The Emergence and Early Evolution of Biological Carbon-Fixation
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{"title"=>"The emergence and early evolution of biological carbon-fixation", "type"=>"journal", "authors"=>[{"first_name"=>"Rogier", "last_name"=>"Braakman", "scopus_author_id"=>"24167681300"}, {"first_name"=>"Eric", "last_name"=>"Smith", "scopus_author_id"=>"55722926600"}], "year"=>2012, "source"=>"PLoS Computational Biology", "identifiers"=>{"doi"=>"10.1371/journal.pcbi.1002455", "sgr"=>"84861138834", "issn"=>"1553734X", "pui"=>"364830861", "isbn"=>"1553-7358 (Electronic)\\n1553-734X (Linking)", "pmid"=>"22536150", "scopus"=>"2-s2.0-84861138834"}, "id"=>"70ed1eec-f8e0-37bf-b757-fc3168b576ac", "abstract"=>"The fixation of CO₂ into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major early divergences in the tree of life. These findings are based on a novel method that fully integrates metabolic and phylogenetic constraints. Comparing gene-profiles across the metabolic cores of deep-branching organisms and requiring that they are capable of synthesizing all their biomass components leads to the surprising conclusion that the most common form for deep-branching autotrophic carbon-fixation combines two disconnected sub-networks, each supplying carbon to distinct biomass components. One of these is a linear folate-based pathway of CO₂ reduction previously only recognized as a fixation route in the complete Wood-Ljungdahl pathway, but which more generally may exclude the final step of synthesizing acetyl-CoA. Using metabolic constraints we then reconstruct a \"phylometabolic\" tree with a high degree of parsimony that traces the evolution of complete carbon-fixation pathways, and has a clear structure down to the root. This tree requires few instances of lateral gene transfer or convergence, and instead suggests a simple evolutionary dynamic in which all divergences have primary environmental causes. Energy optimization and oxygen toxicity are the two strongest forces of selection. The root of this tree combines the reductive citric acid cycle and the Wood-Ljungdahl pathway into a single connected network. This linked network lacks the selective optimization of modern fixation pathways but its redundancy leads to a more robust topology, making it more plausible than any modern pathway as a primitive universal ancestral form.", "link"=>"http://www.mendeley.com/research/emergence-early-evolution-biological-carbonfixation", "reader_count"=>166, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>9, "Researcher"=>52, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>47, "Student > Postgraduate"=>5, "Student > Master"=>17, "Other"=>6, "Student > Bachelor"=>13, "Lecturer > Senior Lecturer"=>1, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>5, "Professor > Associate Professor"=>9, "Researcher"=>52, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>47, "Student > Postgraduate"=>5, "Student > Master"=>17, "Other"=>6, "Student > Bachelor"=>13, "Lecturer > Senior Lecturer"=>1, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>13, "Engineering"=>3, "Environmental Science"=>4, "Biochemistry, Genetics and Molecular Biology"=>15, "Materials Science"=>1, "Agricultural and Biological Sciences"=>93, "Physics and Astronomy"=>8, "Chemistry"=>11, "Social Sciences"=>3, "Computer Science"=>4, "Immunology and Microbiology"=>2, "Earth and Planetary Sciences"=>9}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Materials Science"=>{"Materials Science"=>1}, "Chemistry"=>{"Chemistry"=>11}, "Social Sciences"=>{"Social Sciences"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>8}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>9}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>93}, "Computer Science"=>{"Computer Science"=>4}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>15}, "Unspecified"=>{"Unspecified"=>13}, "Environmental Science"=>{"Environmental Science"=>4}}, "reader_count_by_country"=>{"Republic of Singapore"=>1, "United States"=>10, "Japan"=>1, "United Kingdom"=>3, "Portugal"=>1, "Switzerland"=>1, "India"=>1, "New Zealand"=>1, "Brazil"=>2, "Mexico"=>2, "Italy"=>1, "Chile"=>2, "Australia"=>1, "Peru"=>1}, "group_count"=>9}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/335059"], "description"=>"<div><p>The fixation of into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major early divergences in the tree of life. These findings are based on a novel method that fully integrates