Functional Tradeoffs Underpin Salinity-Driven Divergence in Microbial Community Composition
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{"title"=>"Functional tradeoffs underpin salinity-driven divergence in microbial community composition", "type"=>"journal", "authors"=>[{"first_name"=>"Chris L.", "last_name"=>"Dupont", "scopus_author_id"=>"7201415188"}, {"first_name"=>"John", "last_name"=>"Larsson", "scopus_author_id"=>"36608189500"}, {"first_name"=>"Shibu", "last_name"=>"Yooseph", "scopus_author_id"=>"6602156903"}, {"first_name"=>"Karolina", "last_name"=>"Ininbergs", "scopus_author_id"=>"36608282600"}, {"first_name"=>"Johannes", "last_name"=>"Goll", "scopus_author_id"=>"15022394300"}, {"first_name"=>"Johannes", "last_name"=>"Asplund-Samuelsson", "scopus_author_id"=>"55498292900"}, {"first_name"=>"John P.", "last_name"=>"McCrow", "scopus_author_id"=>"36028518900"}, {"first_name"=>"Narin", "last_name"=>"Celepli", "scopus_author_id"=>"55850674000"}, {"first_name"=>"Lisa Zeigler", "last_name"=>"Allen", "scopus_author_id"=>"37090343200"}, {"first_name"=>"Martin", "last_name"=>"Ekman", "scopus_author_id"=>"7007060953"}, {"first_name"=>"Andrew J.", "last_name"=>"Lucas", "scopus_author_id"=>"7201925660"}, {"first_name"=>"Åke", "last_name"=>"Hagström", "scopus_author_id"=>"7004151979"}, {"first_name"=>"Mathangi", "last_name"=>"Thiagarajan", "scopus_author_id"=>"12139676500"}, {"first_name"=>"Björn", "last_name"=>"Brindefalk", "scopus_author_id"=>"16028157000"}, {"first_name"=>"Alexander R.", "last_name"=>"Richter", "scopus_author_id"=>"12776560300"}, {"first_name"=>"Anders F.", "last_name"=>"Andersson", "scopus_author_id"=>"16052100600"}, {"first_name"=>"Aaron", "last_name"=>"Tenney", "scopus_author_id"=>"8316397800"}, {"first_name"=>"Daniel", "last_name"=>"Lundin", "scopus_author_id"=>"24173634500"}, {"first_name"=>"Andrey", "last_name"=>"Tovchigrechko", "scopus_author_id"=>"14219750600"}, {"first_name"=>"Johan A.A.", "last_name"=>"Nylander", "scopus_author_id"=>"6603105489"}, {"first_name"=>"Daniel", "last_name"=>"Brami", "scopus_author_id"=>"53363172500"}, {"first_name"=>"Jonathan H.", "last_name"=>"Badger", "scopus_author_id"=>"35232327400"}, {"first_name"=>"Andrew E.", "last_name"=>"Allen", "scopus_author_id"=>"7402802528"}, {"first_name"=>"Douglas B.", "last_name"=>"Rusch", "scopus_author_id"=>"7004630429"}, {"first_name"=>"Jeff", "last_name"=>"Hoffman", "scopus_author_id"=>"55420112000"}, {"first_name"=>"Erling", "last_name"=>"Norrby", "scopus_author_id"=>"16073667100"}, {"first_name"=>"Robert", "last_name"=>"Friedman", "scopus_author_id"=>"7401990376"}, {"first_name"=>"Jarone", "last_name"=>"Pinhassi", "scopus_author_id"=>"6603458504"}, {"first_name"=>"J. Craig", "last_name"=>"Venter", "scopus_author_id"=>"35352327000"}, {"first_name"=>"Birgitta", "last_name"=>"Bergman", "scopus_author_id"=>"7201889583"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"24586863", "doi"=>"10.1371/journal.pone.0089549", "sgr"=>"84897894862", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "scopus"=>"2-s2.0-84897894862", "issn"=>"19326203", "pui"=>"372609711"}, "id"=>"d879394c-1a64-3ef8-9152-25946da1215b", "abstract"=>"Bacterial community composition and functional potential change subtly across gradients in the surface ocean. In contrast, while there are significant phylogenetic divergences between communities from freshwater and marine habitats, the underlying mechanisms to this phylogenetic structuring yet remain unknown. We hypothesized that the functional potential of natural bacterial communities is linked to this striking divide between microbiomes. To test this hypothesis, metagenomic sequencing of microbial communities along a 1,800 km transect in the Baltic Sea area, encompassing a continuous natural salinity gradient from limnic to fully marine conditions, was explored. Multivariate statistical analyses showed that salinity is the main determinant of dramatic changes in microbial community composition, but also of large scale changes in core metabolic functions of bacteria. Strikingly, genetically and metabolically different pathways for key metabolic processes, such as respiration, biosynthesis of quinones and isoprenoids, glycolysis and osmolyte transport, were differentially abundant at high and low salinities. These shifts in functional capacities were observed at multiple taxonomic levels and within dominant