Global Patterns of Protein Domain Gain and Loss in Superkingdoms
Publication Date
January 30, 2014
Journal
PLoS Computational Biology
Authors
Arshan Nasir, Kyung Mo Kim & Gustavo Caetano-Anollés
Volume
10
Issue
1
Pages
e1003452
DOI
https://dx.plos.org/10.1371/journal.pcbi.1003452
Publisher URL
http://journals.plos.org/ploscompbiol/article?id=10.1371%2Fjournal.pcbi.1003452
Web of Science
000337948500049
Scopus
84896722637
Mendeley
http://www.mendeley.com/research/global-patterns-protein-domain-gain-loss-superkingdoms-3
Events
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Mendeley | Further Information

{"title"=>"Global Patterns of Protein Domain Gain and Loss in Superkingdoms", "type"=>"journal", "authors"=>[{"first_name"=>"Arshan", "last_name"=>"Nasir", "scopus_author_id"=>"54787967600"}, {"first_name"=>"Kyung Mo", "last_name"=>"Kim", "scopus_author_id"=>"36101192800"}, {"first_name"=>"Gustavo", "last_name"=>"Caetano-Anollés", "scopus_author_id"=>"56269658000"}], "year"=>2014, "source"=>"PLoS Computational Biology", "identifiers"=>{"doi"=>"10.1371/journal.pcbi.1003452", "sgr"=>"84896722637", "isbn"=>"1553-734X", "pmid"=>"24499935", "issn"=>"1553734X", "scopus"=>"2-s2.0-84896722637", "pui"=>"372348767"}, "id"=>"5fd4cd03-d2a8-3d7a-993c-ef20b718bd25", "abstract"=>"Domains are modules within proteins that can fold and function independently and are evolutionarily conserved. Here we compared the usage and distribution of protein domain families in the free-living proteomes of Archaea, Bacteria and Eukarya and reconstructed species phylogenies while tracing the history of domain emergence and loss in proteomes. We show that both gains and losses of domains occurred frequently during proteome evolution. The rate of domain discovery increased approximately linearly in evolutionary time. Remarkably, gains generally outnumbered losses and the gain-to-loss ratios were much higher in akaryotes compared to eukaryotes. Functional annotations of domain families revealed that both Archaea and Bacteria gained and lost metabolic capabilities during the course of evolution while Eukarya acquired a number of diverse molecular functions including those involved in extracellular processes, immunological mechanisms, and cell regulation. Results also highlighted significant contemporary sharing of informational enzymes between Archaea and Eukarya and metabolic enzymes between Bacteria and Eukarya. Finally, the analysis provided useful insights into the evolution of species. The archaeal superkingdom appeared first in evolution by gradual loss of ancestral domains, bacterial lineages were the first to gain superkingdom-specific domains, and eukaryotes (likely) originated when an expanding proto-eukaryotic stem lineage gained organelles through endosymbiosis of already diversified bacterial lineages. The evolutionary dynamics of domain families in proteomes and the increasing number of domain gains is predicted to redefine the persistence strategies of organisms in superkingdoms, influence the make up of molecular functions, and enhance organismal complexity by the generation of new domain architectures. This dynamics highlights ongoing secondary evolutionary adaptations in akaryotic microbes, especially Archaea.", "link"=>"http://www.mendeley.com/research/global-patterns-protein-domain-gain-loss-superkingdoms-3", "reader_count"=>60, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>20, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>22, "Student > Master"=>8, "Lecturer"=>3, "Professor"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>20, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>22, "Student > Master"=>8, "Lecturer"=>3, "Professor"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>14, "Agricultural and Biological Sciences"=>35, "Medicine and Dentistry"=>1, "Computer Science"=>5, "Linguistics"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>35}, "Computer Science"=>{"Computer Science"=>5}, "Linguistics"=>{"Linguistics"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>14}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Canada"=>2, "United States"=>1, "Finland"=>1, "Brazil"=>1, "Mexico"=>1, "United Kingdom"=>1, "Italy"=>1, "Malaysia"=>1, "France"=>1, "Spain"=>1, "India"=>2, "Indonesia"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1368206"], "description"=>"<p>GO accessions, names and <i>P</i>-values for highly-specific biological processes that were significantly associated (FDR<0.01) with FF gains in Archaea, Bacteria, and Eukarya.