Genome Landscapes and Bacteriophage Codon Usage
Publication Date
February 29, 2008
Journal
PLOS Computational Biology
Authors
Julius B. Lucks, David R. Nelson, Grzegorz R. Kudla & Joshua B. Plotkin
Volume
4
Issue
2
Pages
e1000001
DOI
http://doi.org/10.1371/journal.pcbi.1000001
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.1000001
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/18463708
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2266997
Europe PMC
http://europepmc.org/abstract/MED/18463708
Web of Science
000269692800005
Scopus
40149100835
Mendeley
http://www.mendeley.com/research/genome-landscapes-bacteriophage-codon-usage
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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/936628"], "description"=>"<p>The table shows the median and values among phages classified as temperate, non-temperate, or un-identified for all phages included in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-g008\" target=\"_blank\">Figure 8</a> and <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t002\" target=\"_blank\">Table 2</a>. Small median values indicate that these phages have significantly non-random (in either direction) BCAI, controlling for the amino acid sequence and the GC3 sequence, while small median values indicate that these phages have significantly non-random (in either direction) GC3, controlling for the amino acid sequence and the BCAI sequence. We also report the significance of non-parametric ANOVAs that compare these medians between these groups of phages.</p>", "links"=>[], "tags"=>["codon"], "article_id"=>607072, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.t006", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phage_lifestyle_versus_codon_usage_/607072", "title"=>"Phage lifestyle versus codon usage.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-02-29 01:57:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/936513"], "description"=>"<p>The figure shows the aqua (CAI, as in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-g003\" target=\"_blank\">Figure 3</a>) and orange (BCAI, as in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-g005\" target=\"_blank\">Figure 5</a>) randomization tests overlaid with information about protein function: genes classified as structural are shown with a white background and all other genes with a grey background. The histograms indicate a clear relationship between the structural classification of a gene and its significance under the aqua and orange tests: structural genes typically have elevated quantiles in the aqua test, whereas other genes typically have depressed quantiles. In other words, structural genes exhibit elevated CAI values when controlling for their amino acid sequence, compared to codon usage in the genome as a whole. Moreover, as the orange histograms indicate, this pattern is not caused by variation in GC3 content: the structural genes exhibit elevated BCAI values after controlling for both their amino acid sequence and their GC3 sequence.</p>", "links"=>[], "tags"=>["codon", "usage", "lambda"], "article_id"=>606957, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g009", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_relationship_between_codon_usage_and_protein_function_in_lambda_phage_/606957", "title"=>"The relationship between codon usage and protein function in lambda phage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:55:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/936602"], "description"=>"<p>For each phage genome, the GenBank entry was scanned for the presence of tRNA genes. The number of these genes are listed beside the names of the phages for the ten phage genomes in this study that do encode tRNAs.</p>", "links"=>[], "tags"=>["trna", "genes", "phage"], "article_id"=>607047, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.t005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_number_of_tRNA_genes_in_phage_genomes_/607047", "title"=>"The number of tRNA genes in phage genomes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-02-29 01:57:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/935864"], "description"=>"<p>Landscapes of GC3. (left) and CAI (right) measures of codon usage in Lambda phage. Only coding sequences are considered, which when concatenated together are 40,773 bp long (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t002\" target=\"_blank\">Table 2</a>). The GC3 landscape is the mean-centered cumulative sum of the GC3 content (GC3 = 1, AT3 = 0) of codons. The CAI landscape is the mean-centered cumulative sum of the log <i>w</i>-value for each codon. For each landscape, a region exhibiting an uphill slope corresponds to higher than average GC3 or CAI. The horizontal purple band represents the expected amount of variation in a random walk of GC3 or AT3 choices, given by Equation 2. Both landscapes exhibit features far outside of the purple bands, indicating that the patterns of codon usage are highly non-random. Gene boundaries are represented by the bars in the histograms below each landscape. The height of the bars in the histogram indicate the GC3 and CAI values for each gene.