A Single Streptomyces Symbiont Makes Multiple Antifungals to Support the Fungus Farming Ant Acromyrmex octospinosus
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{"title"=>"A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant acromyrmex octospinosus", "type"=>"journal", "authors"=>[{"first_name"=>"Ryan F.", "last_name"=>"Seipke", "scopus_author_id"=>"23989747600"}, {"first_name"=>"Jörg", "last_name"=>"Barke", "scopus_author_id"=>"36499205400"}, {"first_name"=>"Charles", "last_name"=>"Brearley", "scopus_author_id"=>"7004325474"}, {"first_name"=>"Lionel", "last_name"=>"Hill", "scopus_author_id"=>"7202617426"}, {"first_name"=>"Douglas W.", "last_name"=>"Yu", "scopus_author_id"=>"7404666206"}, {"first_name"=>"Rebecca J M", "last_name"=>"Goss", "scopus_author_id"=>"35409325500"}, {"first_name"=>"Matthew I.", "last_name"=>"Hutchings", "scopus_author_id"=>"7101756728"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"21857911", "doi"=>"10.1371/journal.pone.0022028", "sgr"=>"79961040245", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-79961040245", "issn"=>"19326203", "pui"=>"362270491"}, "id"=>"1cf30f34-d000-3ed9-bb82-7f8f69efd446", "abstract"=>"Attine ants are dependent on a cultivated fungus for food and use antibiotics produced by symbiotic Actinobacteria as weedkillers in their fungus gardens. Actinobacterial species belonging to the genera Pseudonocardia, Streptomyces and Amycolatopsis have been isolated from attine ant nests and shown to confer protection against a range of microfungal weeds. In previous work on the higher attine Acromyrmex octospinosus we isolated a Streptomyces strain that produces candicidin, consistent with another report that attine ants use Streptomyces-produced candicidin in their fungiculture. Here we report the genome analysis of this Streptomyces strain and identify multiple antibiotic biosynthetic pathways. We demonstrate, using gene disruptions and mass spectrometry, that this single strain has the capacity to make candicidin and multiple antimycin compounds. Although antimycins have been known for >60 years we report the sequence of the biosynthetic gene cluster for the first time. Crucially, disrupting the candicidin and antimycin gene clusters in the same strain had no effect on bioactivity against a co-evolved nest pathogen called Escovopsis that has been identified in ∼30% of attine ant nests. Since the Streptomyces strain has strong bioactivity against Escovopsis we conclude that it must make additional antifungal(s) to inhibit Escovopsis. However, candicidin and antimycins likely offer protection against other microfungal weeds that infect the attine fungal gardens. Thus, we propose that the selection of this biosynthetically prolific strain from the natural environment provides A. octospinosus with broad spectrum activity against Escovopsis and other microfungal weeds.", "link"=>"http://www.mendeley.com/research/single-streptomyces-symbiont-makes-multiple-antifungals-support-fungus-farming-ant-acromyrmex-octosp", "reader_count"=>92, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>9, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>4, "Student > Master"=>11, "Other"=>2, "Student > Bachelor"=>18, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>9, "Researcher"=>14, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>4, "Student > Master"=>11, "Other"=>2, "Student > Bachelor"=>18, "Lecturer"=>2, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Engineering"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>60, "Medicine and Dentistry"=>1, "Chemistry"=>10, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>10}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>60}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>7}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>4, "Panama"=>1, "Denmark"=>3, "United Kingdom"=>1, "India"=>1, "Spain"=>1}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/749221"], "description"=>"<p>The percent amino acid homology shared between S4 proteins and proteins in <i>S. albus</i> and <i>S. ambofaciens</i> is indicated in the shaded boxes. The draft genomic sequence of <i>S. albus</i> is incomplete and the sequence for the putative antimycin biosynthetic gene cluster is split over contig 11 and contig 12 with an estimated gap of ∼820 bp in the <i>antC</i> gene. The <i>Streptomyces</i> S4 antimycin biosynthetic gene cluster is located on scaffold06 at coordinates 81953–106578. The partial genome sequences of <i>Streptomyces</i> S4, <i>S. albus</i> J1074, and <i>S. ambofaciens</i> ATCC 23877 are available under accession numbers CADY00000000, ABYC00000000 and AM238663, respectively. The gene names for <i>S. albus</i> have been shortened to eliminate the first nine numbers of the gene name (e.g. SalbJ_290 = SalbJ_010100000290).