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "names", "highly-specific", "processes", "ff", "gains"], "article_id"=>919454, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.t004", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GO_accessions_names_and_P_values_for_highly_specific_biological_processes_that_were_significantly_associated_FDR_/919454", "title"=>"GO accessions, names and <i>P</i>-values for highly-specific biological processes that were significantly associated (FDR<0.01) with FF gains in Archaea, Bacteria, and Eukarya.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368203"], "description"=>"<p>The superscripts identify individual species.</p>1<p><i>Staphylothermus marinus,</i></p>2<p><i>Methanosarcina acetovirans,</i></p>3<p><i>Thermoplasma volcanium,</i></p>4<p><i>Haloarcula marismortui,</i></p>5<p><i>Dehalococcoides sp.,</i></p>6<p><i>Citrobacter koseri,</i></p>7<p><i>Burkholderia xenovorans,</i></p>8<p><i>Nitratiruptor sp.,</i></p>9<p><i>Rhodococcus sp.,</i></p>10<p><i>Paramecium tetraurelia,</i></p>11<p><i>Homo sapiens,</i></p>12<p><i>Malassezia globosa,</i></p>13<p><i>Takifugu rubripes.</i></p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "proteomes", "median", "counts", "abundance", "ffs"], "article_id"=>919451, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Descriptive_statistics_on_the_total_number_of_proteomes_N_minimum_min_maximum_max_and_median_values_for_raw_counts_of_occurrence_abundance_and_ratio_of_FFs_in_each_superkingdom_/919451", "title"=>"Descriptive statistics on the total number of proteomes (<i>N</i>), minimum (<i>min</i>), maximum (<i>max</i>) and median values for raw counts of occurrence, abundance and ratio of FFs in each superkingdom.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368202"], "description"=>"<p>Names, SCOP <i>css</i>, and <i>f</i>-value of informational FF domains present in the AE taxonomic group. FFs are sorted by <i>f</i>-value in a descending manner.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "scop", "informational", "ff", "domains", "ae", "taxonomic", "ffs", "sorted", "descending"], "article_id"=>919450, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.t002", "stats"=>{"downloads"=>5, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Names_SCOP_css_and_f_value_of_informational_FF_domains_present_in_the_AE_taxonomic_group_FFs_are_sorted_by_f_value_in_a_descending_manner_/919450", "title"=>"Names, SCOP <i>css</i>, and <i>f</i>-value of informational FF domains present in the AE taxonomic group. FFs are sorted by <i>f</i>-value in a descending manner.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368192"], "description"=>"<p>A) A Venn diagram describes the distribution of FFs in the seven taxonomic groups (reproduced from <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003452#pcbi.1003452-Kim2\" target=\"_blank\">[27]</a>) B) Boxplots represent the distributions of domain ages (<i>nd</i>) for each taxonomic group. Numbers within each distribution indicate group medians, hollow circles the outliers, while the shaded regions identify important evolutionary epochs. Geological time (Gy) was inferred from a molecular clock of protein folds <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003452#pcbi.1003452-Wang4\" target=\"_blank\">[51]</a>, <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003452#pcbi.1003452-CaetanoAnolls5\" target=\"_blank\">[52]</a>. FFs were identified by SCOP <i>css</i>: c.37.1.12, ABC transporter ATPase domain-like; d.122.1.1, Heat shock protein 90, HSP 90, N-terminal domain; c.116.1.4, tRNA(m1G37)-methyltransferase TrmD; g.3.10.1, Colipase-like; a.4.5.41, Transcription factor E/IIe-alpha, N-terminal domain. C) Boxplots represent the distribution index (<i>f</i>-value) of FF domains for each taxonomic group. Numbers within each distribution indicate group medians. Hollow circles represent outliers. D) A 3D scatter plot describes the persistence strategies of Archaea (red), Bacteria (blue), and Eukarya (green). All axes are in logarithmic scale. Numbers in parenthesis indicate total number of proteomes available for study in each superkingdom.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "ffs", "organismal", "persistence"], "article_id"=>919440, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.g001", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_dynamics_of_FFs_and_organismal_persistence_strategies_/919440", "title"=>"Evolutionary dynamics of FFs and organismal persistence strategies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368204"], "description"=>"<p>No significant biological process was lost in either Archaea or Eukarya.