Staphylococcus aureus Survives with a Minimal Peptidoglycan Synthesis Machine but Sacrifices Virulence and Antibiotic Resistance
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{"title"=>"Staphylococcus aureus Survives with a Minimal Peptidoglycan Synthesis Machine but Sacrifices Virulence and Antibiotic Resistance", "type"=>"journal", "authors"=>[{"first_name"=>"Patricia", "last_name"=>"Reed", "scopus_author_id"=>"36755015900"}, {"first_name"=>"Magda L.", "last_name"=>"Atilano", "scopus_author_id"=>"15029741400"}, {"first_name"=>"Renato", "last_name"=>"Alves", "scopus_author_id"=>"37071967900"}, {"first_name"=>"Egbert", "last_name"=>"Hoiczyk", "scopus_author_id"=>"6602320464"}, {"first_name"=>"Xinwei", "last_name"=>"Sher", "scopus_author_id"=>"56667756300"}, {"first_name"=>"Nathalie T.", "last_name"=>"Reichmann", "scopus_author_id"=>"50462327000"}, {"first_name"=>"Pedro M.", "last_name"=>"Pereira", "scopus_author_id"=>"22235487300"}, {"first_name"=>"Terry", "last_name"=>"Roemer", "scopus_author_id"=>"6701580936"}, {"first_name"=>"Sérgio R.", "last_name"=>"Filipe", "scopus_author_id"=>"6603602919"}, {"first_name"=>"José B.", "last_name"=>"Pereira-Leal", "scopus_author_id"=>"55940842900"}, {"first_name"=>"Petros", "last_name"=>"Ligoxygakis", "scopus_author_id"=>"6603262836"}, {"first_name"=>"Mariana G.", "last_name"=>"Pinho", "scopus_author_id"=>"7007036822"}], "year"=>2015, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"604704913", "sgr"=>"84930338794", "issn"=>"15537374", "pmid"=>"25951442", "scopus"=>"2-s2.0-84930338794", "doi"=>"10.1371/journal.ppat.1004891", "isbn"=>"10.1371/journal.ppat.1004891"}, "id"=>"311abf95-850f-3451-89e0-b4a6c61796f0", "abstract"=>"Many important cellular processes are performed by molecular machines, composed of multiple proteins that physically interact to execute biological functions. An example is the bacterial peptidoglycan (PG) synthesis machine, responsible for the synthesis of the main component of the cell wall and the target of many contemporary antibiotics. One approach for the identification of essential components of a cellular machine involves the determination of its minimal protein composition. Staphylococcus aureus is a Gram-positive pathogen, renowned for its resistance to many commonly used antibiotics and prevalence in hospitals. Its genome encodes a low number of proteins with PG synthesis activity (9 proteins), when compared to other model organisms, and is therefore a good model for the study of a minimal PG synthesis machine. We deleted seven of the nine genes encoding PG synthesis enzymes from the S. aureus genome without affecting normal growth or cell morphology, generating a strain capable of PG biosynthesis catalyzed only by two penicillin-binding proteins, PBP1 and the bi-functional PBP2. However, multiple PBPs are important in clinically relevant environments, as bacteria with a minimal PG synthesis machinery became highly susceptible to cell wall-targeting antibiotics, host lytic enzymes and displayed impaired virulence in a Drosophila infection model which is dependent on the presence of specific peptidoglycan receptor proteins, namely PGRP-SA. The fact that S. aureus can grow and divide with only two active PG synthesizing enzymes shows that most of these enzymes are redundant in vitro and identifies the minimal PG synthesis machinery of S. aureus. However a complex molecular machine is important in environments other than in vitro growth as the expendable PG synthesis enzymes play an important role in the pathogenicity and antibiotic resistance of S. aureus.", "link"=>"http://www.mendeley.com/research/staphylococcus-aureus-survives-minimal-peptidoglycan-synthesis-machine-sacrifices-virulence-antibiot", "reader_count"=>86, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Researcher"=>23, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>27, "Student > Postgraduate"=>2, "Student > Master"=>13, "Other"=>3, "Student > Bachelor"=>4, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>1, "Researcher"=>23, "Student > Doctoral Student"=>7, "Student > Ph. D. Student"=>27, "Student > Postgraduate"=>2, "Student > Master"=>13, "Other"=>3, "Student > Bachelor"=>4, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>22, "Agricultural and Biological Sciences"=>44, "Medicine and Dentistry"=>3, "Physics and Astronomy"=>1, "Chemistry"=>4, "Immunology and Microbiology"=>9}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>4}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>9}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>44}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>22}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Canada"=>1, "United States"=>1, "United Kingdom"=>2, "Portugal"=>3}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2059437"], "description"=>"<p><b>(A)</b> The blue, stacked bars represent the total number of proteins present in each species that have a transpeptidase (dark blue) or transglycosylase (light blue) domain. The total number of proteins that have at least one of the two domains is displayed numerically. Strains highlighted in pink are bacteria reported not to possess cell wall, although they may produce small but functional amounts of peptidoglycan. The maximum likelihood species tree was calculated using PhyML [<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004891#ppat.1004891.ref053\" target=\"_blank\">53</a>] and concatenated bacterial marker genes identified with the AMPHORA2 [<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004891#ppat.1004891.ref052\" target=\"_blank\">52</a>] software. <b>(B)</b> Table showing the peptidoglycan synthesis proteins from <i>S</i>. <i>aureus</i> and their established or hypothetical activities.</p>", "links"=>[], "tags"=>["Minimal Peptidoglycan Synthesis Machine", "PG synthesis machinery", "PG biosynthesis", "PBP 1", "Cell Morphology", "genes encoding PG synthesis enzymes", "synthesis machine", "Sacrifices Virulence", "host lytic enzymes", "Antibiotic resistance", "PG synthesizing enzymes", "aureus genome", "peptidoglycan receptor proteins", "protein composition", "Staphylococcus aureus Survives", "PG synthesis machine", "Staphylococcus aureus", "cell wall", "Drosophila infection model", "PG synthesis enzymes", "Model organisms", "genome encodes"], "article_id"=>1408143, "categories"=>["Biological Sciences"], "users"=>["Patricia Reed", "Magda L. Atilano", "Renato Alves", "Egbert Hoiczyk", "Xinwei Sher", "Nathalie T. Reichmann", "Pedro M. Pereira", "Terry Roemer", "Sergio R. Filipe", "José B. Pereira-Leal", "Petros Ligoxygakis", "Mariana G. Pinho"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004891.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_distribution_of_peptidoglycan_synthesis_enzymes_across_selected_bacterial_species_/1408143", "title"=>"Phylogenetic distribution of peptidoglycan synthesis enzymes across selected bacterial species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-07 03:33:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2059439"], "description"=>"<p><b>(A)</b> Growth of the parental strain COL and the minimal mutant strain COL MIN was followed in rich liquid medium by monitoring the absorbance at OD<sub>600nm</sub>. The mutant strain COL MIN (doubling time 40 min) showed similar growth to the parental strain COL (doubling time 36 min). <b>(B)</b> Growth of COL and COL MIN was followed in minimal medium by monitoring the absorbance at OD<sub>600nm</sub>. The mutant strain COL MIN (doubling time 67 min) showed similar growth to the parental strain COL (doubling time 61 min). <b>(C)</b> Depletion of PBP1 from COL PBP1i and COL MIN PBP1i, in which PBP1 expression is under the control of the IPTG inducible P<sub><i>spac</i></sub> promoter, by growing cells in the absence of IPTG, led to a halt in cell growth and subsequent drop in optical density indicating PBP1 is essential for survival of both the parental and mutant strains. <b>(D)</b> In the absence of PBP2, strain COL PBP2i (parental strain COL with PBP2 expression under the control of the IPTG inducible P<sub><i>spac</i></sub> promoter) continues to grow. However, depletion of PBP2 from COL MIN PBP2i causes arrest in growth indicating PBP2 is essential for growth of COL MIN. Averages of three independent replicates are shown and error bars show standard deviations.