Nucleotide Biosynthesis Is Critical for Growth of Bacteria in Human Blood
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{"title"=>"Nucleotide biosynthesis is critical for growth of bacteria in human blood", "type"=>"journal", "authors"=>[{"first_name"=>"Shalaka", "last_name"=>"Samant", "scopus_author_id"=>"57200975090"}, {"first_name"=>"Hyunwoo", "last_name"=>"Lee", "scopus_author_id"=>"36243615800"}, {"first_name"=>"Mahmood", "last_name"=>"Ghassemi", "scopus_author_id"=>"7003966051"}, {"first_name"=>"Juan", "last_name"=>"Chen", "scopus_author_id"=>"55717768100"}, {"first_name"=>"James L.", "last_name"=>"Cook", "scopus_author_id"=>"16486468100"}, {"first_name"=>"Alexander S.", "last_name"=>"Mankin", "scopus_author_id"=>"7005529709"}, {"first_name"=>"Alexander A.", "last_name"=>"Neyfakh", "scopus_author_id"=>"35569225900"}], "year"=>2008, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-40349098615", "sgr"=>"40349098615", "pui"=>"351340705", "isbn"=>"1553-7374 (Electronic)", "pmid"=>"18282099", "doi"=>"10.1371/journal.ppat.0040037"}, "id"=>"124ae758-1705-3bb1-8612-dcf2037d5598", "abstract"=>"Proliferation of bacterial pathogens in blood represents one of the most dangerous stages of infection. Growth in blood serum depends on the ability of a pathogen to adjust metabolism to match the availability of nutrients. Although certain nutrients are scarce in blood and need to be de novo synthesized by proliferating bacteria, it is unclear which metabolic pathways are critical for bacterial growth in blood. In this study, we identified metabolic functions that are essential specifically for bacterial growth in the bloodstream. We used two principally different but complementing techniques to comprehensively identify genes that are required for the growth of Escherichia coli in human serum. A microarray-based and a dye-based mutant screening approach were independently used to screen a library of 3,985 single-gene deletion mutants in all non-essential genes of E. coli (Keio collection). A majority of the mutants identified consistently by both approaches carried a deletion of a gene involved in either the purine or pyrimidine nucleotide biosynthetic pathway and showed a 20- to 1,000-fold drop in viable cell counts as compared to wild-type E. coli after 24 h of growth in human serum. This suggests that the scarcity of nucleotide precursors, but not other nutrients, is the key limitation for bacterial growth in serum. Inactivation of nucleotide biosynthesis genes in another Gram-negative pathogen, Salmonella enterica, and in the Gram-positive pathogen Bacillus anthracis, prevented their growth in human serum. The growth of the mutants could be rescued by genetic complementation or by addition of appropriate nucleotide bases to human serum. Furthermore, the virulence of the B. anthracis purE mutant, defective in purine biosynthesis, was dramatically attenuated in a murine model of bacteremia. Our data indicate that de novo nucleotide biosynthesis represents the single most critical metabolic function for bacterial growth in blood and reveal the corresponding enzymes as putative antibiotic targets for the treatment of bloodstream infections.", "link"=>"http://www.mendeley.com/research/nucleotide-biosynthesis-critical-growth-bacteria-human-blood-4", "reader_count"=>90, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>25, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>14, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>25, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>29, "Student > Postgraduate"=>1, "Student > Master"=>14, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>56, "Medicine and Dentistry"=>6, "Neuroscience"=>1, "Business, Management and Accounting"=>1, "Veterinary Science and Veterinary Medicine"=>2, "Chemistry"=>5, "Immunology and Microbiology"=>7}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>5}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>7}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>56}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>4, "Denmark"=>1, "Poland"=>1, "United Kingdom"=>2, "Chile"=>1, "Estonia"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/937506"], "description"=>"<div><p>(A) Ratios of the viable cell counts of the <i>carA</i>, <i>pyrC</i>, <i>purE</i> and <i>purK</i> mutants as compared to wild-type B. anthracis after 24 h of growth in human serum (<i>p</i> value <1 × 10<sup>−5</sup>). Statistical significance of respective mutants relative to wild type was calculated using <i>t</i>-test in EXCEL.</p><p>(B) Ratios of the viable cell counts of <i>purE</i>, <i>carA</i>, <i>pyrC</i> and <i>purK</i> mutants (black bars) and the viable cell counts of <i>purE</i>/pPurE<sub>BA</sub>, <i>carA</i>/pCarA<sub>BA</sub>, <i>pyrC</i>/pPyrC<sub>BA</sub>, <i>purK</i>/pPurK<sub>BA</sub>, wt + pHT304 and wt + pHTSPAC (grey bars) to that of wild-type B. anthracis following 24 h of growth in serum.