metabolic and phylogenetic constraints. Comparing gene-profiles across the metabolic cores of deep-branching organisms and requiring that they are capable of synthesizing all their biomass components leads to the surprising conclusion that the most common form for deep-branching autotrophic carbon-fixation combines two disconnected sub-networks, each supplying carbon to distinct biomass components. One of these is a linear folate-based pathway of reduction previously only recognized as a fixation route in the complete Wood-Ljungdahl pathway, but which more generally may exclude the final step of synthesizing acetyl-CoA. Using metabolic constraints we then reconstruct a “phylometabolic” tree with a high degree of parsimony that traces the evolution of complete carbon-fixation pathways, and has a clear structure down to the root. This tree requires few instances of lateral gene transfer or convergence, and instead suggests a simple evolutionary dynamic in which all divergences have primary environmental causes. Energy optimization and oxygen toxicity are the two strongest forces of selection. The root of this tree combines the reductive citric acid cycle and the Wood-Ljungdahl pathway into a single connected network. This linked network lacks the selective optimization of modern fixation pathways but its redundancy leads to a more robust topology, making it more plausible than any modern pathway as a primitive universal ancestral form.</p> </div>", "links"=>[], "tags"=>["emergence", "carbon-fixation"], "article_id"=>126206, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Emergence_and_Early_Evolution_of_Biological_Carbon_Fixation/126206", "title"=>"The Emergence and Early Evolution of Biological Carbon-Fixation", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-19 01:43:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/651285"], "description"=>"<p>Notes:</p><p><i><sup>a</sup></i>Glx = Glyoxylate pathways (rxn 12),</p><p><i><sup>b</sup></i>Ox = Oxidative pathway (rxns 9–11),</p><p><i><sup>c</sup></i>Red = Reductive pathway (rxns 1–8),</p><p><i><sup>d</sup></i>Red(-2) = Reductive pathway missing only rxn 2,</p><p><i><sup>e</sup></i>GlyC = Glycine cycle (rxns 5–8),</p><p><i><sup>f</sup></i>FDH = Formate dehydrogenase (rxn 1),</p><p><i><sup>g</sup></i>18 archaeal strains that lack only reaction 5 in the glycine cycle were included. For 7 such sulfulobales and the acidilobale a BLASTp search finds a protein that closely matches to this protein in strains not missing it.</p>", "links"=>[], "tags"=>["synthesis", "pathways", "deep-branching"], "article_id"=>321787, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.t001", "stats"=>{"downloads"=>7, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Complete_Glycine_Serine_synthesis_pathways_in_deep_branching_bacteria_and_archaea_/321787", "title"=>"Complete Glycine/Serine synthesis pathways in deep-branching bacteria and archaea.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-19 00:29:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/650881"], "description"=>"<p>Reactions (highlighted in blue) represent, as we show here, the ancestral route to glycine and serine. In organisms that use the Wood-Ljungdahl pathway as the exclusive route to carbon-fixation, the direct reduction of also culminates in the synthesis of acetyl-CoA, a step absent in many other organisms that do employ the preceding parts of the pathway. Reactions constitute the oxidative route to serine and glycine, which are subsequently cleaved to supply metabolism in many late-branching bacteria and eukaryotes. Reaction constitutes the glyoxylate pathways, important in cyanobacteria and photorespiring plants. Abbreviations: MFR, methanofuran; , tetrahydromethanopterin; THF, tetrahydrofolate; MET, methionine; LA, lipoic acid; GLY, glycine; SER, serine; PSR, phosphoserine; PHP, 3-phosphohydroxypyruvate; 3PG, 3-phosphoglycerate; GLX, glyoxylate. For a more detailed figure and caption, as well as names and EC classes of numbered reactions see <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455.s001\" target=\"_blank\">Text S1</a> and Fig. S1 in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455.s001\" target=\"_blank\">Text S1</a>.</p>", "links"=>[], "tags"=>["genetics and genomics", "microbiology", "Computational biology", "Evolutionary biology", "Biochemistry"], "article_id"=>321374, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_metabolism_/321374", "title"=>"Summary of metabolism.