bacterial phyla, while bacteria, such as SAR11, were able to adapt to the entire salinity gradient. We propose that the large differences in central metabolism required at high and low salinities dictate the striking divide between freshwater and marine microbiomes, and that the ability to inhabit different salinity regimes evolved early during bacterial phylogenetic differentiation. These findings significantly advance our understanding of microbial distributions and stress the need to incorporate salinity in future climate change models that predict increased levels of precipitation and a reduction in salinity.", "link"=>"http://www.mendeley.com/research/functional-tradeoffs-underpin-salinitydriven-divergence-microbial-community-composition", "reader_count"=>134, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>34, "Student > Doctoral Student"=>10, "Student > Ph. D. Student"=>47, "Student > Postgraduate"=>5, "Student > Master"=>16, "Other"=>4, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>34, "Student > Doctoral Student"=>10, "Student > Ph. D. Student"=>47, "Student > Postgraduate"=>5, "Student > Master"=>16, "Other"=>4, "Student > Bachelor"=>6, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Agricultural and Biological Sciences"=>75, "Chemistry"=>1, "Computer Science"=>2, "Earth and Planetary Sciences"=>8, "Engineering"=>1, "Environmental Science"=>14, "Biochemistry, Genetics and Molecular Biology"=>16, "Materials Science"=>2, "Mathematics"=>2, "Medicine and Dentistry"=>3, "Physics and Astronomy"=>1, "Immunology and Microbiology"=>4}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>2}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Mathematics"=>{"Mathematics"=>2}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>14}, "Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>8}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>75}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>16}}, "reader_count_by_country"=>{"Canada"=>1, "Sweden"=>2, "Hong Kong"=>1, "United States"=>5, "Brazil"=>1, "United Kingdom"=>2, "France"=>1, "Germany"=>1, "Spain"=>1}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1402235"], "description"=>"<p>A) KEGG module and metadata correlations with first and second canonical variates for the bacterial communities in combined size fractions. Text labels and associated arrows indicate the position of analogous modules shown in panel B. The outer circle (1) and inner circles (0.5) display the amount of variance explained by the linear combinations of variables. The variance explained for points within the inner circle is less than 25%, thus these have been dimmed. Biplots for each size fraction and the combined communities are shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089549#pone.0089549.s006\" target=\"_blank\">fig. S6</a>. B) Plots showing the distribution of analogous central metabolic pathways highlighted in panel A along the salinity gradient. Note that the spermidine transport system (‘Sp.’) is not shown in panel A due to its non-normal distribution.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Metabolic pathways", "ecology", "Ecological environments", "Marine environments", "Freshwater ecology", "microbial ecology", "Evolutionary biology", "Evolutionary systematics", "taxonomy", "Microbial taxonomy", "phylogenetics", "genomics", "Functional genomics", "metagenomics", "Marine biology", "Marine ecology", "microbiology", "bacteriology", "Bacterial taxonomy", "Bacterial evolution", "Microbial evolution", "Microbial physiology", "marine and aquatic sciences"], "article_id"=>947544, "categories"=>["Biological Sciences"], "users"=>["Chris L. Dupont", "John Larsson", "Shibu Yooseph", "Karolina Ininbergs", "Johannes Goll", "Johannes Asplund-Samuelsson", "John P. McCrow", "Narin Celepli", "Lisa Zeigler Allen", "Martin Ekman", "Andrew J. Lucas", "Åke Hagström", "Mathangi Thiagarajan", "Björn Brindefalk", "Alexander R. Richter", "Anders F. Andersson", "Aaron Tenney", "Daniel Lundin", "Andrey Tovchigrechko", "Johan A. A. Nylander", "Daniel Brami", "Jonathan H. Badger", "Andrew E. Allen", "Douglas B. Rusch", "Jeff Hoffman", "Erling Norrby", "Robert Friedman", "Jarone Pinhassi", "J. Craig Venter", "Birgitta Bergman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089549.g003", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Salinity_and_functional_potential_/947544", "title"=>"Salinity and functional potential.