Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2012-06-25

AUTHORS

Dapeng Zhang, Robson F de Souza, Vivek Anantharaman, Lakshminarayan M Iyer, L Aravind

ABSTRACT

BACKGROUND: Proteinaceous toxins are observed across all levels of inter-organismal and intra-genomic conflicts. These include recently discovered prokaryotic polymorphic toxin systems implicated in intra-specific conflicts. They are characterized by a remarkable diversity of C-terminal toxin domains generated by recombination with standalone toxin-coding cassettes. Prior analysis revealed a striking diversity of nuclease and deaminase domains among the toxin modules. We systematically investigated polymorphic toxin systems using comparative genomics, sequence and structure analysis. RESULTS: Polymorphic toxin systems are distributed across all major bacterial lineages and are delivered by at least eight distinct secretory systems. In addition to type-II, these include type-V, VI, VII (ESX), and the poorly characterized "Photorhabdus virulence cassettes (PVC)", PrsW-dependent and MuF phage-capsid-like systems. We present evidence that trafficking of these toxins is often accompanied by autoproteolytic processing catalyzed by HINT, ZU5, PrsW, caspase-like, papain-like, and a novel metallopeptidase associated with the PVC system. We identified over 150 distinct toxin domains in these systems. These span an extraordinary catalytic spectrum to include 23 distinct clades of peptidases, numerous previously unrecognized versions of nucleases and deaminases, ADP-ribosyltransferases, ADP ribosyl cyclases, RelA/SpoT-like nucleotidyltransferases, glycosyltranferases and other enzymes predicted to modify lipids and carbohydrates, and a pore-forming toxin domain. Several of these toxin domains are shared with host-directed effectors of pathogenic bacteria. Over 90 families of immunity proteins might neutralize anywhere between a single to at least 27 distinct types of toxin domains. In some organisms multiple tandem immunity genes or immunity protein domains are organized into polyimmunity loci or polyimmunity proteins. Gene-neighborhood-analysis of polymorphic toxin systems predicts the presence of novel trafficking-related components, and also the organizational logic that allows toxin diversification through recombination. Domain architecture and protein-length analysis revealed that these toxins might be deployed as secreted factors, through directed injection, or via inter-cellular contact facilitated by filamentous structures formed by RHS/YD, filamentous hemagglutinin and other repeats. Phyletic pattern and life-style analysis indicate that polymorphic toxins and polyimmunity loci participate in cooperative behavior and facultative 'cheating' in several ecosystems such as the human oral cavity and soil. Multiple domains from these systems have also been repeatedly transferred to eukaryotes and their viruses, such as the nucleo-cytoplasmic large DNA viruses. CONCLUSIONS: Along with a comprehensive inventory of toxins and immunity proteins, we present several testable predictions regarding active sites and catalytic mechanisms of toxins, their processing and trafficking and their role in intra-specific and inter-specific interactions between bacteria. These systems provide insights regarding the emergence of key systems at different points in eukaryotic evolution, such as ADP ribosylation, interaction of myosin VI with cargo proteins, mediation of apoptosis, hyphal heteroincompatibility, hedgehog signaling, arthropod toxins, cell-cell interaction molecules like teneurins and different signaling messengers. More... »

PAGES

18-18

References to SciGraph publications

  • 2010-01. An overview on nucleases (DNase, RNase, and phosphodiesterase) in snake venoms in BIOCHEMISTRY (MOSCOW)
  • 2009-12-07. Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement in BMC GENOMICS
  • 2010-01. Twenty years hunting for sulfur in DNA in PROTEIN & CELL
  • 2003-11-26. New connections in the prokaryotic toxin-antitoxin network: relationship with the eukaryotic nonsense-mediated RNA decay system in GENOME BIOLOGY
  • 2003-02-03. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes in GENOME BIOLOGY
  • 2001-10. Genotype versus phenotype: conflicting results in mapping a lung tumor susceptibility locus to the G7c recombination interval in the mouse MHC class III region in IMMUNOGENETICS
  • 2009-06-21. Structure of a lamprey variable lymphocyte receptor in complex with a protein antigen in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 2009-01-20. Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti in BMC GENOMICS
  • 2008-06-17. The AID/APOBEC family of nucleic acid mutators in GENOME BIOLOGY
  • 2001-02. G7c in the lung tumor susceptibility (Lts) region of the Mhc class III region encodes a von Willebrand factor type A domain protein in IMMUNOGENETICS
  • 2008-10-22. Insights beyond Wolbachia–Drosophila interactions: Never completely trust a model: insights from cytoplasmic incompatibility beyond Wolbachia–Drosophila interactions in HEREDITY
  • 2011-07-20. Type VI secretion delivers bacteriolytic effectors to target cells in NATURE
  • 2010-06-20. An Rhs-like genetic element is involved in bacteriocin production by Pseudomonas savastanoi pv. savastanoi in ANTONIE VAN LEEUWENHOEK
  • 2004-07-18. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling in NATURE
  • 2012-02-26. Type VI secretion requires a dynamic contractile phage tail-like structure in NATURE
  • 1989-03. High-resolution (1.5 Å) crystal structure of phospholipase C from Bacillus cereus in NATURE
  • 2006-11. The type III secretion injectisome in NATURE REVIEWS MICROBIOLOGY
  • 2006-07-19. The prokaryotic antecedents of the ubiquitin-signaling system and the early evolution of ubiquitin-like β-grasp domains in GENOME BIOLOGY
  • 2005-10-04. In silico characterization of the family of PARP-like poly(ADP-ribosyl)transferases (pARTs) in BMC GENOMICS
  • 2011-11-18. The PIDDosome, DNA-damage-induced apoptosis and beyond in CELL DEATH & DIFFERENTIATION
  • 2002-05-01. Pore-forming toxins in CELLULAR AND MOLECULAR LIFE SCIENCES
  • 2008-03-17. MutL homologs in restriction-modification systems and the origin of eukaryotic MORC ATPases in BIOLOGY DIRECT
  • 2004-08-19. MUSCLE: a multiple sequence alignment method with reduced time and space complexity in BMC BIOINFORMATICS
  • 2000. Animal Toxins, Facts and Protocols in NONE
  • 2011. The Lysine-Specific Gingipain of Porphyromonas gingivalis in CYSTEINE PROTEASES OF PATHOGENIC ORGANISMS
  • 2010-11-17. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria in NATURE
  • 2010-09-19. Structural basis for ribosomal 16S rRNA cleavage by the cytotoxic domain of colicin E3 in NATURE STRUCTURAL & MOLECULAR BIOLOGY
  • 1997. Sequence and Structural Links between Distant ADP-Ribosyltransferase Families in ADP-RIBOSYLATION IN ANIMAL TISSUES
  • 2007-11-09. Bacterial pore-forming toxins: The (w)hole story? in CELLULAR AND MOLECULAR LIFE SCIENCES
  • 2012-04-15. A Xanthomonas uridine 5′-monophosphate transferase inhibits plant immune kinases in NATURE
  • 2011-12-15. Bacterial outer membrane evolution via sporulation? in NATURE CHEMICAL BIOLOGY
  • Identifiers

