The Non-Flagellar Type III Secretion System Evolved from the Bacterial Flagellum and Diversified into Host-Cell Adapted Systems
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{"title"=>"The Non-Flagellar Type III Secretion System Evolved from the Bacterial Flagellum and Diversified into Host-Cell Adapted Systems", "type"=>"journal", "authors"=>[{"first_name"=>"Sophie S.", "last_name"=>"Abby", "scopus_author_id"=>"16030267900"}, {"first_name"=>"Eduardo P.C.", "last_name"=>"Rocha", "scopus_author_id"=>"56031901800"}], "year"=>2012, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-84866928806", "doi"=>"10.1371/journal.pgen.1002983", "sgr"=>"84866928806", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"23028376", "issn"=>"15537390", "pui"=>"365756009"}, "id"=>"41e92228-a8b8-3afb-a667-c23f39f97073", "abstract"=>"Type 3 secretion systems (T3SSs) are essential components of two complex bacterial machineries: the flagellum, which drives cell motility, and the non-flagellar T3SS (NF-T3SS), which delivers effectors into eukaryotic cells. Yet the origin, specialization, and diversification of these machineries remained unclear. We developed computational tools to identify homologous components of the two systems and to discriminate between them. Our analysis of >1,000 genomes identified 921 T3SSs, including 222 NF-T3SSs. Phylogenomic and comparative analyses of these systems argue that the NF-T3SS arose from an exaptation of the flagellum, i.e. the recruitment of part of the flagellum structure for the evolution of the new protein delivery function. This reconstructed chronology of the exaptation process proceeded in at least two steps. An intermediate ancestral form of NF-T3SS, whose descendants still exist in Myxococcales, lacked elements that are essential for motility and included a subset of NF-T3SS features. We argue that this ancestral version was involved in protein translocation. A second major step in the evolution of NF-T3SSs occurred via recruitment of secretins to the NF-T3SS, an event that occurred at least three times from different systems. In rhizobiales, a partial homologous gene replacement of the secretin resulted in two genes of complementary function. Acquisition of a secretin was followed by the rapid adaptation of the resulting NF-T3SSs to multiple, distinct eukaryotic cell envelopes where they became key in parasitic and mutualistic associations between prokaryotes and eukaryotes. Our work elucidates major steps of the evolutionary scenario leading to extant NF-T3SSs. It demonstrates how molecular evolution can convert one complex molecular machine into a second, equally complex machine by successive deletions, innovations, and recruitment from other molecular systems.", "link"=>"http://www.mendeley.com/research/nonflagellar-type-iii-secretion-system-evolved-bacterial-flagellum-diversified-hostcell-adapted-syst", "reader_count"=>190, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>11, "Student > Doctoral Student"=>11, "Researcher"=>40, "Student > Ph. D. Student"=>59, "Student > Postgraduate"=>3, "Student > Master"=>24, "Other"=>5, "Student > Bachelor"=>24, "Lecturer"=>2, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>11, "Student > Doctoral Student"=>11, "Researcher"=>40, "Student > Ph. D. Student"=>59, "Student > Postgraduate"=>3, "Student > Master"=>24, "Other"=>5, "Student > Bachelor"=>24, "Lecturer"=>2, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>26, "Mathematics"=>1, "Agricultural and Biological Sciences"=>137, "Medicine and Dentistry"=>3, "Philosophy"=>1, "Chemistry"=>4, "Social Sciences"=>1, "Computer Science"=>1, "Immunology and Microbiology"=>5, "Earth and Planetary Sciences"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>4}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>137}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>26}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>3}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Greece"=>1, "Belgium"=>1, "United States"=>3, "United Kingdom"=>4, "France"=>3, "Germany"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/301180", "https://ndownloader.figshare.com/files/301204", "https://ndownloader.figshare.com/files/301226", "https://ndownloader.figshare.com/files/301293", "https://ndownloader.figshare.com/files/301333", "https://ndownloader.figshare.com/files/301992", "https://ndownloader.figshare.com/files/302084", "https://ndownloader.figshare.com/files/302215", "https://ndownloader.figshare.com/files/302286", "https://ndownloader.figshare.com/files/302370", "https://ndownloader.figshare.com/files/302417", "https://ndownloader.figshare.com/files/302482", "https://ndownloader.figshare.com/files/302551", "https://ndownloader.figshare.com/files/302619", "https://ndownloader.figshare.com/files/302708", "https://ndownloader.figshare.com/files/302807", "https://ndownloader.figshare.com/files/302898"], "description"=>"<div><p>Type 3 secretion systems (T3SSs) are essential components of two complex bacterial machineries: the flagellum, which drives cell motility, and the non-flagellar T3SS (NF-T3SS), which delivers effectors into eukaryotic cells. Yet the origin, specialization, and diversification of these machineries remained unclear. We developed computational tools to identify homologous components of the two systems and to discriminate between them. Our analysis of >1,000 genomes identified 921 T3SSs, including 222 NF-T3SSs. Phylogenomic and comparative analyses of these systems argue that the NF-T3SS arose from an exaptation of the flagellum, i.e. the recruitment of part of the flagellum structure for the evolution of the new protein delivery function. This reconstructed chronology of the exaptation process proceeded in at least two steps. An intermediate ancestral form of NF-T3SS, whose descendants still exist in Myxococcales, lacked elements that are essential for motility and included a subset of NF-T3SS features. We argue that this ancestral version was involved in protein translocation. A second major step in the evolution of NF-T3SSs occurred <em>via</em> recruitment of secretins to the NF-T3SS, an event that occurred at least three times from different systems. In rhizobiales, a partial homologous gene replacement of the secretin resulted in two genes of complementary function. Acquisition of a secretin was followed by the rapid adaptation of the resulting NF-T3SSs to multiple, distinct eukaryotic cell envelopes where they became key in parasitic and mutualistic associations between prokaryotes and eukaryotes. Our work elucidates major steps of the evolutionary scenario leading to extant NF-T3SSs. It demonstrates how molecular evolution can convert one complex molecular machine into a second, equally complex machine by successive deletions, innovations, and recruitment from other molecular systems.