Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria
Publication Date
September 08, 2011
Journal
PLOS Genetics
Authors
Jennifer Luciano, Rym Agrebi, Anne Valérie Le Gall, Morgane Wartel, et al
Volume
7
Issue
9
Pages
e1002268
DOI
https://dx.plos.org/10.1371/journal.pgen.1002268
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1002268
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/21931562
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3169522
Europe PMC
http://europepmc.org/abstract/MED/21931562
Web of Science
000295419100021
Scopus
80053436594
Mendeley
http://www.mendeley.com/research/emergence-modular-evolution-novel-motility-machinery-bacteria
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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/373429", "https://ndownloader.figshare.com/files/373497", "https://ndownloader.figshare.com/files/373579", "https://ndownloader.figshare.com/files/373677", "https://ndownloader.figshare.com/files/373788", "https://ndownloader.figshare.com/files/373854", "https://ndownloader.figshare.com/files/373928", "https://ndownloader.figshare.com/files/373988", "https://ndownloader.figshare.com/files/374109", "https://ndownloader.figshare.com/files/374141", "https://ndownloader.figshare.com/files/374176", "https://ndownloader.figshare.com/files/374205", "https://ndownloader.figshare.com/files/374255", "https://ndownloader.figshare.com/files/374283", "https://ndownloader.figshare.com/files/374318", "https://ndownloader.figshare.com/files/374356", "https://ndownloader.figshare.com/files/374377"], "description"=>"<div><p>Bacteria glide across solid surfaces by mechanisms that have remained largely mysterious despite decades of research. In the deltaproteobacterium <em>Myxococcus xanthus</em>, this locomotion allows the formation stress-resistant fruiting bodies where sporulation takes place. However, despite the large number of genes identified as important for gliding, no specific machinery has been identified so far, hampering in-depth investigations. Based on the premise that components of the gliding machinery must have co-evolved and encode both envelope-spanning proteins and a molecular motor, we re-annotated known gliding motility genes and examined their taxonomic distribution, genomic localization, and phylogeny. We successfully delineated three functionally related genetic clusters, which we proved experimentally carry genes encoding the basal gliding machinery in <em>M. xanthus</em>, using genetic and localization techniques. For the first time, this study identifies structural gliding motility genes in the Myxobacteria and opens new perspectives to study the motility mechanism. Furthermore, phylogenomics provide insight into how this machinery emerged from an ancestral conserved core of genes of unknown function that evolved to gliding by the recruitment of functional modules in Myxococcales. Surprisingly, this motility machinery appears to be highly related to a sporulation system, underscoring unsuspected common mechanisms in these apparently distinct morphogenic phenomena.</p> </div>", "links"=>[], "tags"=>["emergence", "modular", "motility", "machinery"], "article_id"=>133746, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.s001", "https://dx.doi.org/10.1371/journal.pgen.1002268.s002", "https://dx.doi.org/10.1371/journal.pgen.1002268.s003", "https://dx.doi.org/10.1371/journal.pgen.1002268.s004", "https://dx.doi.org/10.1371/journal.pgen.1002268.s005", "https://dx.doi.org/10.1371/journal.pgen.1002268.s006", "https://dx.doi.org/10.1371/journal.pgen.1002268.s007", "https://dx.doi.org/10.1371/journal.pgen.1002268.s008", "https://dx.doi.org/10.1371/journal.pgen.1002268.s009", "https://dx.doi.org/10.1371/journal.pgen.1002268.s010", "https://dx.doi.org/10.1371/journal.pgen.1002268.s011", "https://dx.doi.org/10.1371/journal.pgen.1002268.s012", "https://dx.doi.org/10.1371/journal.pgen.1002268.s013", "https://dx.doi.org/10.1371/journal.pgen.1002268.s014", "https://dx.doi.org/10.1371/journal.pgen.1002268.s015", "https://dx.doi.org/10.1371/journal.pgen.1002268.s016", "https://dx.doi.org/10.1371/journal.pgen.1002268.s017"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Emergence_and_Modular_Evolution_of_a_Novel_Motility_Machinery_in_Bacteria/133746", "title"=>"Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-08 01:02:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/738105"], "description"=>"<p>(A) Genetic organisation of the 15 genes composing the G1, G2 and M1 clusters encoding the putative components of the gliding machinery in <i>Myxococcus xanthus</i> DK 1622. Predicted genes are indicated with their locus_tag, and their former and new names. The arrow that represents the putative MXAN_4864 and MXAN_4865 genes is a dotted line because they are likely pseudogenes (see text for more details). Stars indicate genes that were hit by the transposon screens <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002268#pgen.1002268-Youderian1\" target=\"_blank\">[16]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002268#pgen.1002268-Yu1\" target=\"_blank\">[17]</a>. (B) Genetic organization of the G3, G4, G5 and M2 homologue clusters in <i>M. xanthus</i> DK 1622. The colour code indicates homologous genes and will be used throughout the study.