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-27 04:12:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1402233"], "description"=>"<p>A) Bacterial communities characterized by AMPHORA2. The 12 most abundant groups are shown with “Other” defined as the remaining taxonomic groups. Sequences have been combined for all non-viral size fractions (0.1, 0.8 and 3.0 µm) with normalization for genome equivalents. Sampling depth (m) is indicated within circles below sample names, with interconnecting circles indicating samples from the same location. The corresponding basin for samples is shown in the top margin: TT = Torne Träsk, BB = Bothnian Bay, BS = Bothnian Sea, BP = Baltic Proper, BW = Baltic West. A merged set of metagenomes from the coastal eastern Pacific (CalCOFI) was included for comparison. B) RCCA analysis of community composition. The biplot shows correlations between environmental (red) and phylogenetic (color coded by superkingdom) variables with the corresponding first and second canonical variates. The first two canonical variates explain 65% of the environmental variables and 49% of the organismal variables. Biplots for a RCCA at the genus level is shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089549#pone.0089549.s005\" target=\"_blank\">figure S5</a>. The outer circle (1) and inner circles (0.5) display the amount of variance explained by the linear combinations of variables. The variance explained for points within the inner circle is less than 25%, thus these have been dimmed.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Metabolic pathways", "ecology", "Ecological environments", "Marine environments", "Freshwater ecology", "microbial ecology", "Evolutionary biology", "Evolutionary systematics", "taxonomy", "Microbial taxonomy", "phylogenetics", "genomics", "Functional genomics", "metagenomics", "Marine biology", "Marine ecology", "microbiology", "bacteriology", "Bacterial taxonomy", "Bacterial evolution", "Microbial evolution", "Microbial physiology", "marine and aquatic sciences", "shifts", "bacterial"], "article_id"=>947542, "categories"=>["Biological Sciences"], "users"=>["Chris L. Dupont", "John Larsson", "Shibu Yooseph", "Karolina Ininbergs", "Johannes Goll", "Johannes Asplund-Samuelsson", "John P. McCrow", "Narin Celepli", "Lisa Zeigler Allen", "Martin Ekman", "Andrew J. Lucas", "Åke Hagström", "Mathangi Thiagarajan", "Björn Brindefalk", "Alexander R. Richter", "Anders F. Andersson", "Aaron Tenney", "Daniel Lundin", "Andrey Tovchigrechko", "Johan A. A. Nylander", "Daniel Brami", "Jonathan H. Badger", "Andrew E. Allen", "Douglas B. Rusch", "Jeff Hoffman", "Erling Norrby", "Robert Friedman", "Jarone Pinhassi", "J. Craig Venter", "Birgitta Bergman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089549.g002", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Salinity_driven_shifts_in_bacterial_community_composition_/947542", "title"=>"Salinity-driven shifts in bacterial community composition.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-27 04:12:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1402224"], "description"=>"<p>A) Squares with red outlines indicate sites with metagenomic sequencing. 16S rRNA gene tag sequencing was conducted at all sites. B) Temperature, salinity, pH, oxygen, and chlorophyll a measurements across the Baltic Sea transect. Only stations shown on the section were used for section interpolation. The transition from limnic to marine conditions along the 1800 km axis of the Baltic Sea leads to an extensive area of slowly varying brackish conditions. Suboxic, low-pH conditions exist throughout the central basin below 50–60 m. All environmental metadata is in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089549#pone.0089549.s011\" target=\"_blank\">table S1</a>. Sub-basin abbreviations are marked on the map in bold font (BB – Bothnian Bay, BS – Bothnian Sea, BP – Baltic Proper, BW – Baltic West).