</p><p>(C) Grey bars represent ratios of the viable cell counts of each mutant to that of wild-type B. anthracis after 24 h of growth in serum supplemented with 1 mM adenine (purine mutants) and 1 mM uracil (pyrimidine mutants). Black bars represent these ratios in serum without any nucleotide supplements. Error bars indicate SD of triplicate experiments.</p><p>(D) Attenuation of <i>B. anthracis purE</i> mutant in a murine model of bacteremia. Survival curves (Average Latency Survival) were derived from transformation of daily LD<sub>50</sub>s estimated for mouse cohorts challenged intravenously with a dose range (10<sup>3</sup>–10<sup>8</sup>) of vegetative cells of the indicated B. anthracis strains. Points on survival curves represent the mean ± SEM values from three (Sterne, <i>purE</i>) or two (<i>purE</i>/pPurE<sub>BA</sub>, <i>purK</i>) different mouse experiments. LD<sub>50</sub> values shown in the graph represent the final values estimated at the end of the 6-day observation periods. Survival results were unchanged when mice were observed for an additional 2 weeks.</p></div>", "links"=>[], "tags"=>["nucleotide", "biosynthetic", "mutants"], "article_id"=>607949, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Shalaka Samant", "Hyunwoo Lee", "Mahmood Ghassemi", "Juan Chen", "James L Cook", "Alexander S Mankin", "Alexander A Neyfakh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0040037.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_B_anthracis_Nucleotide_Biosynthetic_Mutants_Are_Unable_to_Grow_in_Human_Serum_/607949", "title"=>"B. anthracis Nucleotide Biosynthetic Mutants Are Unable to Grow in Human Serum", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-15 02:12:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/937302"], "description"=>"<p>Purine and pyrimidine nucleotide biosynthesis pathways in E. coli are outlined. Genes that were identified to be essential for the growth of E. coli in human serum by the MGK approach are underlined in black and those identified by the MTT assay are underlined in grey. Essential genes, whose deletions are absent from the defined library of E. coli mutants, are marked by an asterisk. Genes whose deletion does not confer a growth defect in serum are <i>pyrI</i>, <i>ndk</i>, <i>purN</i> and <i>purT</i>. The <i>pyrD</i> mutant was not identified by either screen, although it showed a growth defect in human serum.</p>", "links"=>[], "tags"=>["serum", "mgk", "mtt"], "article_id"=>607742, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Shalaka Samant", "Hyunwoo Lee", "Mahmood Ghassemi", "Juan Chen", "James L Cook", "Alexander S Mankin", "Alexander A Neyfakh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0040037.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_Required_for_the_Growth_of_E_coli_in_Human_Serum_Identified_by_MGK_and_MTT_Assay_/607742", "title"=>"Genes Required for the Growth of E. coli in Human Serum Identified by MGK and MTT Assay", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-15 02:09:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/461845", "https://ndownloader.figshare.com/files/461889", "https://ndownloader.figshare.com/files/461908", "https://ndownloader.figshare.com/files/461934", "https://ndownloader.figshare.com/files/462009", "https://ndownloader.figshare.com/files/462055", "https://ndownloader.figshare.com/files/462083"], "description"=>"<div><p>Proliferation of bacterial pathogens in blood represents one of the most dangerous stages of infection. Growth in blood serum depends on the ability of a pathogen to adjust metabolism to match the availability of nutrients. Although certain nutrients are scarce in blood and need to be <em>de novo</em> synthesized by proliferating bacteria, it is unclear which metabolic pathways are critical for bacterial growth in blood. In this study, we identified metabolic functions that are essential specifically for bacterial growth in the bloodstream. We used two principally different but complementing techniques to comprehensively identify genes that are required for the growth of Escherichia coli in human serum. A microarray-based and a dye-based mutant screening approach were independently used to screen a library of 3,985 single-gene deletion mutants in all non-essential genes of E. coli (Keio collection). A majority of the mutants identified consistently by both approaches carried a deletion of a gene involved in either the purine or pyrimidine nucleotide biosynthetic pathway and showed a 20- to 1,000-fold drop in viable cell counts as compared to wild-type E. coli after 24 h of growth in human serum. This suggests that the scarcity of nucleotide precursors, but not other nutrients, is the key limitation for bacterial growth in serum. Inactivation of nucleotide biosynthesis genes in another Gram-negative pathogen, Salmonella enterica, and in the Gram-positive pathogen Bacillus anthracis, prevented their growth in human serum. The growth of the mutants could be rescued by genetic complementation or by addition of appropriate nucleotide bases to human serum. Furthermore, the virulence of the <em>B. anthracis purE</em> mutant, defective in purine biosynthesis, was dramatically attenuated in a murine model of bacteremia. Our data indicate that <em>de novo</em> nucleotide biosynthesis represents the single most critical metabolic function for bacterial growth in blood and reveal the corresponding enzymes as putative antibiotic targets for the treatment of bloodstream infections.