</p>", "links"=>[], "tags"=>["clusters", "carrying", "gliding", "motility", "genes"], "article_id"=>408467, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_clusters_carrying_gliding_motility_genes_in_M_xanthus_/408467", "title"=>"Genetic clusters carrying gliding motility genes in <i>M. xanthus</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:21:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/738192"], "description"=>"<p>(A) For a given gene, the number of homologues in the corresponding genome is indicated by the numbers within arrows. The relationships between the species carrying the different homologues of the genes are indicated by the phylogeny on the left. Based on their taxonomic distribution, the 14 genes can be divided into Group A (grey background) and Group B (white background). (B) In all non Deltaproteobacteria and in <i>Geobacter</i>, the Group B genes clustered in a single genomic region.</p>", "links"=>[], "tags"=>["homologues", "14", "genes", "composing", "m1"], "article_id"=>408552, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Taxonomic_distribution_of_the_closest_homologues_of_the_14_genes_composing_the_G1_G2_and_M1_clusters_and_genetic_organization_of_the_core_complex_/408552", "title"=>"Taxonomic distribution of the closest homologues of the 14 genes composing the G1, G2, and M1 clusters, and genetic organization of the core complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:22:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/738374"], "description"=>"<p>(A) Motility at the <i>gltA-H</i>and <i>gltK</i> deletion mutants colony edges after 48h incubation at 32°C on hard (1.5%) (upper panel). Lower left panel: twitching motility is unaffected in the <i>gltA-H</i> and <i>gltK</i> deletion mutants and observed in the form of expanded colony swarms on soft (0.5%). Lower right panel: motility of double <i>pilA gltA-H</i> and <i>pilA gltK</i> deletion mutants showing the complete absence of motility in these mutants. (B) Hard agar colony edges of the <i>gltD frzE, gltD frzE pilA</i> and <i>aglZ frzE pilA</i> mutants showing the lack of motility restoration in the <i>gltD</i> mutant. Note that single cells are clearly visible in the <i>aglZ frzE pilA</i> mutant, consistent with previous literature <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002268#pgen.1002268-Mauriello3\" target=\"_blank\">[24]</a>.</p>", "links"=>[], "tags"=>["genes", "encode", "components", "motility"], "article_id"=>408739, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Group_B_genes_encode_structural_components_of_the_motility_machinery_/408739", "title"=>"Group B genes encode structural components of the motility machinery.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:25:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/738486"], "description"=>"<p>Envelope localization of the Glt proteins. GltF localization is determined by western detection of the GltF-mCherry fusion (as indicated by the asterisk). FrzS, PilC and PilQ were used as control markers of the soluble, inner membrane and outer membrane fractions, respectively.</p>", "links"=>[], "tags"=>["localization", "glt"], "article_id"=>408857, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Envelope_localization_of_the_Glt_proteins_/408857", "title"=>"Envelope localization of the Glt proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:27:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/738611"], "description"=>"<p>(A) Localization of GltD-mCherry in different <i>z</i> sections in WT (upper panel) and mutant backgrounds (lower panel). Shown are unprocessed fluorescent micrographs of the different sections (position of the section along the <i>z</i> axis is indicated by a barred circle). Open triangles indicate GltD clusters. Scale bar  = 1 µm. (B) Co-localization of GltD- and GltF-mCherry with AglZ-YFP. Open triangles indicate clusters were the chimeric proteins co-localize. Scale bar  = 1 µm. (C) dynamic localization of GltD-mCherry and AglZ-YFP during movement. Scale bar  = 1 µm.</p>", "links"=>[], "tags"=>["glt", "proteins", "localize", "dynamically", "aglz-yfp", "clusters", "aglq-dependent"], "article_id"=>408967, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Glt_proteins_localize_dynamically_to_the_AglZ_YFP_clusters_in_a_AglQ_dependent_manner_/408967", "title"=>"The Glt proteins localize dynamically to the AglZ-YFP clusters in a AglQ-dependent manner.