    URI

    http://scigraph.springernature.com/pub.10.1186/1745-6150-7-18

    DOI

    http://dx.doi.org/10.1186/1745-6150-7-18

    DIMENSIONS

    https://app.dimensions.ai/details/publication/pub.1040385591

    PUBMED

    https://www.ncbi.nlm.nih.gov/pubmed/22731697


    Indexing Status Check whether this publication has been indexed by Scopus and Web Of Science using the SN Indexing Status Tool
    Incoming Citations Browse incoming citations for this publication using opencitations.net

    JSON-LD is the canonical representation for SciGraph data.

    TIP: You can open this SciGraph record using an external JSON-LD service: JSON-LD Playground Google SDTT

    [
      {
        "@context": "https://springernature.github.io/scigraph/jsonld/sgcontext.json", 
        "about": [
          {
            "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/06", 
            "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
            "name": "Biological Sciences", 
            "type": "DefinedTerm"
          }, 
          {
            "id": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/0601", 
            "inDefinedTermSet": "http://purl.org/au-research/vocabulary/anzsrc-for/2008/", 
            "name": "Biochemistry and Cell Biology", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Amino Acid Sequence", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Animals", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Bacteria", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Bacterial Proteins", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Bacterial Secretion Systems", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Bacterial Toxins", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Catalytic Domain", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Ecosystem", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Endonucleases", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Evolution, Molecular", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Genetic Loci", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Genetic Variation", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Genome, Bacterial", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Genomics", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Humans", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Metalloproteases", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Protein Interaction Mapping", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Protein Structure, Tertiary", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Protein Transport", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Sequence Alignment", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Signal Transduction", 
            "type": "DefinedTerm"
          }, 
          {
            "inDefinedTermSet": "https://www.nlm.nih.gov/mesh/", 
            "name": "Symbiosis", 
            "type": "DefinedTerm"
          }
        ], 
        "author": [
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA", 
              "id": "http://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Zhang", 
            "givenName": "Dapeng", 
            "id": "sg:person.0641126326.37", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0641126326.37"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "Departamento de Microbiologia, Instituto de Ci\u00eancias Biom\u00e9dicas, Universidade de S\u00e3o Paulo, S\u00e3o Paulo, Brazil", 
              "id": "http://www.grid.ac/institutes/grid.11899.38", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA", 
                "Departamento de Microbiologia, Instituto de Ci\u00eancias Biom\u00e9dicas, Universidade de S\u00e3o Paulo, S\u00e3o Paulo, Brazil"
              ], 
              "type": "Organization"
            }, 
            "familyName": "de Souza", 
            "givenName": "Robson F", 
            "id": "sg:person.01234136303.93", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01234136303.93"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA", 
              "id": "http://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Anantharaman", 
            "givenName": "Vivek", 
            "id": "sg:person.0673016603.16", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0673016603.16"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA", 
              "id": "http://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Iyer", 
            "givenName": "Lakshminarayan M", 
            "id": "sg:person.012162224357.20", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.012162224357.20"
            ], 
            "type": "Person"
          }, 
          {
            "affiliation": {
              "alternateName": "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA", 
              "id": "http://www.grid.ac/institutes/grid.419234.9", 
              "name": [
                "National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA"
              ], 
              "type": "Organization"
            }, 
            "familyName": "Aravind", 
            "givenName": "L", 
            "id": "sg:person.01106662166.38", 
            "sameAs": [
              "https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01106662166.38"
            ], 
            "type": "Person"
          }
        ], 
        "citation": [
          {
            "id": "sg:pub.10.1038/nature09490", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1019643796", 
              "https://doi.org/10.1038/nature09490"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature02794", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1000185087", 
              "https://doi.org/10.1038/nature02794"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nrmicro1526", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1031832630", 
              "https://doi.org/10.1038/nrmicro1526"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-1-4419-8414-2_2", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1036685376", 
              "https://doi.org/10.1007/978-1-4419-8414-2_2"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1134/s0006297910010013", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1038699984", 
              "https://doi.org/10.1134/s0006297910010013"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1471-2164-6-139", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1022818110", 
              "https://doi.org/10.1186/1471-2164-6-139"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-3-0348-8466-2", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006928762", 
              "https://doi.org/10.1007/978-3-0348-8466-2"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1745-6150-3-8", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1006845773", 
              "https://doi.org/10.1186/1745-6150-3-8"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s13238-010-0009-y", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007914195", 
              "https://doi.org/10.1007/s13238-010-0009-y"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/hdy.2008.113", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015759634", 
              "https://doi.org/10.1038/hdy.2008.113"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/gb-2003-4-2-r11", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1039399488", 