</p>", "links"=>[], "tags"=>["cai", "landscapes", "lambda"], "article_id"=>606310, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GC3_and_CAI_landscapes_for_lambda_phage_/606310", "title"=>"GC3 and CAI landscapes for lambda phage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:45:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/936206"], "description"=>"<p>Observed landscapes are shown along with randomized landscapes associated with the green and orange tests. The green randomization procedure tests the significance of the GC3 landscape controlling for the observed CAI (actually, BCAI) variation across the genome. The orange randomization procedure tests the significance of the BCAI landscape, controlling for the observed GC3 variation across the genome. Both tests preserve the amino-acid sequence exactly. Both observed landscapes lie outside the distribution of random trials, indicating there is non-random GC3 content controlling for CAI, and non-random CAI content controlling for GC3.</p>", "links"=>[], "tags"=>["randomized", "landscapes", "lambda"], "article_id"=>606647, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Observed_and_randomized_landscapes_for_lambda_phage_/606647", "title"=>"Observed and randomized landscapes for lambda phage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:50:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/936424"], "description"=>"<p>Phage names are listed on the x-axis, and are sorted by their orange <i>p</i>-value. A total of 29 genomes exhibit non-random GC3 content controlling for CAI (green test); and a total of 22 genome exhibit non-random CAI content controlling for GC3 (orange test). 17 genomes pass both of these tests. The dashed horizontal line indicates the threshold for significance after Bonfernni correction (i.e. 5%/50). Upwards arrows indicate p-values that lie beyond the limits of the y-axis. See <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t002\" target=\"_blank\">Table 2</a> for phage properties, including the <i>p</i>-values for these tests. Twenty four phage genomes that failed the aqua GC3 or CAI control tests are not included in this figure.</p>", "links"=>[], "tags"=>["fisher", "p-values", "randomization", "50", "phage"], "article_id"=>606868, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g008", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Combined_Fisher_p_values_for_the_green_and_orange_randomization_tests_across_50_phage_genomes_/606868", "title"=>"Combined Fisher p-values for the green and orange randomization tests across 50 phage genomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:54:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/936009"], "description"=>"<p>The figure shows the observed GC3 (left) and CAI (right) landscapes, plotted in black, along with the mean±1, and ±2 standard deviations of randomized trials, shown in aqua (bold line, dark and light regions, respectively). The aqua randomization test shown here draws random synonymous codons that preserve the exact amino acid sequence, according to probabilities that preserve the global codon usage distribution of the lambda genome. For the most part, the observed landscapes lie significantly outside the distribution of randomized landscapes–implying that the amino acid content of genes is not responsible for the observed pattern of the CAI landscape. In the lower panel, however, genes whose GC3 (left) or CAI (right) values fall between the 0.025 and 0.975 quantile of the random trials are shadowed in grey; the GC3/CAI values of such genes are not significantly different from random, given their amino acid sequence.</p>", "links"=>[], "tags"=>["randomized", "landscapes", "lambda"], "article_id"=>606449, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Observed_and_randomized_landscapes_for_lambda_phage_/606449", "title"=>"Observed and randomized landscapes for lambda phage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:47:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/936676"], "description"=>"<p>Properties are listed for all phages included in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-g008\" target=\"_blank\">Figure 8</a>, in the same order based on the orange <i>p</i>-value. Lifestyle annotations are T (temperate), NT (non-temperate), U (unknown). The coding length refers to the length of all coding sequences concatenated together (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#s4\" target=\"_blank\">Methods</a>).</p>", "links"=>[], "tags"=>["computational biology/genomics", "computational biology/population genetics", "computational biology/sequence motif analysis"], "article_id"=>607120, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.t002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phage_properties_/607120", "title"=>"Phage properties.