Toxin-Antitoxin Systems Are Important for Niche-Specific Colonization and Stress Resistance of Uropathogenic Escherichia coli
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{"title"=>"Toxin-Antitoxin Systems Are Important for Niche-Specific Colonization and Stress Resistance of Uropathogenic Escherichia coli", "type"=>"journal", "authors"=>[{"first_name"=>"J. Paul", "last_name"=>"Norton", "scopus_author_id"=>"55440830600"}, {"first_name"=>"Matthew A.", "last_name"=>"Mulvey", "scopus_author_id"=>"7005936182"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-84868113986", "sgr"=>"84868113986", "pui"=>"365953701", "isbn"=>"1553-7374 (Electronic)\\n1553-7366 (Linking)", "pmid"=>"23055930", "doi"=>"10.1371/journal.ppat.1002954"}, "id"=>"bc902adc-3751-3bf8-be21-8d1a3e70a73d", "abstract"=>"Toxin-antitoxin (TA) systems are prevalent in many bacterial genomes and have been implicated in biofilm and persister cell formation, but the contribution of individual chromosomally encoded TA systems during bacterial pathogenesis is not well understood. Of the known TA systems encoded by Escherichia coli, only a subset is associated with strains of extraintestinal pathogenic E. coli (ExPEC). These pathogens colonize diverse niches and are a major cause of sepsis, meningitis, and urinary tract infections. Using a murine infection model, we show that two TA systems (YefM-YoeB and YbaJ-Hha) independently promote colonization of the bladder by the reference uropathogenic ExPEC isolate CFT073, while a third TA system comprised of the toxin PasT and the antitoxin PasI is critical to ExPEC survival within the kidneys. The PasTI TA system also enhances ExPEC persister cell formation in the presence of antibiotics and markedly increases pathogen resistance to nutrient limitation as well as oxidative and nitrosative stresses. On its own, low-level expression of PasT protects ExPEC from these stresses, whereas overexpression of PasT is toxic and causes bacterial stasis. PasT-induced stasis can be rescued by overexpression of PasI, indicating that PasTI is a bona fide TA system. By mutagenesis, we find that the stress resistance and toxic effects of PasT can be uncoupled and mapped to distinct domains. Toxicity was specifically linked to sequences within the N-terminus of PasT, a region that also promotes the development of persister cells. These results indicate discrete, multipurpose functions for a TA-associated toxin and demonstrate that individual TA systems can provide bacteria with pronounced fitness advantages dependent on toxin expression levels and the specific environmental niche occupied.", "link"=>"http://www.mendeley.com/research/toxinantitoxin-systems-important-nichespecific-colonization-stress-resistance-uropathogenic-escheric", "reader_count"=>107, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>28, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>2, "Student > Master"=>18, "Other"=>1, "Student > Bachelor"=>7, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>5, "Researcher"=>28, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>2, "Student > Master"=>18, "Other"=>1, "Student > Bachelor"=>7, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>16, "Agricultural and Biological Sciences"=>63, "Medicine and Dentistry"=>10, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>8}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>10}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>8}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>63}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>16}, "Unspecified"=>{"Unspecified"=>4}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"Belgium"=>2, "Iran"=>1, "United States"=>2, "United Kingdom"=>1, "Malaysia"=>1, "France"=>1, "Australia"=>1, "Germany"=>1, "India"=>1}, "group_count"=>11}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/299826", "https://ndownloader.figshare.com/files/299855", "https://ndownloader.figshare.com/files/299887", "https://ndownloader.figshare.com/files/299910", "https://ndownloader.figshare.com/files/299939", "https://ndownloader.figshare.com/files/299973", "https://ndownloader.figshare.com/files/300065", "https://ndownloader.figshare.com/files/300172"], "description"=>"<div><p>Toxin-antitoxin (TA) systems are prevalent in many bacterial genomes and have been implicated in biofilm and persister cell formation, but the contribution of individual chromosomally encoded TA systems during bacterial pathogenesis is not well understood. Of the known TA systems encoded by <em>Escherichia coli</em>, only a subset is associated with strains of extraintestinal pathogenic <em>E. coli</em> (ExPEC). These pathogens colonize diverse niches and are a major cause of sepsis, meningitis, and urinary tract infections. Using a murine infection model, we show that two TA systems (YefM-YoeB and YbaJ-Hha) independently promote colonization of the bladder by the reference uropathogenic ExPEC isolate CFT073, while a third TA system comprised of the toxin PasT and the antitoxin PasI is critical to ExPEC survival within the kidneys. The PasTI TA system also enhances ExPEC persister cell formation in the presence of antibiotics and markedly increases pathogen resistance to nutrient limitation as well as oxidative and nitrosative