left flank and right flank indicate positions relative to the target gene.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome analysis tools", "Genetic screens", "genetics", "Functional genomics", "microbiology", "Bacterial pathogens", "streptococci", "Host-pathogen interaction", "Microbial pathogens", "Anatomy and physiology", "Fluid physiology", "primers", "plasmids"], "article_id"=>944416, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Lilly M. Verhagen", "Marien I. de Jonge", "Peter Burghout", "Kiki Schraa", "Lorenza Spagnuolo", "Svenja Mennens", "Marc J. Eleveld", "Christa E. van der Gaast-de Jongh", "Aldert Zomer", "Peter W. M. Hermans", "Hester J. Bootsma"], "doi"=>["http://dx.doi.org/10.1371/journal.pone.0089541.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Bacterial_strains_primers_and_plasmids_used_in_this_study_/944416", "title"=>"Bacterial strains, primers and plasmids used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-02-25 03:36:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/1398332/Table_S1.xlsx"], "description"=>"<div><p>Since <i>Streptococcus pneumoniae</i> transmits through droplet spread, this respiratory tract pathogen may be able to survive in saliva. Here, we show that saliva supports survival of clinically relevant <i>S. pneumoniae</i> strains for more than 24 h in a capsule-independent manner. Moreover, saliva induced growth of <i>S. pneumoniae</i> in growth-permissive conditions, suggesting that <i>S. pneumoniae</i> is well adapted for uptake of nutrients from this bodily fluid. By using Tn-seq, a method for genome-wide negative selection screening, we identified 147 genes potentially required for growth and survival of <i>S. pneumoniae</i> in saliva, among which genes predicted to be involved in cell envelope biosynthesis, cell transport, amino acid metabolism, and stress response predominated. The Tn-seq findings were validated by testing a panel of directed gene deletion mutants for their ability to survive in saliva under two testing conditions: at room temperature without CO<sub>2</sub>, representing transmission, and at 37°C with CO<sub>2</sub>, representing in-host carriage. These validation experiments confirmed that the <i>plsX</i> gene and the <i>amiACDEF</i> and <i>aroDEBC</i> operons, involved in respectively fatty acid metabolism, oligopeptide transport, and biosynthesis of aromatic amino acids play an important role in the growth and survival of <i>S. pneumoniae</i> in saliva at 37°C. In conclusion, this study shows that <i>S. pneumoniae</i> is well-adapted for growth and survival in human saliva and provides a genome-wide list of genes potentially involved in adaptation. This notion supports earlier evidence that <i>S. pneumoniae</i> can use human saliva as a vector for transmission.</p></div>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome analysis tools", "Genetic screens", "genetics", "Functional genomics", "microbiology", "Bacterial pathogens", "streptococci", "Host-pathogen interaction", "Microbial pathogens", "Anatomy and physiology", "Fluid physiology", "genome-wide", "genes", "saliva"], "article_id"=>944417, "categories"=>["Biological Sciences", "Medicine"], "users"=>["Lilly M. Verhagen", "Marien I. de Jonge", "Peter Burghout", "Kiki Schraa", "Lorenza Spagnuolo", "Svenja Mennens", "Marc J. Eleveld", "Christa E. van der Gaast-de Jongh", "Aldert Zomer", "Peter W. M. Hermans", "Hester J. Bootsma"], "doi"=>["http://dx.doi.org/10.1371/journal.pone.0089541"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/Genome_Wide_Identification_of_Genes_Essential_for_the_Survival_of_Streptococcus_pneumoniae_in_Human_Saliva/944417", "title"=>"Genome-Wide Identification of Genes Essential for the Survival of <i>Streptococcus pneumoniae</i> in Human Saliva", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-02-25 03:36:59"}

PMC Usage Stats | Further Information

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Relative Metric

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