</p>", "links"=>[], "tags"=>["schematic", "s4", "antimycin", "biosynthetic", "putative", "clusters"], "article_id"=>419584, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.g004", "stats"=>{"downloads"=>2, "page_views"=>42, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Gene_schematic_of_the_Streptomyces_S4_antimycin_biosynthetic_gene_cluster_and_comparison_to_putative_antimycin_clusters_in_Streptomyces_albus_and_Streptomyces_ambofaciens_/419584", "title"=>"Gene schematic of the <i>Streptomyces</i> S4 antimycin biosynthetic gene cluster and comparison to putative antimycin clusters in <i>Streptomyces albus</i> and <i>Streptomyces ambofaciens</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-03 02:39:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/749350"], "description"=>"<p>Amp<sup>R</sup>, ampicillin resistance, Apr<sup>R</sup>, apramycin resistance, Hyg<sup>R</sup>, hygromycin resistance, Kan<sup>R</sup>, kanamycin resistance, <i>oriT</i>, origin of transfer.</p>", "links"=>[], "tags"=>["plasmids"], "article_id"=>419720, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.t003", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Strains_and_plasmids_used_in_this_study_/419720", "title"=>"Strains and plasmids used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-03 02:42:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/748987"], "description"=>"<p>Bioassays with <i>Streptomyces lividans</i>, S4 wild-type, S4 Δ<i>fscC</i>, S4 Δ<i>antC</i> and S4 Δ<i>fscC</i> Δ<i>antC</i> against <i>Escovopsis weberi</i> (top panel) and <i>C. albicans</i> (bottom panel) demonstrate that deletion of <i>fscC</i> does not abolish antifungal activity and that deletion of <i>antC</i> only reduces antifungal activity against <i>C. albicans</i> and not <i>E. weberi</i>. The S4 Δ<i>fscC</i> Δ<i>antC</i> double mutant does not display reduced antifungal activity against <i>E. weberi</i> suggesting the presence of an additional antifungal compound that is responsible for the phenotype observed during in vitro bioassays.</p>", "links"=>[], "tags"=>["bioactivity", "non-antifungal-producing", "s4", "wild-type", "mutant"], "article_id"=>419348, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.g002", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Antifungal_bioactivity_of_the_non_antifungal_producing_strain_Streptomyces_lividans_Streptomyces_S4_wild_type_and_mutant_strains_/419348", "title"=>"Antifungal bioactivity of the non-antifungal-producing strain <i>Streptomyces lividans</i>, <i>Streptomyces</i> S4 wild-type and mutant strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-03 02:35:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/749384"], "description"=>"<p>NRPS, non-ribosomal peptide synthetase, PKS, polyketide synthase.</p>", "links"=>[], "tags"=>["metabolites", "encoded"], "article_id"=>419754, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.t001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Putative_secondary_metabolites_encoded_by_Streptomyces_S4_/419754", "title"=>"Putative secondary metabolites encoded by <i>Streptomyces</i> S4.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-03 02:42:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/748856"], "description"=>"<p>LC-MS was used to analyze supernatant from <i>Streptomyces</i> S4 wild-type and S4 Δ<i>fscC</i>. The extracted ion chromatogram for candicidin (<i>m/z</i> 1109.6) is shown and confirmed that only S4 wild-type and not the Δ<i>fscC</i> mutant produced candicidin. The UV visible spectra for the peak at RT 5.15 min displays absorption characteristics consistent with polyene compounds is also shown (bottom).</p>", "links"=>[], "tags"=>["candicidin", "biosynthetic", "abolishes"], "article_id"=>419223, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.g001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletion_of_the_candicidin_biosynthetic_gene_fscC_abolishes_production_of_candicidin_/419223", "title"=>"Deletion of the candicidin biosynthetic gene, <i>fscC</i> abolishes production of candicidin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-03 02:33:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/749114"], "description"=>"<p>The extracted ion chromatograms for antimcyins A1–A4 are shown. Eight compounds consistent with the mass of antimycin A1–A4 were produced by S4 wild-type and S4 Δ<i>fscC</i>, but were not produced by the Δ<i>antC</i> mutant. Co-injection of antimycin A1–A4 with the S4 wild-type extract demonstrated that antimycin A1–A4 have the same retention time as four of the eight compounds produced by S4 wild-type. The UV visible spectra and ESI positive mode mass spectra for antimycin A1–A4 and the eight antimycin compounds produced by S4 wild-type are shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022028#pone.0022028.s001\" target=\"_blank\">Fig. S1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0022028#pone.0022028.s002\" target=\"_blank\">Fig. S2</a>, respectively. Antimycin A1: R<sub>1</sub> = CH(CH<sub>3</sub>)CH<sub>2</sub>CH<sub>3</sub>, R<sub>2</sub> = (CH<sub>2</sub>)<sub>5</sub>CH<sub>3</sub>. Antimycin A2: R<sub>1</sub> = CH(CH<sub>3</sub>)<sub>2</sub>, R<sub>2</sub> = (CH<sub>2</sub>)<sub>5</sub>CH<sub>3</sub>. Antimycin A3: R<sub>1</sub> = CH(CH<sub>3</sub>)CH<sub>2</sub>CH<sub>3</sub>, R<sub>2</sub> = (CH<sub>2</sub>)<sub>3</sub>CH<sub>3</sub>. Antimycin A4: R1 = CH(CH<sub>3</sub>)<sub>2</sub> R<sub>2</sub> = (CH<sub>2</sub>)<sub>3</sub>CH<sub>3</sub>.