</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Metabolic pathways", "ecology", "Ecological environments", "Marine environments", "Freshwater ecology", "microbial ecology", "Evolutionary biology", "Evolutionary systematics", "taxonomy", "Microbial taxonomy", "phylogenetics", "genomics", "Functional genomics", "metagenomics", "Marine biology", "Marine ecology", "microbiology", "bacteriology", "Bacterial taxonomy", "Bacterial evolution", "Microbial evolution", "Microbial physiology", "marine and aquatic sciences", "baltic", "sampling"], "article_id"=>947540, "categories"=>["Biological Sciences"], "users"=>["Chris L. Dupont", "John Larsson", "Shibu Yooseph", "Karolina Ininbergs", "Johannes Goll", "Johannes Asplund-Samuelsson", "John P. McCrow", "Narin Celepli", "Lisa Zeigler Allen", "Martin Ekman", "Andrew J. Lucas", "Åke Hagström", "Mathangi Thiagarajan", "Björn Brindefalk", "Alexander R. Richter", "Anders F. Andersson", "Aaron Tenney", "Daniel Lundin", "Andrey Tovchigrechko", "Johan A. A. Nylander", "Daniel Brami", "Jonathan H. Badger", "Andrew E. Allen", "Douglas B. Rusch", "Jeff Hoffman", "Erling Norrby", "Robert Friedman", "Jarone Pinhassi", "J. Craig Venter", "Birgitta Bergman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089549.g001", "stats"=>{"downloads"=>3, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Baltic_Sea_region_and_sampling_locations_/947540", "title"=>"The Baltic Sea region and sampling locations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-27 04:12:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1402236"], "description"=>"<p>A) Metagenomic sequences classified as SAR11 placed onto a reference tree built from 31 concatenated core genes (see Methods). The Rickettsiales sister group (not shown for clarity) of <i>Candidatus</i> Pelagibacter was chosen as outgroup from AMPHORA2 reference trees. Terminal branches are colored according to the legend in the left margin. Sequences with likelihood weights<0.9 were pruned from the tree. Branches corresponding to sequences from the freshwater Lake Gatun and coastal California metagenomes are colored purple and dark blue, respectively. Numbers in the boxes indicate salinity (PSU). B) Functional differences between the low and high salinity SAR11 populations. Plot of differences in KEGG categories related to biosynthesis (“Synthesis”) and transport (“Transport”) of amino acids, nucleotides and cofactors. Bar plots show mean proportions for each category in the different populations and the confidence interval. Welch's t-test p-values (corrected using the Bonferroni method) are shown in the right margin of the plot.</p>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Metabolic pathways", "ecology", "Ecological environments", "Marine environments", "Freshwater ecology", "microbial ecology", "Evolutionary biology", "Evolutionary systematics", "taxonomy", "Microbial taxonomy", "phylogenetics", "genomics", "Functional genomics", "metagenomics", "Marine biology", "Marine ecology", "microbiology", "bacteriology", "Bacterial taxonomy", "Bacterial evolution", "Microbial evolution", "Microbial physiology", "marine and aquatic sciences", "sar11", "phylogeny"], "article_id"=>947545, "categories"=>["Biological Sciences"], "users"=>["Chris L. Dupont", "John Larsson", "Shibu Yooseph", "Karolina Ininbergs", "Johannes Goll", "Johannes Asplund-Samuelsson", "John P. McCrow", "Narin Celepli", "Lisa Zeigler Allen", "Martin Ekman", "Andrew J. Lucas", "Åke Hagström", "Mathangi Thiagarajan", "Björn Brindefalk", "Alexander R. Richter", "Anders F. Andersson", "Aaron Tenney", "Daniel Lundin", "Andrey Tovchigrechko", "Johan A. A. Nylander", "Daniel Brami", "Jonathan H. Badger", "Andrew E. Allen", "Douglas B. Rusch", "Jeff Hoffman", "Erling Norrby", "Robert Friedman", "Jarone Pinhassi", "J. Craig Venter", "Birgitta Bergman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0089549.g004", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Baltic_Sea_SAR11_phylogeny_and_function_/947545", "title"=>"Baltic Sea SAR11 phylogeny and function.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-02-27 04:12:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/1402243", "https://ndownloader.figshare.com/files/1402244", "https://ndownloader.figshare.com/files/1402245", "https://ndownloader.figshare.com/files/1402246", "https://ndownloader.figshare.com/files/1402247", "https://ndownloader.figshare.com/files/1402248", "https://ndownloader.figshare.com/files/1402249", "https://ndownloader.figshare.com/files/1402250", "https://ndownloader.figshare.com/files/1402251", "https://ndownloader.figshare.com/files/1402252", "https://ndownloader.figshare.com/files/1402253", "https://ndownloader.figshare.com/files/1402254", "https://ndownloader.figshare.com/files/1402255", "https://ndownloader.figshare.com/files/1402256"], "description"=>"<div><p>Bacterial