              "https://doi.org/10.1186/gb-2003-4-2-r11"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nsmb.1619", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1047619820", 
              "https://doi.org/10.1038/nsmb.1619"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nsmb.1896", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1013910559", 
              "https://doi.org/10.1038/nsmb.1896"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature10244", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1002229949", 
              "https://doi.org/10.1038/nature10244"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s00018-002-8471-1", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1019930863", 
              "https://doi.org/10.1007/s00018-002-8471-1"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/gb-2006-7-7-r60", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1027241290", 
              "https://doi.org/10.1186/gb-2006-7-7-r60"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1471-2164-10-584", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1001222619", 
              "https://doi.org/10.1186/1471-2164-10-584"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/gb-2008-9-6-229", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1021664284", 
              "https://doi.org/10.1186/gb-2008-9-6-229"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s00251-001-0381-0", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1035823889", 
              "https://doi.org/10.1007/s00251-001-0381-0"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s002510100297", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1032416368", 
              "https://doi.org/10.1007/s002510100297"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/978-1-4419-8632-0_12", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1051522575", 
              "https://doi.org/10.1007/978-1-4419-8632-0_12"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/338357a0", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1007053259", 
              "https://doi.org/10.1038/338357a0"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nchembio.748", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1044207924", 
              "https://doi.org/10.1038/nchembio.748"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s00018-007-7434-y", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1031121043", 
              "https://doi.org/10.1007/s00018-007-7434-y"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1471-2164-10-33", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1011169430", 
              "https://doi.org/10.1186/1471-2164-10-33"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature10962", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1005452992", 
              "https://doi.org/10.1038/nature10962"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1007/s10482-010-9468-7", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1011482058", 
              "https://doi.org/10.1007/s10482-010-9468-7"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/1471-2105-5-113", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1040413794", 
              "https://doi.org/10.1186/1471-2105-5-113"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1186/gb-2003-4-12-r81", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1016542336", 
              "https://doi.org/10.1186/gb-2003-4-12-r81"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/nature10846", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1015413547", 
              "https://doi.org/10.1038/nature10846"
            ], 
            "type": "CreativeWork"
          }, 
          {
            "id": "sg:pub.10.1038/cdd.2011.162", 
            "sameAs": [
              "https://app.dimensions.ai/details/publication/pub.1041318416", 
              "https://doi.org/10.1038/cdd.2011.162"
            ], 
            "type": "CreativeWork"
          }
        ], 
        "datePublished": "2012-06-25", 
        "datePublishedReg": "2012-06-25", 
        "description": "BACKGROUND: Proteinaceous toxins are observed across all levels of inter-organismal and intra-genomic conflicts. These include recently discovered prokaryotic polymorphic toxin systems implicated in intra-specific conflicts. They are characterized by a remarkable diversity of C-terminal toxin domains generated by recombination with standalone toxin-coding cassettes. Prior analysis revealed a striking diversity of nuclease and deaminase domains among the toxin modules. We systematically investigated polymorphic toxin systems using comparative genomics, sequence and structure analysis.\nRESULTS: Polymorphic toxin systems are distributed across all major bacterial lineages and are delivered by at least eight distinct secretory systems. In addition to type-II, these include type-V, VI, VII (ESX), and the poorly characterized \"Photorhabdus virulence cassettes (PVC)\", PrsW-dependent and MuF phage-capsid-like systems. We present evidence that trafficking of these toxins is often accompanied by autoproteolytic processing catalyzed by HINT, ZU5, PrsW, caspase-like, papain-like, and a novel metallopeptidase associated with the PVC system. We identified over 150 distinct toxin domains in these systems. These span an extraordinary catalytic spectrum to include 23 distinct clades of peptidases, numerous previously unrecognized versions of nucleases and deaminases, ADP-ribosyltransferases, ADP ribosyl cyclases, RelA/SpoT-like nucleotidyltransferases, glycosyltranferases and other enzymes predicted to modify lipids and carbohydrates, and a pore-forming toxin domain. Several of these toxin domains are shared with host-directed effectors of pathogenic bacteria. Over 90 families of immunity proteins might neutralize anywhere between a single to at least 27 distinct types of toxin domains. In some organisms multiple tandem immunity genes or immunity protein domains are organized into polyimmunity loci or polyimmunity proteins. Gene-neighborhood-analysis of polymorphic toxin systems predicts the presence of novel trafficking-related components, and also the organizational logic that allows toxin diversification through recombination. Domain architecture and protein-length analysis revealed that these toxins might be deployed as secreted factors, through directed injection, or via inter-cellular contact facilitated by filamentous structures formed by RHS/YD, filamentous hemagglutinin and other repeats. Phyletic pattern and life-style analysis indicate that polymorphic toxins and polyimmunity loci participate in cooperative behavior and facultative 'cheating' in several ecosystems such as the human oral cavity and soil. Multiple domains from these systems have also been repeatedly transferred to eukaryotes and their viruses, such as the nucleo-cytoplasmic large DNA viruses.\nCONCLUSIONS: Along with a comprehensive inventory of toxins and immunity proteins, we present several testable predictions regarding active sites and catalytic mechanisms of toxins, their processing and trafficking and their role in intra-specific and inter-specific interactions between bacteria. These systems provide insights regarding the emergence of key systems at different points in eukaryotic evolution, such as ADP ribosylation, interaction of myosin VI with cargo proteins, mediation of apoptosis, hyphal heteroincompatibility, hedgehog signaling, arthropod toxins, cell-cell interaction molecules like teneurins and different signaling messengers.", 