</p></div>", "links"=>[], "tags"=>["nucleotide", "biosynthesis"], "article_id"=>151017, "categories"=>["Cancer", "Microbiology"], "users"=>["Shalaka Samant", "Hyunwoo Lee", "Mahmood Ghassemi", "Juan Chen", "James L Cook", "Alexander S Mankin", "Alexander A Neyfakh"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.0040037.sg001", "https://dx.doi.org/10.1371/journal.ppat.0040037.sg002", "https://dx.doi.org/10.1371/journal.ppat.0040037.sg003", "https://dx.doi.org/10.1371/journal.ppat.0040037.sd001", "https://dx.doi.org/10.1371/journal.ppat.0040037.st001", "https://dx.doi.org/10.1371/journal.ppat.0040037.st002", "https://dx.doi.org/10.1371/journal.ppat.0040037.st003"], "stats"=>{"downloads"=>8, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Nucleotide_Biosynthesis_Is_Critical_for_Growth_of_Bacteria_in_Human_Blood/151017", "title"=>"Nucleotide Biosynthesis Is Critical for Growth of Bacteria in Human Blood", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-02-15 00:16:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/937393"], "description"=>"<div><p>(A) Ratios of the viable cell counts of 19 mutants identified by either MGK or MTT assay as compared to wild-type E. coli after 24 h of growth in human serum. <i>p</i> Values for each mutant relative to wild type were lower than 0.001.</p><p>(B) Ratios of the viable cell counts of <i>carA</i>, <i>pyrE</i>, <i>purA</i>, <i>purE</i> and <i>guaB</i> mutants (black bars) and the viable cell counts of <i>carA</i>/pCarA<sub>EC</sub>, <i>pyrE</i>/pPyrE<sub>EC</sub>, <i>purA</i>/pPurA<sub>EC</sub>, <i>purE</i>/pPurE<sub>EC</sub>, <i>guaB</i>/pGuaB<sub>EC</sub> and wt+pBAD22 (grey bars) to those of wild-type E. coli following 24 h of growth in serum.</p><p>(C) Grey bars represent ratios of the viable cell counts of each pyrimidine mutant to that of the wild-type E. coli after 24 h of growth in serum supplemented with 1 mM uracil. Black bars represent these ratios in serum without any nucleotide supplements.</p><p>(D) Grey bars represent ratios of the viable cell counts of each purine mutant to that of the wild-type E. coli after 24 h of growth in serum supplemented with 1 mM adenine. Black bars represent these ratios in serum without any nucleotide supplements.</p><p>(E) Ratios of the viable cell counts of Tn5 transposon insertion mutants in several <i>pur</i> and <i>pyr</i> genes of S. typhimurium to that of the wild type determined after 24 h of growth in human serum by plating serial dilutions on LB agar plates are represented by vertical bars. <i>p</i> Values for each mutant relative to wild type were lower than 0.01. Error bars indicate standard deviation (SD) for two independent experiments. Statistical significance of the data was calculated using <i>t</i>-test in EXCEL.</p></div>", "links"=>[], "tags"=>["typhimurium", "mutants", "defect"], "article_id"=>607834, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Shalaka Samant", "Hyunwoo Lee", "Mahmood Ghassemi", "Juan Chen", "James L Cook", "Alexander S Mankin", "Alexander A Neyfakh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0040037.g003", "stats"=>{"downloads"=>3, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_E_coli_and_S_typhimurium_pur_and_pyr_Mutants_Have_a_Growth_Defect_in_Human_Serum_/607834", "title"=>"E. coli and <i>S. typhimurium pur</i> and <i>pyr</i> Mutants Have a Growth Defect in Human Serum", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-15 02:10:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/937223"], "description"=>"<div><p>(A) Schematic representation of the identification of E. coli mutants from the Keio library with a growth defect in human serum using Monitoring of Gene Knockouts (MGK).</p><p>(B) MTT dye-based screening for mutants with a growth defect in human serum. MTT was added after 24 h of growing the arrayed mutant library in 96-well plates in either LB medium or serum. Mutants that could grow in serum generated a deep blue color by reducing MTT. The lack of a blue color in a serum bacterial culture served as a qualitative indicator of the inability of that mutant to grow in serum.</p></div>", "links"=>[], "tags"=>["genes"], "article_id"=>607665, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Shalaka Samant", "Hyunwoo Lee", "Mahmood Ghassemi", "Juan Chen", "James L Cook", "Alexander S Mankin", "Alexander A Neyfakh"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.0040037.g001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_Genes_Required_for_the_Growth_of_E_coli_in_Human_Serum_/607665", "title"=>"Identification of Genes Required for the Growth of E. coli in Human Serum", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-15 02:07:45"}

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Relative Metric

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