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "names", "highly-specific", "processes", "ff"], "article_id"=>919452, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.t005", "stats"=>{"downloads"=>4, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GO_accessions_names_and_P_values_for_highly_specific_biological_processes_that_were_significantly_associated_FDR_/919452", "title"=>"GO accessions, names and <i>P</i>-values for highly-specific biological processes that were significantly associated (FDR<0.01) with FF loss in Bacteria.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368201"], "description"=>"<p>FFs are sorted by <i>nd</i> value in an ascending manner.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "scop", "id", "evolutionary", "ffs", "keyword", "dataset", "ff"], "article_id"=>919449, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.t003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Names_SCOP_Id_and_css_and_evolutionary_age_nd_of_FFs_that_were_identified_by_keyword_search_Mitochondria_on_the_dataset_of_2_397_FF_domains_/919449", "title"=>"Names, SCOP Id and <i>css</i>, and evolutionary age (<i>nd</i>) of FFs that were identified by keyword search ‘Mitochondria’ on the dataset of 2,397 FF domains.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368199"], "description"=>"<p>Scatter plots reveal an approximately linear trend in the accumulation of FF gains and losses in both the global analysis (A) and in individual superkingdoms (B). Gains are identified in red while losses in blue. The three evolutionary epochs are marked with corresponding gain-to-loss ratios in italics.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "numbers", "gains"], "article_id"=>919447, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cumulative_numbers_of_gains_and_losses_/919447", "title"=>"Cumulative numbers of gains and losses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368200"], "description"=>"<p>Boxplots comparing the distribution of net gains and losses in 100 random phylogenetic trees for both <i>abundance</i> (A) and <i>occurrence</i> (B). Numbers in parentheses indicate group median values.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "sampling"], "article_id"=>919448, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Equal_sampling_of_proteomes_/919448", "title"=>"Equal sampling of proteomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368198"], "description"=>"<p>A) Sum of gains and losses for each FF domain is represented in boxplots for <i>Total</i>, <i>Archaea</i>, <i>Bacteria</i>, and <i>Eukarya</i> reconstructions using <i>abundance</i> and <i>occurrence</i> models. Numbers in parentheses indicate total number of parsimony informative characters in each analysis. A horizontal red line passes through zero on the <i>x</i>-axis. B) Histograms comparing the relative counts of gains and losses for each FF domain character, plotted on the <i>nd</i> scale. Bars in red and blue indicate gains and losses respectively. The global gain-to-loss ratios are listed along with the total number of gain and loss events and gain-to-loss ratios. <i>n</i> is the number of parsimony informative characters in each analysis. C) Histograms comparing the distribution of FF gains and losses in <i>Archaea</i>, <i>Bacteria</i> and <i>Eukarya</i>. Bars in red and blue indicate gains and losses respectively. The <i>x</i>-axes indicates evolutionary time. Numbers in parenthesis indicate total number of proteomes in each dataset.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "patterns", "gains", "losses"], "article_id"=>919446, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.g004", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_patterns_of_gains_and_losses_in_superkingdoms_/919446", "title"=>"Global patterns of gains and losses in superkingdoms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368195"], "description"=>"<p>A) A ToL reconstructed from the genomic abundance counts of 2,397 FF domains (2,262 parsimony informative, tree length = 128,752, RI = 0.76, <i>g<sub>1</sub></i> = −0.33) describing the evolution of 420 free-living organisms. Values on branches indicate bootstrap support values. Taxa were colored red for Archaea, blue for Bacteria and green for Eukarya. B) A ToL reconstructed from the presence/absence of 2,397 FF domains (2,249 parsimony informative, tree length = 30,599, RI = 0.79, <i>g<sub>1</sub></i> = −0.28) describing the evolution of 420 free-living organisms. Values on branches indicate bootstrap support values. Taxa are colored as in A. Difference between trees was calculated using the nodal module of TOPD/FMTS package <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003452#pcbi.1003452-Puigbo1\" target=\"_blank\">[50]</a>.