</p>", "links"=>[], "tags"=>["Minimal Peptidoglycan Synthesis Machine", "PG synthesis machinery", "PG biosynthesis", "PBP 1", "Cell Morphology", "genes encoding PG synthesis enzymes", "synthesis machine", "Sacrifices Virulence", "host lytic enzymes", "Antibiotic resistance", "PG synthesizing enzymes", "aureus genome", "peptidoglycan receptor proteins", "protein composition", "Staphylococcus aureus Survives", "PG synthesis machine", "Staphylococcus aureus", "cell wall", "Drosophila infection model", "PG synthesis enzymes", "Model organisms", "genome encodes"], "article_id"=>1408145, "categories"=>["Biological Sciences"], "users"=>["Patricia Reed", "Magda L. Atilano", "Renato Alves", "Egbert Hoiczyk", "Xinwei Sher", "Nathalie T. Reichmann", "Pedro M. Pereira", "Terry Roemer", "Sergio R. Filipe", "José B. Pereira-Leal", "Petros Ligoxygakis", "Mariana G. Pinho"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004891.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_S_aureus_minimal_mutant_strain_COL_MIN_displays_normal_growth_and_requires_PBP1_and_PBP2_for_survival_/1408145", "title"=>"<i>S</i>. <i>aureus</i> minimal mutant strain COL MIN displays normal growth and requires PBP1 and PBP2 for survival.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-07 03:33:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2059441"], "description"=>"<p><b>(A)</b> Structured illumination microscopy images of cells incubated with (i) Van-FL, and (ii) Hoechst 33342 to label the cell wall and DNA, respectively, show no difference between the parental strain COL and COL MIN, (iii) overlay of Van-FL and Hoechst labeled cells. Scale bars represent 1μm. (<b>B</b>) Percentage of cells with complete septa (i), partial septa (ii) and no septa (iii) in COL (n = 333) and COL MIN (n = 223) strains. <b>(C)</b> Representative electron microscopy images of COL and COL MIN show that cells retain a normal shape and septum placement in the absence of seven PG synthesis enzymes. <b>(D)</b> Localization of PBP1 (i), PBP2 (ii) and FtsZ (iii), by immunofluorescence, in COLΔ<i>spa</i> and COL MIN Δ<i>spa</i> cells shows that the three proteins localize to the septum in the COL MIN strain, similarly to the parental strain COL. FtsZ was used as a control for septal localization. Strains lacking the <i>spa</i> gene were used for immunofluorescence experiments as the <i>spa</i> gene product Protein A binds with high affinity to IgG molecules. Scale bar represents 1μm.</p>", "links"=>[], "tags"=>["Minimal Peptidoglycan Synthesis Machine", "PG synthesis machinery", "PG biosynthesis", "PBP 1", "Cell Morphology", "genes encoding PG synthesis enzymes", "synthesis machine", "Sacrifices Virulence", "host lytic enzymes", "Antibiotic resistance", "PG synthesizing enzymes", "aureus genome", "peptidoglycan receptor proteins", "protein composition", "Staphylococcus aureus Survives", "PG synthesis machine", "Staphylococcus aureus", "cell wall", "Drosophila infection model", "PG synthesis enzymes", "Model organisms", "genome encodes"], "article_id"=>1408147, "categories"=>["Biological Sciences"], "users"=>["Patricia Reed", "Magda L. Atilano", "Renato Alves", "Egbert Hoiczyk", "Xinwei Sher", "Nathalie T. Reichmann", "Pedro M. Pereira", "Terry Roemer", "Sergio R. Filipe", "José B. Pereira-Leal", "Petros Ligoxygakis", "Mariana G. Pinho"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004891.