        "genre": "article", 
        "id": "sg:pub.10.1186/1745-6150-7-18", 
        "inLanguage": "en", 
        "isAccessibleForFree": true, 
        "isFundedItemOf": [
          {
            "id": "sg:grant.2726065", 
            "type": "MonetaryGrant"
          }
        ], 
        "isPartOf": [
          {
            "id": "sg:journal.1036001", 
            "issn": [
              "1745-6150"
            ], 
            "name": "Biology Direct", 
            "publisher": "Springer Nature", 
            "type": "Periodical"
          }, 
          {
            "issueNumber": "1", 
            "type": "PublicationIssue"
          }, 
          {
            "type": "PublicationVolume", 
            "volumeNumber": "7"
          }
        ], 
        "keywords": [
          "polymorphic toxin systems", 
          "Photorhabdus virulence cassettes", 
          "toxin systems", 
          "toxin domain", 
          "comparative genomics", 
          "immunity protein", 
          "nucleo-cytoplasmic large DNA viruses", 
          "major bacterial lineages", 
          "intra-genomic conflict", 
          "terminal toxin domains", 
          "large DNA viruses", 
          "cell-cell interaction molecules", 
          "inter-specific interactions", 
          "mediation of apoptosis", 
          "intra-specific conflicts", 
          "toxin diversification", 
          "eukaryotic evolution", 
          "bacterial lineages", 
          "phyletic patterns", 
          "polymorphic toxins", 
          "distinct clades", 
          "domain architecture", 
          "cargo proteins", 
          "protein domains", 
          "striking diversity", 
          "ADP-ribosyltransferases", 
          "immunity genes", 
          "remarkable diversity", 
          "myosin VI", 
          "toxin module", 
          "interaction molecules", 
          "deaminase domain", 
          "proteinaceous toxins", 
          "secretory system", 
          "autoproteolytic processing", 
          "ADP-ribosyl", 
          "loci participate", 
          "DNA viruses", 
          "ADP-ribosylation", 
          "virulence cassette", 
          "filamentous structures", 
          "catalytic mechanism", 
          "arthropod toxins", 
          "human oral cavity", 
          "protein", 
          "genomics", 
          "pathogenic bacteria", 
          "nuclease", 
          "trafficking", 
          "comprehensive inventory", 
          "active site", 
          "mechanism of action", 
          "diversity", 
          "testable predictions", 
          "cassette", 
          "bacteria", 
          "toxin", 
          "comprehensive characterization", 
          "recombination", 
          "domain", 
          "structure analysis", 
          "ZU5", 
          "eukaryotes", 
          "teneurins", 
          "clade", 
          "nucleotidyltransferases", 
          "lineages", 
          "deaminases", 
          "glycosyltranferases", 
          "genes", 
          "ecology", 
          "loci", 
          "repeats", 
          "distinct types", 
          "hedgehog", 
          "ecosystems", 
          "peptidase", 
          "effectors", 
          "messenger", 
          "metallopeptidase", 
          "diversification", 
          "cooperative behavior", 
          "ribosylation", 
          "apoptosis", 
          "enzyme", 
          "virus", 
          "mechanism", 
          "ribosyl", 
          "sequence", 
          "participates", 
          "interaction", 
          "type II", 
          "lipids", 
          "family", 
          "filamentous hemagglutinin", 
          "carbohydrates", 
          "soil", 
          "sites", 
          "evolution", 
          "molecules", 
          "prior analysis", 
          "analysis", 
          "hemagglutinin", 
          "insights", 
          "type V", 
          "like system", 
          "role", 
          "PRSW", 
          "multiple domains", 
          "characterization", 
          "immunity", 
          "patterns", 
          "emergence", 
          "life style analysis", 
          "presence", 
          "key system", 
          "evidence", 
          "components", 
          "levels", 
          "structure", 
          "addition", 
          "factors", 
          "action", 
          "YD", 
          "system", 
          "PVC system", 
          "types", 
          "processing", 
          "hints", 
          "oral cavity", 
          "cheating", 
          "contact", 
          "module", 
          "architecture", 
          "organizational logic", 
          "prediction", 
          "mediation", 
          "Single", 
          "different points", 
          "mode", 
          "cavity", 
          "behavior", 
          "conflict", 
          "spectra", 
          "Inventory", 
          "point", 
          "MUF", 
          "injection", 
          "version", 
          "logic", 
          "prokaryotic polymorphic toxin systems", 
          "standalone toxin-coding cassettes", 
          "toxin-coding cassettes", 
          "distinct secretory systems", 
          "novel metallopeptidase", 
          "distinct toxin domains", 
          "extraordinary catalytic spectrum", 
          "catalytic spectrum", 
          "unrecognized versions", 
          "RelA/SpoT-like nucleotidyltransferases", 
          "SpoT-like nucleotidyltransferases", 
          "host-directed effectors", 
          "organisms multiple tandem immunity genes", 
          "multiple tandem immunity genes", 
          "tandem immunity genes", 
          "immunity protein domains", 
          "polyimmunity loci", 
          "polyimmunity proteins", 
          "novel trafficking-related components", 
          "trafficking-related components", 
          "protein-length analysis", 
          "inter-cellular contact", 
          "RHS/YD", 
          "polyimmunity loci participate", 
          "hyphal heteroincompatibility", 
          "heteroincompatibility", 
          "different signaling messengers", 
          "signaling messengers", 
          "trafficking modes"
        ], 
        "name": "Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics", 
        "pagination": "18-18", 
        "productId": [
          {
            "name": "dimensions_id", 
            "type": "PropertyValue", 
            "value": [
              "pub.1040385591"
            ]
          }, 
          {
            "name": "doi", 
            "type": "PropertyValue", 
            "value": [
              "10.1186/1745-6150-7-18"
            ]
          }, 
          {
            "name": "pubmed_id", 
            "type": "PropertyValue", 
            "value": [
              "22731697"
            ]
          }
        ], 
        "sameAs": [
          "https://doi.org/10.1186/1745-6150-7-18", 
          "https://app.dimensions.ai/details/publication/pub.1040385591"
        ], 
        "sdDataset": "articles", 
        "sdDatePublished": "2022-01-01T18:26", 
        "sdLicense": "https://scigraph.springernature.com/explorer/license/", 
        "sdPublisher": {
          "name": "Springer Nature - SN SciGraph project", 
          "type": "Organization"
        }, 
        "sdSource": "s3://com-springernature-scigraph/baseset/20220101/entities/gbq_results/article/article_558.jsonl", 
        "type": "ScholarlyArticle", 
        "url": "https://doi.org/10.1186/1745-6150-7-18"
      }
    ]
     