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "patterns"], "article_id"=>919443, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenomic_patterns_in_the_three_superkingdoms_/919443", "title"=>"Phylogenomic patterns in the three superkingdoms.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368194"], "description"=>"<p>A) Stacked bar plots describe the distribution of molecular functions in each of the seven taxonomic groups. The size of each bar is proportional to the percentage of FF domains in each functional category, while the numbers indicate total counts of FFs annotated in that category. B–H) Scatter plots illustrate the emergence of molecular functions in taxonomic groups. The <i>x</i>-axes represents evolutionary time (<i>nd</i>), while the <i>y</i>-axes indicate the distribution index (<i>f</i>-value) of FFs. Evolutionary epochs identified as previously. Numbers in parenthesis indicate total number of FF domains in each taxonomic group for which SUPERFAMILY functional annotations (based on SCOP 1.73) were available.</p>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "annotation", "ff"], "article_id"=>919442, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1003452.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_annotation_of_FF_domains_/919442", "title"=>"Functional annotation of FF domains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-01-30 03:39:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1368207", "https://ndownloader.figshare.com/files/1368208", "https://ndownloader.figshare.com/files/1368209", "https://ndownloader.figshare.com/files/1368210"], "description"=>"<div><p>Domains are modules within proteins that can fold and function independently and are evolutionarily conserved. Here we compared the usage and distribution of protein domain families in the free-living proteomes of Archaea, Bacteria and Eukarya and reconstructed species phylogenies while tracing the history of domain emergence and loss in proteomes. We show that both gains and losses of domains occurred frequently during proteome evolution. The rate of domain discovery increased approximately linearly in evolutionary time. Remarkably, gains generally outnumbered losses and the gain-to-loss ratios were much higher in akaryotes compared to eukaryotes. Functional annotations of domain families revealed that both Archaea and Bacteria gained and lost metabolic capabilities during the course of evolution while Eukarya acquired a number of diverse molecular functions including those involved in extracellular processes, immunological mechanisms, and cell regulation. <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1003452#s3\" target=\"_blank\">Results</a> also highlighted significant contemporary sharing of informational enzymes between Archaea and Eukarya and metabolic enzymes between Bacteria and Eukarya. Finally, the analysis provided useful insights into the evolution of species. The archaeal superkingdom appeared first in evolution by gradual loss of ancestral domains, bacterial lineages were the first to gain superkingdom-specific domains, and eukaryotes (likely) originated when an expanding proto-eukaryotic stem lineage gained organelles through endosymbiosis of already diversified bacterial lineages. The evolutionary dynamics of domain families in proteomes and the increasing number of domain gains is predicted to redefine the persistence strategies of organisms in superkingdoms, influence the make up of molecular functions, and enhance organismal complexity by the generation of new domain architectures. This dynamics highlights ongoing secondary evolutionary adaptations in akaryotic microbes, especially Archaea.</p></div>", "links"=>[], "tags"=>["Computational biology", "genomics", "Genome evolution", "patterns"], "article_id"=>919455, "categories"=>["Biological Sciences"], "users"=>["Arshan Nasir", "Kyung Mo Kim", "Gustavo Caetano-Anollés"], "doi"=>["https://dx.doi.org/10.1371/journal.pcbi.1003452.s001", "https://dx.doi.org/10.1371/journal.pcbi.1003452.s002", "https://dx.doi.org/10.1371/journal.pcbi.1003452.s003", "https://dx.doi.org/10.1371/journal.pcbi.1003452.s004"], "stats"=>{"downloads"=>10, "page_views"=>33, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Global_Patterns_of_Protein_Domain_Gain_and_Loss_in_Superkingdoms_/919455", "title"=>"Global Patterns of Protein Domain Gain and Loss in Superkingdoms", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-01-30 03:39:36"}

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Relative Metric

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