stresses. On its own, low-level expression of PasT protects ExPEC from these stresses, whereas overexpression of PasT is toxic and causes bacterial stasis. PasT-induced stasis can be rescued by overexpression of PasI, indicating that PasTI is a bona fide TA system. By mutagenesis, we find that the stress resistance and toxic effects of PasT can be uncoupled and mapped to distinct domains. Toxicity was specifically linked to sequences within the N-terminus of PasT, a region that also promotes the development of persister cells. These results indicate discrete, multipurpose functions for a TA-associated toxin and demonstrate that individual TA systems can provide bacteria with pronounced fitness advantages dependent on toxin expression levels and the specific environmental niche occupied.</p> </div>", "links"=>[], "tags"=>["microbiology", "toxin-antitoxin", "systems", "are", "niche-specific", "colonization", "uropathogenic"], "article_id"=>119121, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.s001", "https://dx.doi.org/10.1371/journal.ppat.1002954.s002", "https://dx.doi.org/10.1371/journal.ppat.1002954.s003", "https://dx.doi.org/10.1371/journal.ppat.1002954.s004", "https://dx.doi.org/10.1371/journal.ppat.1002954.s005", "https://dx.doi.org/10.1371/journal.ppat.1002954.s006", "https://dx.doi.org/10.1371/journal.ppat.1002954.s007", "https://dx.doi.org/10.1371/journal.ppat.1002954.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Toxin_Antitoxin_Systems_Are_Important_for_Niche_Specific_Colonization_and_Stress_Resistance_of_Uropathogenic_Escherichia_coli_/119121", "title"=>"Toxin-Antitoxin Systems Are Important for Niche-Specific Colonization and Stress Resistance of Uropathogenic <em>Escherichia coli</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-10-04 02:32:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/564590"], "description"=>"<p>(A) Based on similarities among 21 type II TA alleles, the eBURST algorithm clusters members of phylotype B2 (yellow) together, separate from other sequenced <i>E. coli</i> strains (blue). Strains connected by a line differ by a single TA allele. (B) Genomic maps denoting the relative locations of the type II TA systems encoded by MG1655 and CFT073. Red denotes TA systems that are present in both genomes; <i>yeeUV</i> and its allelic variants are shown in blue.</p>", "links"=>[], "tags"=>["microbiology", "encode", "subsets", "ii", "ta"], "article_id"=>235083, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ExPEC_encode_distinct_subsets_of_type_II_TA_systems_/235083", "title"=>"ExPEC encode distinct subsets of type II TA systems.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:24:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/564700"], "description"=>"<p>(A–H) Adult female CBA/J mice were infected via catheterization with equal numbers of wild type CFT073 and isogenic mutants lacking the indicated type II TA systems as part of either (A–F) competitive or (G and H) non-competitive assays. (A–H) Graphs show bacterial titers present in the bladder or kidneys, as indicated, at 3 d post-inoculation. (E and F) For competitive assays involving wild type CFT073 and CFT073Δ<i>pasTI</i>, bacterial titers recovered from mice at 1 d post-inoculation are also indicated. Bars denote median values for each group; n≥10 mice. <i>P</i> values determined using (A–F) Wilcoxon-matched paired signed rank and (G–H) Mann-Whitney U tests.</p>", "links"=>[], "tags"=>["microbiology", "ta", "systems", "upec", "urinary"], "article_id"=>235197, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distinct_TA_systems_enhance_UPEC_fitness_within_the_urinary_tract_/235197", "title"=>"Distinct TA systems enhance UPEC fitness within the urinary tract.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:26:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/564783"], "description"=>"<p>Adult female (A–B) C3H/HeN and (C–D) C3H/HeJ mice were infected via catheterization with equal numbers of wild type CFT073 and CFT073Δ<i>pasTI</i>. Graphs show bacterial titers present in the (A, C) bladders and (B, D) kidneys at 3 d post-inoculation. Bars indicate median values for each group; n≥10 mice per competitive assay. <i>P</i> values were determined using the Wilcoxon-matched paired signed rank test.</p>", "links"=>[], "tags"=>["microbiology", "colonization", "kidneys"], "article_id"=>235283, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Defective_colonization_of_the_kidneys_by_CFT073_pasTI_in_C3H_HeN_and_C3H_HeJ_mice_/235283", "title"=>"Defective colonization of the kidneys by CFT073Δ<i>pasTI</i> in C3H/HeN and C3H/HeJ mice.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:28:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/564888"], "description"=>"<p>Development of persister cells by (A) wild type CFT073 and associated type II TA system knockout mutants or (B) MG1655 and associated Δ<i>pasTI</i> mutant 5 h after the addition of 100 µg/mL ampicillin or 10 µg/mL ciprofloxacin to cultures in exponential growth phase. Data represent mean results ± SD from three independent experiments. <i>P</i> values were determined by Student's <i>t</i> test.