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-19 00:22:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/650938"], "description"=>"<p>Dark purple dots indicate clades in which the complete gene complement for direct reductive synthesis of glycine and serine is found, light purple dots indicate clades where a complete pathway is suspected. Red dots indicate clades in which direct reduction of is known to be active, but in a form that lacks synthesis of glycine and serine. See main text for further details. The unrooted phylogenetic tree was adapted, with modification, from <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455-Puigbo1\" target=\"_blank\">[14]</a>. In that work, the tree was created from an analysis of 102 ‘nearly universal’ clusters of orthologous groups of proteins (COGs) (present in of species in the tree) <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455-Puigbo1\" target=\"_blank\">[14]</a>.</p>", "links"=>[], "tags"=>["pathways", "archaea"], "article_id"=>321433, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_distribution_of_direct_pathways_in_Archaea_and_Bacteria_/321433", "title"=>"Phylogenetic distribution of direct pathways in Archaea and Bacteria.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-19 00:23:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/650775"], "description"=>"<p><b>A</b> - <i>Example metabolic network structure</i>. Two essential metabolites, X and Y, can be synthesized through three known metabolic pathways, indicated by magenta, orange and purple arrows. Individual arrows represent enzymes catalyzing different steps in the pathway, and they can be either absent (empty arrows) or present (filled arrows) in the annotated genome of a particular strain R. Arrows in black are universal metabolic genes. <b>B</b> - <i>Phylogenetics constrains metabolic analysis</i>. Each branch in this phylogenetic tree represents an individual strain. The gap structure in the metabolic network of strain R, which was difficult to interpret in isolation becomes much less uncertain when placed in a phylogenetic context, suggesting that in this organism the orange pathway should be completed. <b>C</b> - <i>Metabolic analysis constrains phylogenetics</i>. Each branch in this tree represents a clade and individual (horizontal) rows within the metabolic gene profile matrices represent the profile of individual strains. Here the metabolic context suggests proper placement of a clade-level branch that was uncertain in an unconstrained phylogenetic tree. <b>D</b> - <i>Fully integrated phylometabolic tree</i>. Metabolic sequences are now drawn at the pathway level, and this tree represents a reconstruction of the evolution of the synthesis pathways of metabolites X and Y. Because mechanisms of regulation or heredity are not modeled, this phylometabolic tree is indifferent to distinctions of ecosystems or species, and the shown ‘phenotypes’ refer exclusively to the biochemistry of these pathways (see text for further details). <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi-1002455-g001\" target=\"_blank\">Fig. 1C</a> suggested that the orange pathway was ancestral, and that the magenta and purple pathways were derived from it. The only sequences that are then allowed under the constraint that essential metabolites X and Y are continuously produced, is the appearance of the purple and magenta pathways from stages in which they are co-present with the orange pathway.</p>", "links"=>[], "tags"=>["phylometabolic"], "article_id"=>321271, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.g001", "stats"=>{"downloads"=>2, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Principles_of_phylometabolic_analysis_/321271", "title"=>"Principles of phylometabolic analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-19 00:21:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/651030"], "description"=>"<p>The sequences on the left show how the key reactions in the synthesis of tetrahydrofolate (THF) and tetrahydromethanopterin () diverge starting from GTP. The structures on the right show the observed variants within the modified folate family and the domain within which they are observed. Unlike other pterins, those observed within Pyrococcus and Thermococcus were not named, hence the name of the clades containing them is shown instead. Within the chemical structures, the core structure that is universal across the folate family, and derived from GTP