    Download the RDF metadata as:  json-ld nt turtle xml License info

    HOW TO GET THIS DATA PROGRAMMATICALLY:

    JSON-LD is a popular format for linked data which is fully compatible with JSON.

    curl -H 'Accept: application/ld+json' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-7-18'

    N-Triples is a line-based linked data format ideal for batch operations.

    curl -H 'Accept: application/n-triples' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-7-18'

    Turtle is a human-readable linked data format.

    curl -H 'Accept: text/turtle' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-7-18'

    RDF/XML is a standard XML format for linked data.

    curl -H 'Accept: application/rdf+xml' 'https://scigraph.springernature.com/pub.10.1186/1745-6150-7-18'


     

    This table displays all metadata directly associated to this object as RDF triples.

    486 TRIPLES      22 PREDICATES      258 URIs      219 LITERALS      29 BLANK NODES

    Subject Predicate Object
    1 sg:pub.10.1186/1745-6150-7-18 schema:about N07e945dfad164a519aa8d7ac0121087c
    2 N0ea0a94700574a54ad12a189348e7b28
    3 N0ead513066d64b21b30b9764311de6ec
    4 N3a532cd0c90548f782624b86c9f69286
    5 N500369790dfa4fd98878c8e7e03f4810
    6 N73ab4b8150254c4789952ad8f207b5e8
    7 N75ed4703230743c190d86c94605d3b91
    8 N82ac5e63e68d49889499b1e942d116f4
    9 N834cfd50a7a9466b9020fb92fcb7a1ff
    10 N9181ab49c2674dda96e4ed6f28a1e53b
    11 N9850a84cf62c486c89cde1777c290453
    12 N999bef2bea0f4551bf3024651edd57e3
    13 Nbad78fff463d405dbfc6336fde0eb97a
    14 Nc8430f6b7f7c4b5a9ac2aa5d27f3f7e1
    15 Ncdc480cd43144d9e9e790f2b5c8be156
    16 Nce1775dfa3d64975b477977b16c53cb6
    17 Nd077dd56d85a4adf900cdbc2ebd9d811
    18 Ne7ba9f0b987f40c9ab9c46df6d601ac5
    19 Nea4adfb295b547ffa41cf4c64f88edfc
    20 Nee2c890e81144d54b9fa07c2e6a4f355
    21 Nf02851145dc748ca9a12bc3e8168a2fb
    22 Nfd925eacb1c24684b593185c5124bf64
    23 anzsrc-for:06
    24 anzsrc-for:0601
    25 schema:author N85797d6ecffb47d9a20156dbc0ddaed7
    26 schema:citation sg:pub.10.1007/978-1-4419-8414-2_2
    27 sg:pub.10.1007/978-1-4419-8632-0_12
    28 sg:pub.10.1007/978-3-0348-8466-2
    29 sg:pub.10.1007/s00018-002-8471-1
    30 sg:pub.10.1007/s00018-007-7434-y
    31 sg:pub.10.1007/s00251-001-0381-0
    32 sg:pub.10.1007/s002510100297
    33 sg:pub.10.1007/s10482-010-9468-7
    34 sg:pub.10.1007/s13238-010-0009-y
    35 sg:pub.10.1038/338357a0
    36 sg:pub.10.1038/cdd.2011.162
    37 sg:pub.10.1038/hdy.2008.113
    38 sg:pub.10.1038/nature02794
    39 sg:pub.10.1038/nature09490
    40 sg:pub.10.1038/nature10244
    41 sg:pub.10.1038/nature10846
    42 sg:pub.10.1038/nature10962
    43 sg:pub.10.1038/nchembio.748
    44 sg:pub.10.1038/nrmicro1526
    45 sg:pub.10.1038/nsmb.1619
    46 sg:pub.10.1038/nsmb.1896
    47 sg:pub.10.1134/s0006297910010013
    48 sg:pub.10.1186/1471-2105-5-113
    49 sg:pub.10.1186/1471-2164-10-33
    50 sg:pub.10.1186/1471-2164-10-584
    51 sg:pub.10.1186/1471-2164-6-139
    52 sg:pub.10.1186/1745-6150-3-8
    53 sg:pub.10.1186/gb-2003-4-12-r81
    54 sg:pub.10.1186/gb-2003-4-2-r11
    55 sg:pub.10.1186/gb-2006-7-7-r60
    56 sg:pub.10.1186/gb-2008-9-6-229
    57 schema:datePublished 2012-06-25
    58 schema:datePublishedReg 2012-06-25
    59 schema:description BACKGROUND: Proteinaceous toxins are observed across all levels of inter-organismal and intra-genomic conflicts. These include recently discovered prokaryotic polymorphic toxin systems implicated in intra-specific conflicts. They are characterized by a remarkable diversity of C-terminal toxin domains generated by recombination with standalone toxin-coding cassettes. Prior analysis revealed a striking diversity of nuclease and deaminase domains among the toxin modules. We systematically investigated polymorphic toxin systems using comparative genomics, sequence and structure analysis. RESULTS: Polymorphic toxin systems are distributed across all major bacterial lineages and are delivered by at least eight distinct secretory systems. In addition to type-II, these include type-V, VI, VII (ESX), and the poorly characterized "Photorhabdus virulence cassettes (PVC)", PrsW-dependent and MuF phage-capsid-like systems. We present evidence that trafficking of these toxins is often accompanied by autoproteolytic processing catalyzed by HINT, ZU5, PrsW, caspase-like, papain-like, and a novel metallopeptidase associated with the PVC system. We identified over 150 distinct toxin domains in these systems. These span an extraordinary catalytic spectrum to include 23 distinct clades of peptidases, numerous previously unrecognized versions of nucleases and deaminases, ADP-ribosyltransferases, ADP ribosyl cyclases, RelA/SpoT-like nucleotidyltransferases, glycosyltranferases and other enzymes predicted to modify lipids and carbohydrates, and a pore-forming toxin domain. Several of these toxin domains are shared with host-directed effectors of pathogenic bacteria. Over 90 families of immunity proteins might neutralize anywhere between a single to at least 27 distinct types of toxin domains. In some organisms multiple tandem immunity genes or immunity protein domains are organized into polyimmunity loci or polyimmunity proteins. Gene-neighborhood-analysis of polymorphic toxin systems predicts the presence of novel trafficking-related components, and also the organizational logic that allows toxin diversification through recombination. Domain architecture and protein-length analysis revealed that these toxins might be deployed as secreted factors, through directed injection, or via inter-cellular contact facilitated by filamentous structures formed by RHS/YD, filamentous hemagglutinin and other repeats. Phyletic pattern and life-style analysis indicate that polymorphic toxins and polyimmunity loci participate in cooperative behavior and facultative 'cheating' in several ecosystems such as the human oral cavity and soil. Multiple domains from these systems have also been repeatedly transferred to eukaryotes and their viruses, such as the nucleo-cytoplasmic large DNA viruses. CONCLUSIONS: Along with a comprehensive inventory of toxins and immunity proteins, we present several testable predictions regarding active sites and catalytic mechanisms of toxins, their processing and trafficking and their role in intra-specific and inter-specific interactions between bacteria. These systems provide insights regarding the emergence of key systems at different points in eukaryotic evolution, such as ADP ribosylation, interaction of myosin VI with cargo proteins, mediation of apoptosis, hyphal heteroincompatibility, hedgehog signaling, arthropod toxins, cell-cell interaction molecules like teneurins and different signaling messengers.