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_S_aureus_strain_COL_MIN_displays_normal_morphology_and_correct_localization_of_PBP1_and_PBP2_/1408147", "title"=>"<i>S</i>. <i>aureus</i> strain COL MIN displays normal morphology and correct localization of PBP1 and PBP2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-07 03:33:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2059443"], "description"=>"<p><b>(A, B)</b> Estimated survival curves for wild type (WT) and PGRP-SA mutant (<i>seml</i>) flies infected with COL and COL MIN <i>S</i>. <i>aureus</i> strains or PBS (to monitor the physical effects of the injection <i>per se</i>). WT flies strongly succumbed to infection with COL by 96 hours whereas 88% of WT flies infected with COL MIN survived. Curves were statistically separable, log-rank test P<0.05. At least 90% of the PGRP-SA-deficient flies were killed by WT bacteria (within 60 hours) and by COL MIN mutant strain (within 96 hours). Curves were statistically separable, log-rank test P<0.05. (<b>C)</b> Bacterial cell lysis monitored through the decrease of OD<sub>600</sub> was determined for COL and COL MIN strains in the presence (+) or absence (-) of lysozyme (300 μg/ml). The minimal strain showed increased cell lysis in the presence of lysozyme. Data shows mean with 95% confidence intervals of three independent biological repeats.</p>", "links"=>[], "tags"=>["Minimal Peptidoglycan Synthesis Machine", "PG synthesis machinery", "PG biosynthesis", "PBP 1", "Cell Morphology", "genes encoding PG synthesis enzymes", "synthesis machine", "Sacrifices Virulence", "host lytic enzymes", "Antibiotic resistance", "PG synthesizing enzymes", "aureus genome", "peptidoglycan receptor proteins", "protein composition", "Staphylococcus aureus Survives", "PG synthesis machine", "Staphylococcus aureus", "cell wall", "Drosophila infection model", "PG synthesis enzymes", "Model organisms", "genome encodes"], "article_id"=>1408149, "categories"=>["Biological Sciences"], "users"=>["Patricia Reed", "Magda L. Atilano", "Renato Alves", "Egbert Hoiczyk", "Xinwei Sher", "Nathalie T. Reichmann", "Pedro M. Pereira", "Terry Roemer", "Sergio R. Filipe", "José B. Pereira-Leal", "Petros Ligoxygakis", "Mariana G. Pinho"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004891.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_S_aureus_COL_MIN_showed_attenuated_virulence_in_a_Drosophila_infection_model_and_increased_susceptibility_to_lysozyme_/1408149", "title"=>"<i>S</i>. <i>aureus</i> COL MIN showed attenuated virulence in a <i>Drosophila</i> infection model and increased susceptibility to lysozyme.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-05-07 03:33:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2059444"], "description"=>"<p>* preferential target of antibiotic shown in parenthesis</p><p>MICs of antibiotics for parental and mutant strains.</p>", "links"=>[], "tags"=>["Minimal Peptidoglycan Synthesis Machine", "PG synthesis machinery", "PG biosynthesis", "PBP 1", "Cell Morphology", "genes encoding PG synthesis enzymes", "synthesis machine", "Sacrifices Virulence", "host lytic enzymes", "Antibiotic resistance", "PG synthesizing enzymes", "aureus genome", "peptidoglycan receptor proteins", "protein composition", "Staphylococcus aureus Survives", "PG synthesis machine", "Staphylococcus aureus", "cell wall", "Drosophila infection model", "PG synthesis enzymes", "Model organisms", "genome encodes"], "article_id"=>1408150, "categories"=>["Biological Sciences"], "users"=>["Patricia Reed", "Magda L. Atilano", "Renato Alves", "Egbert Hoiczyk", "Xinwei Sher", "Nathalie T. Reichmann", "Pedro M. Pereira", "Terry Roemer", "Sergio R. Filipe", "José B. Pereira-Leal", "Petros Ligoxygakis", "Mariana G. Pinho"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004891.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MICs_of_antibiotics_for_parental_and_mutant_strains_/1408150", "title"=>"MICs of antibiotics for parental and mutant strains.