Genome-Based Discovery of a Novel Membrane-Bound 1,6-Dihydroxyphenazine Prenyltransferase from a Marine Actinomycete
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{"title"=>"Genome-based discovery of a novel membrane-bound 1,6-dihydroxyphenazine prenyltransferase from a marine actinomycete", "type"=>"journal", "authors"=>[{"first_name"=>"Philipp", "last_name"=>"Zeyhle", "scopus_author_id"=>"56205327700"}, {"first_name"=>"Judith S.", "last_name"=>"Bauer", "scopus_author_id"=>"47660963100"}, {"first_name"=>"J??rn", "last_name"=>"Kalinowski", "scopus_author_id"=>"7101959761"}, {"first_name"=>"Kazuo", "last_name"=>"Shin-ya", "scopus_author_id"=>"7005327343"}, {"first_name"=>"Harald", "last_name"=>"Gross", "scopus_author_id"=>"9044866400"}, {"first_name"=>"Lutz", "last_name"=>"Heide", "scopus_author_id"=>"7005463910"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"373323735", "isbn"=>"1932-6203", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0099122", "sgr"=>"84902532344", "scopus"=>"2-s2.0-84902532344", "pmid"=>"24892559"}, "id"=>"fef92889-dc57-354b-8822-4235439b7487", "abstract"=>"Recently, novel prenylated derivatives of 1,6-dihydroxyphenazine have been isolated from the marine sponge-associated Streptomyces sp. SpC080624SC-11. Genome sequencing of this strain now revealed a gene cluster containing all genes necessary for the synthesis of the phenazine and the isoprenoid moieties. Unexpectedly, however, the cluster did not contain a gene with similarity to previously investigated phenazine prenyltransferases, but instead a gene with modest similarity to the membrane-bound prenyltransferases of ubiquinone and menaquinone biosynthesis. Expression of this gene in E. coli and isolation of the membrane fraction proved that the encoded enzyme, Mpz10, catalyzes two successive prenylations of 1,6-dihydroxyphenazine. Mpz10 is the first example of a membrane-bound enzyme catalyzing the prenylation of a phenazine substrate, and one of few examples of membrane-bound enzymes involved in the prenylation of aromatic secondary metabolites in microorganisms.", "link"=>"http://www.mendeley.com/research/genomebased-discovery-novel-membranebound-16dihydroxyphenazine-prenyltransferase-marine-actinomycete", "reader_count"=>22, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>4, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>6, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>4, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>5, "Student > Postgraduate"=>1, "Student > Master"=>6, "Student > Bachelor"=>2, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>17, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Philippines"=>1, "Mexico"=>1, "United Kingdom"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1519097"], "description"=>"<p>(A) and (B): Incubations containing 1,6-dihydroxyphenazine, dimethylallyl diphosphate (DMAPP), and Mg<sup>2+</sup> with the membrane fractions of <i>E. coli</i> harboring either the empty vector pET-28a(+) (A) or the Mpz10 expression vector pPH23 (B). (C) Authentic DHDMP (structure see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone-0099122-g002\" target=\"_blank\">Figure 2B</a>). (D) and (E): Authentic JBIR-47 and JBIR-46 (structures see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone-0099122-g001\" target=\"_blank\">Figure 1B</a>). (F) Incubation containing 1-hydroxyphenazine, DMAPP, and Mg<sup>2+</sup> with the membrane fraction of <i>E. coli</i> harboring the Mpz10 expression vector pPH23 (for the structure of <b>3</b> see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone-0099122-g005\" target=\"_blank\">Figure 5</a>). Mass spectra of the three enzymatic products are shown on the right. Detection: A-E, UV 275 nm; F, UV 368 nm.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "lc-ms"], "article_id"=>1044525, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.g003", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HPLC_and_LC_MS_analysis_of_the_reaction_products_of_Mpz10_/1044525", "title"=>"HPLC and LC-MS analysis of the reaction products of Mpz10.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519096"], "description"=>"<p>(A) Putative biosynthetic gene cluster of JBIR-46, -47, and -48. (B) Proposed pathway for the biosynthesis of JBIR-46, -47, and -48. See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone-0099122-t001\" target=\"_blank\">Table 1</a> for additional information on the genes contained in the depicted gene cluster.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation"], "article_id"=>1044524, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.g002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phenazine_biosynthesis_in_Streptomyces_sp_SpC080624SC_11_/1044524", "title"=>"Phenazine biosynthesis in <i>Streptomyces</i> sp. SpC080624SC-11.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519101"], "description"=>"<p>NMR spectra were recorded in acetone-<i>d</i><sub>6</sub> (<i>δ</i> in ppm, <i>J</i> in Hz). The corresponding <sup>13</sup>C and <sup>1</sup>H NMR spectra are depicted in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone.0099122.s001\" target=\"_blank\">Figure S1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone.0099122.s002\" target=\"_blank\">Figure S2</a>, respectively.</p>a<p>Recorded at 400 MHz. <sup>b</sup>Measured values were in good agreement with published NMR data for 1-hydroxy- or 1-methoxy-phenazine <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone.0099122-Breitmaier1\" target=\"_blank\">[20]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#pone.0099122-Rmer1\" target=\"_blank\">[52]</a>. <sup>c</sup>Recorded at 101 MHz. <sup>d</sup>Multiplicity determined by a multiplicity edited <sup>1</sup>H-<sup>13</sup>C HSQC NMR experiment. <sup>e</sup>Recorded at 600 MHz. <sup>f</sup>Recorded at 151 MHz. <sup>g</sup>Protons showing long-range correlation with indicated carbon. <sup>h,i,j</sup>Assignments interchangeable.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "spectroscopic", "1-hydroxyphenazine", "enzymatic"], "article_id"=>1044529, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.t003", "stats"=>{"downloads"=>2, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_NMR_spectroscopic_data_for_1_hydroxyphenazine_and_the_enzymatic_product_3_structure_see_Figure_5_/1044529", "title"=>"NMR spectroscopic data for 1-hydroxyphenazine and the enzymatic product 3 (structure see Figure 5).