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-02-29 01:58:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/461217", "https://ndownloader.figshare.com/files/461343"], "description"=>"<div><p>Across all kingdoms of biological life, protein-coding genes exhibit unequal usage of synonymous codons. Although alternative theories abound, translational selection has been accepted as an important mechanism that shapes the patterns of codon usage in prokaryotes and simple eukaryotes. Here we analyze patterns of codon usage across 74 diverse bacteriophages that infect <em>E. coli</em>, <em>P. aeruginosa</em>, and <em>L. lactis</em> as their primary host. We use the concept of a “genome landscape,” which helps reveal non-trivial, long-range patterns in codon usage across a genome. We develop a series of randomization tests that allow us to interrogate the significance of one aspect of codon usage, such as GC content, while controlling for another aspect, such as adaptation to host-preferred codons. We find that 33 phage genomes exhibit highly non-random patterns in their GC3-content, use of host-preferred codons, or both. We show that the head and tail proteins of these phages exhibit significant bias towards host-preferred codons, relative to the non-structural phage proteins. Our results support the hypothesis of translational selection on viral genes for host-preferred codons, over a broad range of bacteriophages.</p></div>", "links"=>[], "tags"=>["genome", "landscapes", "bacteriophage", "codon", "usage"], "article_id"=>150891, "categories"=>["Cancer"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1000001.s001", "https://dx.doi.org/10.1371/journal.pcbi.1000001.s002"], "stats"=>{"downloads"=>1, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genome_Landscapes_and_Bacteriophage_Codon_Usage/150891", "title"=>"Genome Landscapes and Bacteriophage Codon Usage", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-02-29 00:14:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/936066"], "description"=>"<p>The table of 61 codons along with their associated <i>w</i>-values is shown for <i>E. coli</i>. The <i>w</i>-value of each codon reflects its frequency in highly transcribed <i>E. coli</i> genes (see main text). The <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t001\" target=\"_blank\">Table 1</a> is divided into four regions: codons with high CAI (w≥0.9) ending in G or C (dark red); codons with high CAI ending in A or T (dark blue); codons with low CAI (<i>w</i><0.9) ending in G or C (light red); codons with low CAI ending in A or T (light blue). As the table shows, there is a slight bias for GC3 in the high-CAI codons (58%), and slight bias away from GC3 in the low-CAI codons (48%).</p>", "links"=>[], "tags"=>["codon", "usage"], "article_id"=>606514, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g004", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_E_coli_codon_usage_master_table_/606514", "title"=>"<i>E. coli</i> codon usage master table.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:48:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/936699"], "description"=>"<p>The table shows the median <i>p</i><sup>></sup> values among structural and non-structural genes, under the aqua and orange randomization tests. Small <i>p</i><sup>></sup> values indicate significantly elevated CAI, controlling for the amino acid sequence (aqua test) and the GC3 sequence (orange test). We also report the significance of non-parametric ANOVAs that compare median <i>p</i><sup>></sup>-values between the structural and non-structural genes. Analyses are limited to those genes that pass the aqua test, as described in the main text; similar results are found without this restriction.</p>", "links"=>[], "tags"=>["annotation", "verses", "codon"], "article_id"=>607146, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.t003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structural_annotation_verses_codon_usage_/607146", "title"=>"Structural annotation verses codon usage.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-02-29 01:59:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/936647"], "description"=>"<p>The three randomization tests used in the paper are color-coded according to what genome properties are constrained in the random trials.</p>", "links"=>[], "tags"=>["computational biology/genomics", "computational biology/population genetics", "computational biology/sequence motif analysis"], "article_id"=>607095, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Randomization_test_descriptions_/607095", "title"=>"Randomization test descriptions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-02-29 01:58:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/936264"], "description"=>"<p>Unlike <i>E. coli</i>, <i>P. aeruginosa</i> strongly favors GC3 in high-CAI codons (94%), and <i>L. lactis</i> strongly favors AT3 in high-CAI codons (72%).</p>", "links"=>[], "tags"=>["preferred", "codon", "usage", "tables", "conventions"], "article_id"=>606712, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g006", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematics_of_preferred_codon_usage_tables_for_E_coli_P_aeruginosa_and_L_lactis_following_the_conventions_of_Figure_4_/606712", "title"=>"Schematics of preferred codon usage tables for <i>E. coli</i>, <i>P. aeruginosa</i>, and <i>L. lactis</i> following the conventions of Figure 4.