community composition and functional potential change subtly across gradients in the surface ocean. In contrast, while there are significant phylogenetic divergences between communities from freshwater and marine habitats, the underlying mechanisms to this phylogenetic structuring yet remain unknown. We hypothesized that the functional potential of natural bacterial communities is linked to this striking divide between microbiomes. To test this hypothesis, metagenomic sequencing of microbial communities along a 1,800 km transect in the Baltic Sea area, encompassing a continuous natural salinity gradient from limnic to fully marine conditions, was explored. Multivariate statistical analyses showed that salinity is the main determinant of dramatic changes in microbial community composition, but also of large scale changes in core metabolic functions of bacteria. Strikingly, genetically and metabolically different pathways for key metabolic processes, such as respiration, biosynthesis of quinones and isoprenoids, glycolysis and osmolyte transport, were differentially abundant at high and low salinities. These shifts in functional capacities were observed at multiple taxonomic levels and within dominant bacterial phyla, while bacteria, such as SAR11, were able to adapt to the entire salinity gradient. We propose that the large differences in central metabolism required at high and low salinities dictate the striking divide between freshwater and marine microbiomes, and that the ability to inhabit different salinity regimes evolved early during bacterial phylogenetic differentiation. These findings significantly advance our understanding of microbial distributions and stress the need to incorporate salinity in future climate change models that predict increased levels of precipitation and a reduction in salinity.</p></div>", "links"=>[], "tags"=>["Biochemistry", "metabolism", "Metabolic pathways", "ecology", "Ecological environments", "Marine environments", "Freshwater ecology", "microbial ecology", "Evolutionary biology", "Evolutionary systematics", "taxonomy", "Microbial taxonomy", "phylogenetics", "genomics", "Functional genomics", "metagenomics", "Marine biology", "Marine ecology", "microbiology", "bacteriology", "Bacterial taxonomy", "Bacterial evolution", "Microbial evolution", "Microbial physiology", "marine and aquatic sciences", "tradeoffs", "underpin", "salinity-driven", "divergence", "microbial"], "article_id"=>947551, "categories"=>["Biological Sciences"], "users"=>["Chris L. Dupont", "John Larsson", "Shibu Yooseph", "Karolina Ininbergs", "Johannes Goll", "Johannes Asplund-Samuelsson", "John P. McCrow", "Narin Celepli", "Lisa Zeigler Allen", "Martin Ekman", "Andrew J. Lucas", "Åke Hagström", "Mathangi Thiagarajan", "Björn Brindefalk", "Alexander R. Richter", "Anders F. Andersson", "Aaron Tenney", "Daniel Lundin", "Andrey Tovchigrechko", "Johan A. A. Nylander", "Daniel Brami", "Jonathan H. Badger", "Andrew E. Allen", "Douglas B. Rusch", "Jeff Hoffman", "Erling Norrby", "Robert Friedman", "Jarone Pinhassi", "J. Craig Venter", "Birgitta Bergman"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0089549.s001", "https://dx.doi.org/10.1371/journal.pone.0089549.s002", "https://dx.doi.org/10.1371/journal.pone.0089549.s003", "https://dx.doi.org/10.1371/journal.pone.0089549.s004", "https://dx.doi.org/10.1371/journal.pone.0089549.s005", "https://dx.doi.org/10.1371/journal.pone.0089549.s006", "https://dx.doi.org/10.1371/journal.pone.0089549.s007", "https://dx.doi.org/10.1371/journal.pone.0089549.s008", "https://dx.doi.org/10.1371/journal.pone.0089549.s009", "https://dx.doi.org/10.1371/journal.pone.0089549.s010", "https://dx.doi.org/10.1371/journal.pone.0089549.s011", "https://dx.doi.org/10.1371/journal.pone.0089549.s012", "https://dx.doi.org/10.1371/journal.pone.0089549.s013", "https://dx.doi.org/10.1371/journal.pone.0089549.s014"], "stats"=>{"downloads"=>116, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_Tradeoffs_Underpin_Salinity_Driven_Divergence_in_Microbial_Community_Composition_/947551", "title"=>"Functional Tradeoffs Underpin Salinity-Driven Divergence in Microbial Community Composition", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-02-27 04:12:09"}

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