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519099"], "description"=>"<p>Bold lines indicate key <sup>1</sup>H-<sup>1</sup>H COSY and arrows key <sup>1</sup>H-<sup>13</sup>C HMBC correlations.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "enzymatic", "1-hydroxy-4-dimethylallyl-phenazine"], "article_id"=>1044527, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.g005", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_of_the_enzymatic_product_1_hydroxy_4_dimethylallyl_phenazine_3_/1044527", "title"=>"Structure of the enzymatic product 1-hydroxy-4-dimethylallyl-phenazine (3).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519100"], "description"=>"<p>Genes in the putative biosynthetic gene cluster for JBIR-46, -47, and -48.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "putative", "biosynthetic"], "article_id"=>1044528, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.t001", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_in_the_putative_biosynthetic_gene_cluster_for_JBIR_46_47_and_48_/1044528", "title"=>"Genes in the putative biosynthetic gene cluster for JBIR-46, -47, and -48.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519098"], "description"=>"<p>(A) HPLC analysis of the time-dependent formation of products <b>1</b> and <b>2</b>. Detection: UV, 275 nm. (B) and (C): Product formation at different concentrations of 1,6-dihydroxyphenazine and dimethylallyl diphosphate (DMAPP). In the experiments shown in (B), DMAPP was kept constant at 0.5 mM. In the experiments shown in (C), 1,6-dihydroxyphenazine was kept constant at 0.2 mM. <i>K</i><sub>m</sub> values were determined by nonlinear regression, using GraphPad Prism software. Data represent mean ± SD of triplicate determinations.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "mpz10"], "article_id"=>1044526, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Biochemical_investigation_of_the_Mpz10_reaction_/1044526", "title"=>"Biochemical investigation of the Mpz10 reaction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519095"], "description"=>"<p>(A) Reaction catalyzed by the previously discovered prenyltransferases PpzP and EpzP. (B) Structures of the phenazines JBIR-46, -47, and -48 from <i>Streptomyces</i> sp. SpC080624SC-11.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation"], "article_id"=>1044523, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.g001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Prenylation_in_the_biosynthesis_of_phenazines_/1044523", "title"=>"Prenylation in the biosynthesis of phenazines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519103", "https://ndownloader.figshare.com/files/1519104"], "description"=>"<div><p>Recently, novel prenylated derivatives of 1,6-dihydroxyphenazine have been isolated from the marine sponge-associated <i>Streptomyces</i> sp. SpC080624SC-11. Genome sequencing of this strain now revealed a gene cluster containing all genes necessary for the synthesis of the phenazine and the isoprenoid moieties. Unexpectedly, however, the cluster did not contain a gene with similarity to previously investigated phenazine prenyltransferases, but instead a gene with modest similarity to the membrane-bound prenyltransferases of ubiquinone and menaquinone biosynthesis. Expression of this gene in <i>E. coli</i> and isolation of the membrane fraction proved that the encoded enzyme, Mpz10, catalyzes two successive prenylations of 1,6-dihydroxyphenazine. Mpz10 is the first example of a membrane-bound enzyme catalyzing the prenylation of a phenazine substrate, and one of few examples of membrane-bound enzymes involved in the prenylation of aromatic secondary metabolites in microorganisms.</p></div>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "membrane-bound", "prenyltransferase"], "article_id"=>1044531, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0099122.s001", "https://dx.doi.org/10.1371/journal.pone.0099122.s002"], "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genome_Based_Discovery_of_a_Novel_Membrane_Bound_1_6_Dihydroxyphenazine_Prenyltransferase_from_a_Marine_Actinomycete_/1044531", "title"=>"Genome-Based Discovery of a Novel Membrane-Bound 1,6-Dihydroxyphenazine Prenyltransferase from a Marine Actinomycete", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-06-03 03:16:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/1519102"], "description"=>"<p>Comparison of the prenyltransferase activity of different cell fractions. Activity was tested with 1,6-dihydroxyphenazine, DMAPP, and Mg<sup>2+</sup> as described in the <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0099122#s4\" target=\"_blank\">Experimental Procedures</a>. The membrane fraction was obtained by centrifugation at 100,000×<i>g</i>.</p>", "links"=>[], "tags"=>["Biochemistry", "lipids", "isoprenoids", "metabolism", "Secondary metabolism", "biosynthesis", "enzymology", "microbiology", "bacteriology", "Bacterial biochemistry", "Medical microbiology", "Microbial pathogens", "Fungal pathogens", "streptomyces", "molecular biology", "Molecular biology techniques", "Sequencing techniques", "Genome sequencing", "chemistry", "Chemical reactions", "prenylation", "mpz10", "membrane"], "article_id"=>1044530, "categories"=>["Biological Sciences"], "users"=>["Philipp Zeyhle", "Judith S. Bauer", "Jörn Kalinowski", "Kazuo Shin-ya", "Harald Gross", "Lutz Heide"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0099122.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Localization_of_the_Mpz10_activity_in_the_membrane_fraction_/1044530", "title"=>"Localization of the Mpz10 activity in the membrane fraction.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-06-03 03:16:43"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}

Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences", "average_usage"=>[291]}, {"subject_area"=>"/Biology and life sciences/Microbiology", "average_usage"=>[317]}, {"subject_area"=>"/Biology and life sciences/Mycology", "average_usage"=>[348, 543]}, {"subject_area"=>"/Medicine and health sciences", "average_usage"=>[285]}]}
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