    60 schema:genre article
    61 schema:inLanguage en
    62 schema:isAccessibleForFree true
    63 schema:isPartOf N034151abba1b447e9ddfd08a5f65bb53
    64 Nc066e56645244821b8c8792a2f82f782
    65 sg:journal.1036001
    66 schema:keywords ADP-ribosyl
    67 ADP-ribosylation
    68 ADP-ribosyltransferases
    69 DNA viruses
    70 Inventory
    71 MUF
    72 PRSW
    73 PVC system
    74 Photorhabdus virulence cassettes
    75 RHS/YD
    76 RelA/SpoT-like nucleotidyltransferases
    77 Single
    78 SpoT-like nucleotidyltransferases
    79 YD
    80 ZU5
    81 action
    82 active site
    83 addition
    84 analysis
    85 apoptosis
    86 architecture
    87 arthropod toxins
    88 autoproteolytic processing
    89 bacteria
    90 bacterial lineages
    91 behavior
    92 carbohydrates
    93 cargo proteins
    94 cassette
    95 catalytic mechanism
    96 catalytic spectrum
    97 cavity
    98 cell-cell interaction molecules
    99 characterization
    100 cheating
    101 clade
    102 comparative genomics
    103 components
    104 comprehensive characterization
    105 comprehensive inventory
    106 conflict
    107 contact
    108 cooperative behavior
    109 deaminase domain
    110 deaminases
    111 different points
    112 different signaling messengers
    113 distinct clades
    114 distinct secretory systems
    115 distinct toxin domains
    116 distinct types
    117 diversification
    118 diversity
    119 domain
    120 domain architecture
    121 ecology
    122 ecosystems
    123 effectors
    124 emergence
    125 enzyme
    126 eukaryotes
    127 eukaryotic evolution
    128 evidence
    129 evolution
    130 extraordinary catalytic spectrum
    131 factors
    132 family
    133 filamentous hemagglutinin
    134 filamentous structures
    135 genes
    136 genomics
    137 glycosyltranferases
    138 hedgehog
    139 hemagglutinin
    140 heteroincompatibility
    141 hints
    142 host-directed effectors
    143 human oral cavity
    144 hyphal heteroincompatibility
    145 immunity
    146 immunity genes
    147 immunity protein
    148 immunity protein domains
    149 injection
    150 insights
    151 inter-cellular contact
    152 inter-specific interactions
    153 interaction
    154 interaction molecules
    155 intra-genomic conflict
    156 intra-specific conflicts
    157 key system
    158 large DNA viruses
    159 levels
    160 life style analysis
    161 like system
    162 lineages
    163 lipids
    164 loci
    165 loci participate
    166 logic
    167 major bacterial lineages
    168 mechanism
    169 mechanism of action
    170 mediation
    171 mediation of apoptosis
    172 messenger
    173 metallopeptidase
    174 mode
    175 module
    176 molecules
    177 multiple domains
    178 multiple tandem immunity genes
    179 myosin VI
    180 novel metallopeptidase
    181 novel trafficking-related components
    182 nuclease
    183 nucleo-cytoplasmic large DNA viruses
    184 nucleotidyltransferases
    185 oral cavity
    186 organisms multiple tandem immunity genes
    187 organizational logic
    188 participates
    189 pathogenic bacteria
    190 patterns
    191 peptidase
    192 phyletic patterns
    193 point
    194 polyimmunity loci
    195 polyimmunity loci participate
    196 polyimmunity proteins
    197 polymorphic toxin systems
    198 polymorphic toxins
    199 prediction
    200 presence
    201 prior analysis
    202 processing
    203 prokaryotic polymorphic toxin systems
    204 protein
    205 protein domains
    206 protein-length analysis
    207 proteinaceous toxins
    208 recombination
    209 remarkable diversity
    210 repeats
    211 ribosyl
    212 ribosylation
    213 role
    214 secretory system
    215 sequence
    216 signaling messengers
    217 sites
    218 soil
    219 spectra
    220 standalone toxin-coding cassettes
    221 striking diversity
    222 structure
    223 structure analysis
    224 system
    225 tandem immunity genes
    226 teneurins
    227 terminal toxin domains
    228 testable predictions
    229 toxin
    230 toxin diversification
    231 toxin domain
    232 toxin module
    233 toxin systems
    234 toxin-coding cassettes
    235 trafficking
    236 trafficking modes
    237 trafficking-related components
    238 type II
    239 type V
    240 types
    241 unrecognized versions
    242 version
    243 virulence cassette
    244 virus
    245 schema:name Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics
    246 schema:pagination 18-18
    247 schema:productId N797edeba30154d3a8a188c77274766f8
    248 Nd9ee4616f0f740948bb78faff8334dbf
    249 Nf1c0e98ca192431aa028ce20ad0f88df
    250 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040385591
    251 https://doi.org/10.1186/1745-6150-7-18
    252 schema:sdDatePublished 2022-01-01T18:26
    253 schema:sdLicense https://scigraph.springernature.com/explorer/license/
    254 schema:sdPublisher N2f04dbf85f1a401494ef9f7019490f32
    255 schema:url https://doi.org/10.1186/1745-6150-7-18
    256 sgo:license sg:explorer/license/
    257 sgo:sdDataset articles
    258 rdf:type schema:ScholarlyArticle
    259 N034151abba1b447e9ddfd08a5f65bb53 schema:issueNumber 1
    260 rdf:type schema:PublicationIssue
    261 N07e945dfad164a519aa8d7ac0121087c schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    262 schema:name Signal Transduction
    263 rdf:type schema:DefinedTerm
    264 N0ea0a94700574a54ad12a189348e7b28 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    265 schema:name Catalytic Domain
    266 rdf:type schema:DefinedTerm
    267 N0ead513066d64b21b30b9764311de6ec schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    268 schema:name Amino Acid Sequence
    269 rdf:type schema:DefinedTerm
    270 N2f04dbf85f1a401494ef9f7019490f32 schema:name Springer Nature - SN SciGraph project
    271 rdf:type schema:Organization
    272 N3a532cd0c90548f782624b86c9f69286 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    273 schema:name Symbiosis
    274 rdf:type schema:DefinedTerm