</p>", "links"=>[], "tags"=>["s4", "wild-type", "mutant", "strains", "compared", "antimycin"], "article_id"=>419480, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.g003", "stats"=>{"downloads"=>2, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_LC_MS_analysis_of_Streptomyces_S4_wild_type_and_mutant_strains_compared_to_antimycin_standards_/419480", "title"=>"LC/MS analysis of <i>Streptomyces</i> S4 wild-type and mutant strains compared to antimycin standards.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-08-03 02:38:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/377439", "https://ndownloader.figshare.com/files/377507", "https://ndownloader.figshare.com/files/377554"], "description"=>"<div><p>Attine ants are dependent on a cultivated fungus for food and use antibiotics produced by symbiotic Actinobacteria as weedkillers in their fungus gardens. Actinobacterial species belonging to the genera <em>Pseudonocardia, Streptomyces</em> and <em>Amycolatopsis</em> have been isolated from attine ant nests and shown to confer protection against a range of microfungal weeds. In previous work on the higher attine <em>Acromyrmex octospinosus</em> we isolated a <em>Streptomyces</em> strain that produces candicidin, consistent with another report that attine ants use <em>Streptomyces</em>-produced candicidin in their fungiculture. Here we report the genome analysis of this <em>Streptomyces</em> strain and identify multiple antibiotic biosynthetic pathways. We demonstrate, using gene disruptions and mass spectrometry, that this single strain has the capacity to make candicidin and multiple antimycin compounds. Although antimycins have been known for >60 years we report the sequence of the biosynthetic gene cluster for the first time. Crucially, disrupting the candicidin and antimycin gene clusters in the same strain had no effect on bioactivity against a co-evolved nest pathogen called <em>Escovopsis</em> that has been identified in ∼30% of attine ant nests. Since the <em>Streptomyces</em> strain has strong bioactivity against <em>Escovopsis</em> we conclude that it must make additional antifungal(s) to inhibit <em>Escovopsis</em>. However, candicidin and antimycins likely offer protection against other microfungal weeds that infect the attine fungal gardens. Thus, we propose that the selection of this biosynthetically prolific strain from the natural environment provides <em>A. octospinosus</em> with broad spectrum activity against <em>Escovopsis</em> and other microfungal weeds.</p> </div>", "links"=>[], "tags"=>["symbiont", "makes", "antifungals", "fungus", "farming", "ant"], "article_id"=>134582, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0022028.s001", "https://dx.doi.org/10.1371/journal.pone.0022028.s002", "https://dx.doi.org/10.1371/journal.pone.0022028.s003"], "stats"=>{"downloads"=>12, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Single_Streptomyces_Symbiont_Makes_Multiple_Antifungals_to_Support_the_Fungus_Farming_Ant_Acromyrmex_octospinosus_/134582", "title"=>"A Single <em>Streptomyces</em> Symbiont Makes Multiple Antifungals to Support the Fungus Farming Ant <em>Acromyrmex octospinosus</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-08-03 01:16:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/749317"], "description"=>"<p>Proposed functions of proteins encoded by the antimycin biosynthetic gene cluster.</p>", "links"=>[], "tags"=>["functions", "proteins", "encoded", "antimycin", "biosynthetic"], "article_id"=>419681, "categories"=>["Ecology", "Genetics", "Microbiology"], "users"=>["Ryan F. Seipke", "Jörg Barke", "Charles Brearley", "Lionel Hill", "Douglas W. Yu", "Rebecca J. M. Goss", "Matthew I. Hutchings"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0022028.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_functions_of_proteins_encoded_by_the_antimycin_biosynthetic_gene_cluster_/419681", "title"=>"Proposed functions of proteins encoded by the antimycin biosynthetic gene cluster.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-08-03 02:41:21"}

PMC Usage Stats | Further Information

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Relative Metric

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