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-05-07 03:33:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/2059460", "https://ndownloader.figshare.com/files/2059461", "https://ndownloader.figshare.com/files/2059462", "https://ndownloader.figshare.com/files/2059463", "https://ndownloader.figshare.com/files/2059464", "https://ndownloader.figshare.com/files/2059465", "https://ndownloader.figshare.com/files/2059466", "https://ndownloader.figshare.com/files/2059467"], "description"=>"<div><p>Many important cellular processes are performed by molecular machines, composed of multiple proteins that physically interact to execute biological functions. An example is the bacterial peptidoglycan (PG) synthesis machine, responsible for the synthesis of the main component of the cell wall and the target of many contemporary antibiotics. One approach for the identification of essential components of a cellular machine involves the determination of its minimal protein composition. <i>Staphylococcus aureus</i> is a Gram-positive pathogen, renowned for its resistance to many commonly used antibiotics and prevalence in hospitals. Its genome encodes a low number of proteins with PG synthesis activity (9 proteins), when compared to other model organisms, and is therefore a good model for the study of a minimal PG synthesis machine. We deleted seven of the nine genes encoding PG synthesis enzymes from the <i>S</i>. <i>aureus</i> genome without affecting normal growth or cell morphology, generating a strain capable of PG biosynthesis catalyzed only by two penicillin-binding proteins, PBP1 and the bi-functional PBP2. However, multiple PBPs are important in clinically relevant environments, as bacteria with a minimal PG synthesis machinery became highly susceptible to cell wall-targeting antibiotics, host lytic enzymes and displayed impaired virulence in a <i>Drosophila</i> infection model which is dependent on the presence of specific peptidoglycan receptor proteins, namely PGRP-SA. The fact that <i>S</i>. <i>aureus</i> can grow and divide with only two active PG synthesizing enzymes shows that most of these enzymes are redundant <i>in vitro</i> and identifies the minimal PG synthesis machinery of <i>S</i>. <i>aureus</i>. However a complex molecular machine is important in environments other than <i>in vitro</i> growth as the expendable PG synthesis enzymes play an important role in the pathogenicity and antibiotic resistance of <i>S</i>. <i>aureus</i>.</p></div>", "links"=>[], "tags"=>["Minimal Peptidoglycan Synthesis Machine", "PG synthesis machinery", "PG biosynthesis", "PBP 1", "Cell Morphology", "genes encoding PG synthesis enzymes", "synthesis machine", "Sacrifices Virulence", "host lytic enzymes", "Antibiotic resistance", "PG synthesizing enzymes", "aureus genome", "peptidoglycan receptor proteins", "protein composition", "Staphylococcus aureus Survives", "PG synthesis machine", "Staphylococcus aureus", "cell wall", "Drosophila infection model", "PG synthesis enzymes", "Model organisms", "genome encodes"], "article_id"=>1408157, "categories"=>["Biological Sciences"], "users"=>["Patricia Reed", "Magda L. Atilano", "Renato Alves", "Egbert Hoiczyk", "Xinwei Sher", "Nathalie T. Reichmann", "Pedro M. Pereira", "Terry Roemer", "Sergio R. Filipe", "José B. Pereira-Leal", "Petros Ligoxygakis", "Mariana G. Pinho"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004891.s001", "https://dx.doi.org/10.1371/journal.ppat.1004891.s002", "https://dx.doi.org/10.1371/journal.ppat.1004891.s003", "https://dx.doi.org/10.1371/journal.ppat.1004891.s004", "https://dx.doi.org/10.1371/journal.ppat.1004891.s005", "https://dx.doi.org/10.1371/journal.ppat.1004891.s006", "https://dx.doi.org/10.1371/journal.ppat.1004891.s007", "https://dx.doi.org/10.1371/journal.ppat.1004891.s008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Staphylococcus_aureus_Survives_with_a_Minimal_Peptidoglycan_Synthesis_Machine_but_Sacrifices_Virulence_and_Antibiotic_Resistance/1408157", "title"=>"<i>Staphylococcus aureus</i> Survives with a Minimal Peptidoglycan Synthesis Machine but Sacrifices Virulence and Antibiotic Resistance", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-05-07 03:33:15"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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