    275 N500369790dfa4fd98878c8e7e03f4810 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    276 schema:name Endonucleases
    277 rdf:type schema:DefinedTerm
    278 N73ab4b8150254c4789952ad8f207b5e8 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    279 schema:name Sequence Alignment
    280 rdf:type schema:DefinedTerm
    281 N75ed4703230743c190d86c94605d3b91 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    282 schema:name Bacteria
    283 rdf:type schema:DefinedTerm
    284 N797edeba30154d3a8a188c77274766f8 schema:name doi
    285 schema:value 10.1186/1745-6150-7-18
    286 rdf:type schema:PropertyValue
    287 N82ac5e63e68d49889499b1e942d116f4 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    288 schema:name Humans
    289 rdf:type schema:DefinedTerm
    290 N834cfd50a7a9466b9020fb92fcb7a1ff schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    291 schema:name Genetic Variation
    292 rdf:type schema:DefinedTerm
    293 N85797d6ecffb47d9a20156dbc0ddaed7 rdf:first sg:person.0641126326.37
    294 rdf:rest Nad2ebbcae5e84e3b824f9160c0ea0273
    295 N8d45dadfe0804e5fa6fbc4e43a66da4c rdf:first sg:person.01106662166.38
    296 rdf:rest rdf:nil
    297 N9181ab49c2674dda96e4ed6f28a1e53b schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    298 schema:name Ecosystem
    299 rdf:type schema:DefinedTerm
    300 N9850a84cf62c486c89cde1777c290453 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    301 schema:name Bacterial Secretion Systems
    302 rdf:type schema:DefinedTerm
    303 N999bef2bea0f4551bf3024651edd57e3 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    304 schema:name Protein Structure, Tertiary
    305 rdf:type schema:DefinedTerm
    306 Nad2ebbcae5e84e3b824f9160c0ea0273 rdf:first sg:person.01234136303.93
    307 rdf:rest Nf76f1639539a44898b1802f22010fa0a
    308 Naf811679d48e42218c63ed62af3e8f91 rdf:first sg:person.012162224357.20
    309 rdf:rest N8d45dadfe0804e5fa6fbc4e43a66da4c
    310 Nbad78fff463d405dbfc6336fde0eb97a schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    311 schema:name Metalloproteases
    312 rdf:type schema:DefinedTerm
    313 Nc066e56645244821b8c8792a2f82f782 schema:volumeNumber 7
    314 rdf:type schema:PublicationVolume
    315 Nc8430f6b7f7c4b5a9ac2aa5d27f3f7e1 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    316 schema:name Bacterial Toxins
    317 rdf:type schema:DefinedTerm
    318 Ncdc480cd43144d9e9e790f2b5c8be156 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    319 schema:name Animals
    320 rdf:type schema:DefinedTerm
    321 Nce1775dfa3d64975b477977b16c53cb6 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    322 schema:name Genetic Loci
    323 rdf:type schema:DefinedTerm
    324 Nd077dd56d85a4adf900cdbc2ebd9d811 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    325 schema:name Protein Transport
    326 rdf:type schema:DefinedTerm
    327 Nd9ee4616f0f740948bb78faff8334dbf schema:name dimensions_id
    328 schema:value pub.1040385591
    329 rdf:type schema:PropertyValue
    330 Ne7ba9f0b987f40c9ab9c46df6d601ac5 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    331 schema:name Genomics
    332 rdf:type schema:DefinedTerm
    333 Nea4adfb295b547ffa41cf4c64f88edfc schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    334 schema:name Evolution, Molecular
    335 rdf:type schema:DefinedTerm
    336 Nee2c890e81144d54b9fa07c2e6a4f355 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    337 schema:name Bacterial Proteins
    338 rdf:type schema:DefinedTerm
    339 Nf02851145dc748ca9a12bc3e8168a2fb schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    340 schema:name Protein Interaction Mapping
    341 rdf:type schema:DefinedTerm
    342 Nf1c0e98ca192431aa028ce20ad0f88df schema:name pubmed_id
    343 schema:value 22731697
    344 rdf:type schema:PropertyValue
    345 Nf76f1639539a44898b1802f22010fa0a rdf:first sg:person.0673016603.16
    346 rdf:rest Naf811679d48e42218c63ed62af3e8f91
    347 Nfd925eacb1c24684b593185c5124bf64 schema:inDefinedTermSet https://www.nlm.nih.gov/mesh/
    348 schema:name Genome, Bacterial
    349 rdf:type schema:DefinedTerm
    350 anzsrc-for:06 schema:inDefinedTermSet anzsrc-for:
    351 schema:name Biological Sciences
    352 rdf:type schema:DefinedTerm
    353 anzsrc-for:0601 schema:inDefinedTermSet anzsrc-for:
    354 schema:name Biochemistry and Cell Biology
    355 rdf:type schema:DefinedTerm
    356 sg:grant.2726065 http://pending.schema.org/fundedItem sg:pub.10.1186/1745-6150-7-18
    357 rdf:type schema:MonetaryGrant
    358 sg:journal.1036001 schema:issn 1745-6150
    359 schema:name Biology Direct
    360 schema:publisher Springer Nature
    361 rdf:type schema:Periodical
    362 sg:person.01106662166.38 schema:affiliation grid-institutes:grid.419234.9
    363 schema:familyName Aravind
    364 schema:givenName L
    365 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01106662166.38
    366 rdf:type schema:Person
    367 sg:person.012162224357.20 schema:affiliation grid-institutes:grid.419234.9
    368 schema:familyName Iyer
    369 schema:givenName Lakshminarayan M
    370 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.012162224357.20
    371 rdf:type schema:Person
    372 sg:person.01234136303.93 schema:affiliation grid-institutes:grid.11899.38
    373 schema:familyName de Souza
    374 schema:givenName Robson F
    375 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.01234136303.93
    376 rdf:type schema:Person
    377 sg:person.0641126326.37 schema:affiliation grid-institutes:grid.419234.9
    378 schema:familyName Zhang
    379 schema:givenName Dapeng
    380 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0641126326.37
    381 rdf:type schema:Person
    382 sg:person.0673016603.16 schema:affiliation grid-institutes:grid.419234.9
    383 schema:familyName Anantharaman
    384 schema:givenName Vivek
    385 schema:sameAs https://app.dimensions.ai/discover/publication?and_facet_researcher=ur.0673016603.16
    386 rdf:type schema:Person
    387 sg:pub.10.1007/978-1-4419-8414-2_2 schema:sameAs https://app.dimensions.ai/details/publication/pub.1036685376
    388 https://doi.org/10.1007/978-1-4419-8414-2_2
    389 rdf:type schema:CreativeWork
    390 sg:pub.10.1007/978-1-4419-8632-0_12 schema:sameAs https://app.dimensions.ai/details/publication/pub.1051522575
    391 https://doi.org/10.1007/978-1-4419-8632-0_12