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:51:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/936338"], "description"=>"<p>Bacteriophages P2 (A) and T3 (B) both infect <i>E. coli</i>. Phage D3112 (C) infects <i>P. aeruginosa</i>. Phage bIL286 (D) infects <i>L. lactis</i>. T3 is the only non-temperate phage of this group. See <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t002\" target=\"_blank\">Table 2</a> for combined Fisher p-values for these tests. In the case of bIL286, note the lack of evidence for codon bias evident in the green and orange tests for bIL286, as confirmed by the insignificant <i>p</i>-values in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t002\" target=\"_blank\">Table 2</a>. In this case, we cannot rule out the possibility that the observed pattern in GC3 is determined completely by the amino acid and CAI sequence (green), or that the observed pattern in CAI is determined by the amino acid and GC3 sequence (orange).</p>", "links"=>[], "tags"=>["randomization"], "article_id"=>606788, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g007", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Green_left_and_orange_right_randomization_tests_for_several_phages_/606788", "title"=>"Green (left) and orange (right) randomization tests for several phages.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:53:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/936574"], "description"=>"<p>As in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-t003\" target=\"_blank\">Table 3</a>, we compare the median aqua and orange <i>p</i><sup>></sup> values among head genes, tail genes, and non-structural genes. We report the significance of pairwise non-parametric ANOVAs comparing head to non-structural, tail to non-structural, and head to tail genes. These analyses are limited to genes that pass the aqua test; similar results are found without this restriction.</p>", "links"=>[], "tags"=>["codon", "usage", "refined"], "article_id"=>607019, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.t004", "stats"=>{"downloads"=>5, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_between_codon_usage_and_refined_structural_annotations_/607019", "title"=>"Comparison between codon usage and refined structural annotations.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-02-29 01:56:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/935919"], "description"=>"<p>(A) Shows GC3 and (B) shows CAI landscapes. In between successive snapshots (labeled by integers), <i>N</i> synonymous mutations are introduced into the genome and the resulting landscape is shown, where <i>N</i> is the number of codons in the lambda phage genome (see the Genome Landscapes section). These snapshots show that the simulated genome landscapes approach the random null model, indicated by the purple band (see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi-1000001-g001\" target=\"_blank\">Figure 1</a>). The final CAI landscape (3) lies almost completely within the purple band. Using the lambda phage mutation rate of 7.7×10<sup>−8</sup> mutations/bp/replication <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1000001#pcbi.1000001-Drake1\" target=\"_blank\">[57]</a>, we can estimate that approximately 10<sup>7</sup> genome replications would be required to relax within the purple bars.</p>", "links"=>[], "tags"=>["simulated", "synonymous", "mutation", "lambda", "phage"], "article_id"=>606361, "categories"=>["Infectious Diseases", "Virology"], "users"=>["Julius B. Lucks", "David R. Nelson", "Grzegorz R. Kudla", "Joshua B. Plotkin"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1000001.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Snapshots_of_simulated_synonymous_mutation_in_the_lambda_phage_genome_/606361", "title"=>"Snapshots of simulated synonymous mutation in the lambda phage genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-02-29 01:46:01"}

PMC Usage Stats | Further Information

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  • {"scanned-page-browse"=>"0", "month"=>"4", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"9", "unique-ip"=>"9", "pdf"=>"6", "year"=>"2010", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"5", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"5", "year"=>"2010", "pdf"=>"6", "unique-ip"=>"5", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"scanned-page-browse"=>"0", "month"=>"6", "cited-by"=>"0", "abstract"=>"1", "full-text"=>"7", "unique-ip"=>"8", "pdf"=>"4", "year"=>"2010", "figure"=>"2", "scanned-summary"=>"0", "supp-data"=>"0"}
  • {"month"=>"7", "scanned-page-browse"=>"0", "cited-by"=>"0", "abstract"=>"0", "full-text"=>"5", "year"=>"2010", "pdf"=>"3", "unique-ip"=>"6", "figure"=>"0", "scanned-summary"=>"0", "supp-data"=>"0"}
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Relative Metric

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