and aminobenzoate, is highlighted in blue. Numbered and highlighted in green are the and positions of the folates, upon which chemical processing of units occurs (see Fig. S1 in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455.s001\" target=\"_blank\">Text S1</a>). The carbon highlighted with an asterisk () has the same chirality upon reduction in the final step in both THF and synthesis, further highlighting their relatedness. Highlighted in red is the carbonyl group resultant from aminobenzoate that is present in THF but absent in all modified folates, resulting in a large difference in electron density at between these two groups. Highlighted in purple are structural methyl groups, which are absent in THF but present in . The modified folates as a group show variation in the number of methyl groups they contain in the same order in which they are added in the synthesis of . Abbreviations: PRPP, phosphoribosyl pyrophosphate; Glu, Glutamate; -KG, -ketoglutarate; SAM, S-adenosyl methionine. The information used to create this figure draws on results from a wide range of experimental studies, including on the synthesis of THF and <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455-Graham1\" target=\"_blank\">[55]</a>–<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455-White3\" target=\"_blank\">[58]</a>, and on modified folates found in the archaeal domain <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455-vanBeelen1\" target=\"_blank\">[59]</a>–<a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi.1002455-White5\" target=\"_blank\">[64]</a>.</p>", "links"=>[], "tags"=>["folate"], "article_id"=>321528, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.g004", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synthesis_of_and_structural_variation_in_the_folate_family_/321528", "title"=>"Synthesis of and structural variation in the folate family.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-19 00:25:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/651130"], "description"=>"<p>The grey line represents the maximum-parsimony tree linking the major metabolic phenotypes (diagrams). Three major modules shown schematically (see the legend) are pterin/folate- metabolism, the pentose-phosphate pathway, and the TCA cycle reactions. Lost reactions (symbol) include the acetyl-CoA synthase (in metabolism), and ferredoxin-dependent succinyl-CoA synthase (in TCA loop) or citryl-CoA synthase (not shown). Abbreviations: , formyl; , methylene; ACA, acetyl-CoA; PYR, pyruvate; GAP, glyceraldehyde-3-phosphate; F6B, fructose-1,6-bisphosphate; RIB, ribose-phosphate; RBL, ribulose-phosphate; ALK, alkalinity; others as in <a href=\"http://www.ploscompbiol.org/article/info:doi/10.1371/journal.pcbi.1002455#pcbi-1002455-g002\" target=\"_blank\">Fig. 2</a>. Arrows indicate reaction directions; dashed line connecting 3PG to SER indicates intermittent or bidirectional reaction. Highlighted in yellow are the innovations underlying divergences, while red labels on links indicate evolutionary force associated with each innovation, explained in the text. Beneath each diagram is an extant species or clade name where the phenotype is found. Colored regions indicate domains within which all known instances of the indicated phenotypes are restricted.</p>", "links"=>[], "tags"=>["genetics and genomics", "microbiology", "Computational biology", "Evolutionary biology", "Biochemistry"], "article_id"=>321619, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylometabolic_tree_of_carbon_fixation_/321619", "title"=>"Phylometabolic tree of carbon-fixation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-19 00:26:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/651256"], "description"=>"<p>ATP and reductant cost for synthetic routes to glycine and serine.</p>", "links"=>[], "tags"=>["reductant", "synthetic", "routes", "glycine"], "article_id"=>321753, "categories"=>["Biological Sciences", "Biochemistry", "Genetics", "Microbiology", "Evolutionary Biology"], "users"=>["Rogier Braakman", "Eric Smith"], "doi"=>"https://dx.doi.org/10.1371/journal.pcbi.1002455.t002", "stats"=>{"downloads"=>2, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATP_and_reductant_cost_for_synthetic_routes_to_glycine_and_serine_/321753", "title"=>"ATP and reductant cost for synthetic routes to glycine and serine.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-19 00:29:13"}

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