    392 rdf:type schema:CreativeWork
    393 sg:pub.10.1007/978-3-0348-8466-2 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006928762
    394 https://doi.org/10.1007/978-3-0348-8466-2
    395 rdf:type schema:CreativeWork
    396 sg:pub.10.1007/s00018-002-8471-1 schema:sameAs https://app.dimensions.ai/details/publication/pub.1019930863
    397 https://doi.org/10.1007/s00018-002-8471-1
    398 rdf:type schema:CreativeWork
    399 sg:pub.10.1007/s00018-007-7434-y schema:sameAs https://app.dimensions.ai/details/publication/pub.1031121043
    400 https://doi.org/10.1007/s00018-007-7434-y
    401 rdf:type schema:CreativeWork
    402 sg:pub.10.1007/s00251-001-0381-0 schema:sameAs https://app.dimensions.ai/details/publication/pub.1035823889
    403 https://doi.org/10.1007/s00251-001-0381-0
    404 rdf:type schema:CreativeWork
    405 sg:pub.10.1007/s002510100297 schema:sameAs https://app.dimensions.ai/details/publication/pub.1032416368
    406 https://doi.org/10.1007/s002510100297
    407 rdf:type schema:CreativeWork
    408 sg:pub.10.1007/s10482-010-9468-7 schema:sameAs https://app.dimensions.ai/details/publication/pub.1011482058
    409 https://doi.org/10.1007/s10482-010-9468-7
    410 rdf:type schema:CreativeWork
    411 sg:pub.10.1007/s13238-010-0009-y schema:sameAs https://app.dimensions.ai/details/publication/pub.1007914195
    412 https://doi.org/10.1007/s13238-010-0009-y
    413 rdf:type schema:CreativeWork
    414 sg:pub.10.1038/338357a0 schema:sameAs https://app.dimensions.ai/details/publication/pub.1007053259
    415 https://doi.org/10.1038/338357a0
    416 rdf:type schema:CreativeWork
    417 sg:pub.10.1038/cdd.2011.162 schema:sameAs https://app.dimensions.ai/details/publication/pub.1041318416
    418 https://doi.org/10.1038/cdd.2011.162
    419 rdf:type schema:CreativeWork
    420 sg:pub.10.1038/hdy.2008.113 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015759634
    421 https://doi.org/10.1038/hdy.2008.113
    422 rdf:type schema:CreativeWork
    423 sg:pub.10.1038/nature02794 schema:sameAs https://app.dimensions.ai/details/publication/pub.1000185087
    424 https://doi.org/10.1038/nature02794
    425 rdf:type schema:CreativeWork
    426 sg:pub.10.1038/nature09490 schema:sameAs https://app.dimensions.ai/details/publication/pub.1019643796
    427 https://doi.org/10.1038/nature09490
    428 rdf:type schema:CreativeWork
    429 sg:pub.10.1038/nature10244 schema:sameAs https://app.dimensions.ai/details/publication/pub.1002229949
    430 https://doi.org/10.1038/nature10244
    431 rdf:type schema:CreativeWork
    432 sg:pub.10.1038/nature10846 schema:sameAs https://app.dimensions.ai/details/publication/pub.1015413547
    433 https://doi.org/10.1038/nature10846
    434 rdf:type schema:CreativeWork
    435 sg:pub.10.1038/nature10962 schema:sameAs https://app.dimensions.ai/details/publication/pub.1005452992
    436 https://doi.org/10.1038/nature10962
    437 rdf:type schema:CreativeWork
    438 sg:pub.10.1038/nchembio.748 schema:sameAs https://app.dimensions.ai/details/publication/pub.1044207924
    439 https://doi.org/10.1038/nchembio.748
    440 rdf:type schema:CreativeWork
    441 sg:pub.10.1038/nrmicro1526 schema:sameAs https://app.dimensions.ai/details/publication/pub.1031832630
    442 https://doi.org/10.1038/nrmicro1526
    443 rdf:type schema:CreativeWork
    444 sg:pub.10.1038/nsmb.1619 schema:sameAs https://app.dimensions.ai/details/publication/pub.1047619820
    445 https://doi.org/10.1038/nsmb.1619
    446 rdf:type schema:CreativeWork
    447 sg:pub.10.1038/nsmb.1896 schema:sameAs https://app.dimensions.ai/details/publication/pub.1013910559
    448 https://doi.org/10.1038/nsmb.1896
    449 rdf:type schema:CreativeWork
    450 sg:pub.10.1134/s0006297910010013 schema:sameAs https://app.dimensions.ai/details/publication/pub.1038699984
    451 https://doi.org/10.1134/s0006297910010013
    452 rdf:type schema:CreativeWork
    453 sg:pub.10.1186/1471-2105-5-113 schema:sameAs https://app.dimensions.ai/details/publication/pub.1040413794
    454 https://doi.org/10.1186/1471-2105-5-113
    455 rdf:type schema:CreativeWork
    456 sg:pub.10.1186/1471-2164-10-33 schema:sameAs https://app.dimensions.ai/details/publication/pub.1011169430
    457 https://doi.org/10.1186/1471-2164-10-33
    458 rdf:type schema:CreativeWork
    459 sg:pub.10.1186/1471-2164-10-584 schema:sameAs https://app.dimensions.ai/details/publication/pub.1001222619
    460 https://doi.org/10.1186/1471-2164-10-584
    461 rdf:type schema:CreativeWork
    462 sg:pub.10.1186/1471-2164-6-139 schema:sameAs https://app.dimensions.ai/details/publication/pub.1022818110
    463 https://doi.org/10.1186/1471-2164-6-139
    464 rdf:type schema:CreativeWork
    465 sg:pub.10.1186/1745-6150-3-8 schema:sameAs https://app.dimensions.ai/details/publication/pub.1006845773
    466 https://doi.org/10.1186/1745-6150-3-8
    467 rdf:type schema:CreativeWork
    468 sg:pub.10.1186/gb-2003-4-12-r81 schema:sameAs https://app.dimensions.ai/details/publication/pub.1016542336
    469 https://doi.org/10.1186/gb-2003-4-12-r81
    470 rdf:type schema:CreativeWork
    471 sg:pub.10.1186/gb-2003-4-2-r11 schema:sameAs https://app.dimensions.ai/details/publication/pub.1039399488
    472 https://doi.org/10.1186/gb-2003-4-2-r11
    473 rdf:type schema:CreativeWork
    474 sg:pub.10.1186/gb-2006-7-7-r60 schema:sameAs https://app.dimensions.ai/details/publication/pub.1027241290
    475 https://doi.org/10.1186/gb-2006-7-7-r60
    476 rdf:type schema:CreativeWork
    477 sg:pub.10.1186/gb-2008-9-6-229 schema:sameAs https://app.dimensions.ai/details/publication/pub.1021664284
    478 https://doi.org/10.1186/gb-2008-9-6-229
    479 rdf:type schema:CreativeWork
    480 grid-institutes:grid.11899.38 schema:alternateName Departamento de Microbiologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, Brazil
    481 schema:name Departamento de Microbiologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, São Paulo, Brazil
    482 National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA
    483 rdf:type schema:Organization
    484 grid-institutes:grid.419234.9 schema:alternateName National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA
    485 schema:name National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD, 20894, USA
    486 rdf:type schema:Organization
     




    Preview window. Press ESC to close (or click here)


    ...