</p>", "links"=>[], "tags"=>["microbiology", "requires"], "article_id"=>235391, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Persister_cell_formation_by_CFT073_but_not_MG1655_requires_PasTI_/235391", "title"=>"Persister cell formation by CFT073, but not MG1655, requires PasTI.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:29:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/564968"], "description"=>"<p>Growth of wild type CFT073 and type II TA system knockouts in (A) M9 medium+0.2% casein amino acids, (B) a modified, lower-nutrient M9 medium+Thr, (C) LB broth, (D) LB broth containing 0.5 mM MV, (E) LB buffered to pH 5.0 with MES (MES-LB), and (F) MES-LB with 1 mM ASN. Graphs are representative of at least three independent experiments performed in quadruplicate.</p>", "links"=>[], "tags"=>["microbiology"], "article_id"=>235468, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PasTI_promotes_the_stress_resistance_of_CFT073_/235468", "title"=>"PasTI promotes the stress resistance of CFT073.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:31:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/565093"], "description"=>"<p>(A–B) Images show wild type and CFT073Δ<i>pasTI</i> colonies on LB agar after overnight growth at 37°C; inset images show images of individual wild type and CFT073Δ<i>pasTI</i> colonies at identical magnification. (C–D) Colony sizes of CFT073Δ<i>pasTI</i> complemented with empty vector (pRR48) or pPN007, which allows for leaky expression of PasT from a P<i>tac</i> promoter. (E–G, left) Images show colonies of ExPEC strains and associated Δ<i>pasTI</i> mutants on LB agar after overnight growth at 37°C. (E–G, right) Growth of the ExPEC Δ<i>pasTI</i> mutants in 1 mM ASN is delayed compared to wild type. In each graph, solid lines represent the wild type strains and dashed lines indicate the Δ<i>pasTI</i> mutants. Images in A–G were taken at the same magnification (scale bar, 1 cm). All Δ<i>pasTI</i> colonies eventually reach wild type size.</p>", "links"=>[], "tags"=>["microbiology", "expec"], "article_id"=>235592, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_pasTI_reduces_the_stress_resistance_of_multiple_ExPEC_isolates_/235592", "title"=>"Deletion of <i>pasTI</i> reduces the stress resistance of multiple ExPEC isolates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:33:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/565246"], "description"=>"<p>(A–C) Graphs show growth of recombinant CFT073 strains in (A) 1 mM ASN or (B, C) standard LB broth. (D) Curves show growth of recombinant MG1655 strains in 1 mM ASN. In B and C, IPTG and arabinose were added as indicated to induce high-level expression of PasT and PasI, respectively. (A, D) Alternatively, recombinant PasT and PasI were expressed at lower levels from a leaky P<i>tac</i> promoter. The <i>pasT</i> gene cloned from MG1655 was used as indicated. Otherwise, recombinant genes were derived from CFT073. Graphs are representative of at least 3 independent experiments performed in quadruplicate. (E) Bottom, the <i>pasT</i> gene carried by CFT073 and other ExPEC has a conserved set of synonymous (purple hashes) and two non-synonymous (red hashes) base pair changes relative to <i>pasT</i> encoded by MG1655 and many other <i>E. coli</i> strains. Top, the predicted secondary structure of PasT, with two conserved amino acid differences between the MG1655 and ExPEC-associated protein sequences highlighted.</p>", "links"=>[], "tags"=>["microbiology", "countered"], "article_id"=>235743, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PasT_has_stress_resistance_and_toxic_effects_the_latter_of_which_can_be_countered_by_PasI_/235743", "title"=>"PasT has stress resistance and toxic effects, the latter of which can be countered by PasI.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:35:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/565317"], "description"=>"<p>(A) Table indicates if the specified PasT truncation mutants and fusions display toxic, growth inhibitory effects when overexpressed in CFT073Δ<i>pasTI</i>, if their leaky expression rescues wild type (WT) growth of the Δ<i>pasTI</i> mutant in 1 mM ASN and on LB agar plates, and if their leaky expression rescues the ability of CFT073Δ<i>pasTI</i> to form persisters in the presence of ciprofloxacin (10 µg/mL). ND, not determined. (B) Western blot shows expression levels of C-terminal FLAG-tagged PasT constructs—denoted (ii)–(vi), as in (A)—following induction with IPTG. Lane (i) represents an empty vector control. A nonspecific band recognized by the anti-FLAG antibody was used as loading control. Equal loading was also verified by Coomassie staining (data not shown).</p>", "links"=>[], "tags"=>["microbiology", "salubrious", "genetically"], "article_id"=>235816, "categories"=>["Biological Sciences"], "users"=>["J. Paul Norton", "Matthew A. Mulvey"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002954.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_toxic_and_salubrious_effects_of_PasT_can_be_genetically_uncoupled_/235816", "title"=>"The toxic and salubrious effects of PasT can be genetically uncoupled.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-10-04 01:36:56"}

PMC Usage Stats | Further Information

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Relative Metric

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