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:29:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/738760"], "description"=>"<p>AglR interacts with GltG in a bacterial two-hybrid assay.</p>", "links"=>[], "tags"=>["aglrqs", "interacts", "gliding", "motility"], "article_id"=>409124, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_AglRQS_motor_interacts_directly_with_the_gliding_motility_machinery_/409124", "title"=>"The AglRQS motor interacts directly with the gliding motility machinery.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:32:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/738870"], "description"=>"<p>Rooted Bayesian phylogenetic trees of concatenated alignments of (A) GltD, GltE and GltG (39 sequences, 586 positions) and (B) AglR, AglQ and AglS (38 sequences, 376 positions). The root has been placed according to the phylogenies of the individual proteins. Numbers at nodes indicate posterior probabilities (PP) computed by MrBayes and bootstrap values (BV) computed by Treefinder and PhyML. Only PP and BV above 0.5 and 50% are shown. The scale bars represent the average number of substitutions per site. In each phylogenetic tree the putative <i>M. xanthus</i> gliding motility proteins are underlined and are illustrated with colour-coded gene symbols. For each species the individual locus_tags of the concatenated proteins are indicated in brackets. The position of multiple duplications of the concatenated proteins in <i>M. xanthus</i> are highlighted by black rectangles.</p>", "links"=>[], "tags"=>["genetics and genomics", "Evolutionary biology"], "article_id"=>409238, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Co_evolution_of_gltD_E_G_and_aglR_Q_S_/409238", "title"=>"Co-evolution of <i>gltD-E-G</i> and <i>aglR-Q-S</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:33:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/739003"], "description"=>"<p>(A) Evolutionary scenario describing the emergence and evolution of the gliding motility machinery in <i>M. xanthus</i>. The relationships between organisms carrying close homologues of the 14 genes encoding putative components of the gliding machinery in <i>M. xanthus</i> are represented by the phylogeny. Green and red arrows respectively indicate gene acquisition and gene loss. The number of gene copies that were acquired or lost is indicated within arrows. The purple dotted arrows represent horizontal gene transfer events of one or several components. WGD marks the putative whole genome duplication event that occurred in the ancestor of Myxococcales. For each gene, locus_tag, former (<i>agm</i>/<i>agl</i>/<i>agn</i>) and new (<i>glt</i> and <i>agl</i>) names are provided. The number of complete genomes that contain homologues of <i>glt</i> and <i>agl</i> genes compared to the total number of complete genomes available at the beginning of this study are indicated in brackets. (B) The <i>Myxococcus</i> gliding machinery. The diagram compiles data from this work and published literature. Components were added based on bioinformatic predictions, mutagenesis, interaction and localization studies. Exhaustive information is not available for all proteins and thus the diagram largely is subject to modifications once more data will be available. Known interactions within the complex from experimental evidence are AglR-GltG, AglZ-MglA and interactions within the AglRQS molecular motor <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002268#pgen.1002268-Sun1\" target=\"_blank\">[13]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002268#pgen.1002268-Mauriello2\" target=\"_blank\">[15]</a>. For clarity, the proteins were colour-coded as in the rest of the manuscript.</p>", "links"=>[], "tags"=>["gliding", "motility"], "article_id"=>409371, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolution_and_structure_of_the_Myxococcus_gliding_motility_machinery_/409371", "title"=>"Evolution and structure of the <i>Myxococcus</i> gliding motility machinery.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-08 02:36:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/739122"], "description"=>"a<p>ND = Not Detected. The relative expression of the <i>gltK</i>, <i>gltB</i>, <i>gltA</i> and <i>gltC</i> genes in the wild-type strain and in deletion mutant strains was determined by q-RT-PCR. All the values are representative values from several independent experiments.</p>", "links"=>[], "tags"=>["mrna", "g2", "deletion"], "article_id"=>409493, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.t003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_glt_mRNA_expression_in_the_cluster_G2_deletion_strains_/409493", "title"=>"<i>glt</i> mRNA expression in the cluster G2 deletion strains.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:38:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/739166"], "description"=>"a<p>ND = Not Detected. The relative expression of the <i>gltD</i>, <i>gltE</i>, <i>gltF</i>, <i>gltG</i> and <i>gltH</i> genes in the wild-type strain and in deletion mutant strains was determined by q-RT-PCR. All the values are representative values from several independent experiments.</p>", "links"=>[], "tags"=>["mrna", "g1", "deletion"], "article_id"=>409533, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_glt_mRNA_expression_in_cluster_G1_deletion_strains_/409533", "title"=>"<i>glt</i> mRNA expression in cluster G1 deletion strains.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:38:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/739195"], "description"=>"<p>Bioinformatic analysis of G1, G2, and M1 cluster genes.</p>", "links"=>[], "tags"=>["m1"], "article_id"=>409562, "categories"=>["Genetics", "Evolutionary Biology"], "users"=>["Jennifer Luciano", "Rym Agrebi", "Anne Valérie Le Gall", "Morgane Wartel", "Francesca Fiegna", "Adrien Ducret", "Celine Brochier-Armanet", "Tâm Mignot"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002268.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bioinformatic_analysis_of_G1_G2_and_M1_cluster_genes_/409562", "title"=>"Bioinformatic analysis of G1, G2, and M1 cluster genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-08 02:39:22"}

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  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"7"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"7", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"15", "supp-data"=>"17", "cited-by"=>"1", "year"=>"2015", "month"=>"8"}
  • {"unique-ip"=>"15", "full-text"=>"12", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2015", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"6", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"2", "year"=>"2015", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2015", "month"=>"12"}
  • {"unique-ip"=>"9", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"1"}
  • {"unique-ip"=>"8", "full-text"=>"8", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"2"}
  • {"unique-ip"=>"9", "full-text"=>"11", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"3"}
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  • {"unique-ip"=>"5", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2016", "month"=>"6"}
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  • {"unique-ip"=>"4", "full-text"=>"7", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"3", "cited-by"=>"0", "year"=>"2016", "month"=>"9"}
  • {"unique-ip"=>"11", "full-text"=>"10", "pdf"=>"8", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"10"}
  • {"unique-ip"=>"9", "full-text"=>"9", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"5", "cited-by"=>"0", "year"=>"2016", "month"=>"11"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2016", "month"=>"12"}
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  • {"unique-ip"=>"3", "full-text"=>"3", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"6"}
  • {"unique-ip"=>"4", "full-text"=>"5", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"3", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}
  • {"unique-ip"=>"2", "full-text"=>"2", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"9"}
  • {"unique-ip"=>"26", "full-text"=>"13", "pdf"=>"2", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"53", "supp-data"=>"16", "cited-by"=>"0", "year"=>"2017", "month"=>"10"}
  • {"unique-ip"=>"6", "full-text"=>"6", "pdf"=>"0", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"11"}
  • {"unique-ip"=>"4", "full-text"=>"4", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"12"}
  • {"unique-ip"=>"21", "full-text"=>"11", "pdf"=>"1", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"9", "supp-data"=>"3", "cited-by"=>"1", "year"=>"2018", "month"=>"1"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"3"}
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  • {"unique-ip"=>"7", "full-text"=>"6", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"4"}
  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"7"}
  • {"unique-ip"=>"6", "full-text"=>"7", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"4", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"16", "full-text"=>"15", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"6", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"15", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"5", "full-text"=>"5", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"7", "full-text"=>"7", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"15", "full-text"=>"16", "pdf"=>"5", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"12", "full-text"=>"12", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
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Relative Metric

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