</p> </div>", "links"=>[], "tags"=>["non-flagellar", "iii", "secretion", "evolved", "bacterial", "flagellum", "diversified", "host-cell", "adapted", "systems"], "article_id"=>119390, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.s001", "https://dx.doi.org/10.1371/journal.pgen.1002983.s002", "https://dx.doi.org/10.1371/journal.pgen.1002983.s003", "https://dx.doi.org/10.1371/journal.pgen.1002983.s004", "https://dx.doi.org/10.1371/journal.pgen.1002983.s005", "https://dx.doi.org/10.1371/journal.pgen.1002983.s006", "https://dx.doi.org/10.1371/journal.pgen.1002983.s007", "https://dx.doi.org/10.1371/journal.pgen.1002983.s008", "https://dx.doi.org/10.1371/journal.pgen.1002983.s009", "https://dx.doi.org/10.1371/journal.pgen.1002983.s010", "https://dx.doi.org/10.1371/journal.pgen.1002983.s011", "https://dx.doi.org/10.1371/journal.pgen.1002983.s012", "https://dx.doi.org/10.1371/journal.pgen.1002983.s013", "https://dx.doi.org/10.1371/journal.pgen.1002983.s014", "https://dx.doi.org/10.1371/journal.pgen.1002983.s015", "https://dx.doi.org/10.1371/journal.pgen.1002983.s016", "https://dx.doi.org/10.1371/journal.pgen.1002983.s017"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Non_Flagellar_Type_III_Secretion_System_Evolved_from_the_Bacterial_Flagellum_and_Diversified_into_Host_Cell_Adapted_Systems/119390", "title"=>"The Non-Flagellar Type III Secretion System Evolved from the Bacterial Flagellum and Diversified into Host-Cell Adapted Systems", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-09-27 02:36:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/567789"], "description"=>"<p>(A) Representation of the proposed organization of a NF-T3SS system, inspired from the <i>Salmonella</i> system <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983-Erhardt1\" target=\"_blank\">[139]</a>. For consistency with the main text, nomenclature follows that of <i>Yersinia</i> for some genes (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s009\" target=\"_blank\">Table S1</a> for equivalence). Genes in red have homologs in the flagellum (main text, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s009\" target=\"_blank\">Table S1</a>). “Euka” stands for eukaryotic, “mb” stands for membrane, “IM” for inner membrane, and “OM” for outer membrane. (B) Distribution of the number of different protein profiles of the 9 core genes of NF-T3SS matched per replicon (i-evalue<10<sup>−3</sup>). Bar colors discriminate between systems in flagella or NF-T3SSs and other systems including only a secretin (SctC) and/or the ATPase (SctN). Numbers of replicons are indicated above the corresponding bars, with the number of uncharacterized cases (“Others”, colored in magenta in bars) in parenthesis if different from the total. “Nb” is an abbreviation for “Number”.</p>", "links"=>[], "tags"=>["t3ss", "genes"], "article_id"=>238285, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_T3SS_core_genes_in_complete_genomes_/238285", "title"=>"Identification of T3SS core genes in complete genomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:18:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/567869"], "description"=>"<p>Each T3SS core protein was scored using the protein profiles for flagella (Y axis) and for NF-T3SSs (X axis). One sees a clear separation around the main diagonal. The color indicates the system (blue for flagellar proteins, red for NF-T3SS proteins). A circle indicates a correct prediction, and a triangle a wrong prediction. The analysis is described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#s4\" target=\"_blank\">Materials and Methods</a>, and the learning dataset is shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s003\" target=\"_blank\">Figure S1</a>.</p>", "links"=>[], "tags"=>["nf-t3sss", "flagella", "hmmer"], "article_id"=>238368, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Discrimination_between_NF_T3SSs_and_flagella_based_on_Hmmer_profile_scores_/238368", "title"=>"Discrimination between NF-T3SSs and flagella based on Hmmer profile scores.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:19:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/567955"], "description"=>"<p>(A) Representation of the three possible scenarios for the relative emergence of the flagellum and of the NF-T3SS. The numbers represent the percentage of each scenario in the bootstrap analysis of the ATPase family (out of 997 bootstrap trees where outgroup sequences were monophyletic, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s004\" target=\"_blank\">Figure S2</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s008\" target=\"_blank\">Protocol S1</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s014\" target=\"_blank\">Text S1</a>). (B) The maximum likelihood tree of the ATPase family shows that the NF-T3SS derives from the flagellum. Support values are shown only for relationships important to discriminate between the three scenarios in the panel (A). They correspond to the occurrence of the splits in 1000 bootstrap replicates. The multiple alignment used to build this tree had 296 informative sites and is supplied in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s001\" target=\"_blank\">Dataset S1</a>.</p>", "links"=>[], "tags"=>["microbiology", "Computational biology", "Evolutionary biology"], "article_id"=>238452, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rooting_the_history_of_T3SS_/238452", "title"=>"Rooting the history of T3SS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:20:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/568019"], "description"=>"<p>The eight individual gene trees are displayed in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s005\" target=\"_blank\">Figure S3</a>. The large monophyletic clades highlighted by different colors correspond to the NF-T3SS families (names in bold, see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s015\" target=\"_blank\">Text S2</a>). Colored circles indicate the bootstrap support of these families and of the relationships between them. The “Ecology/Host” panel indicates the predominant bacterium/eukaryote associations for each family (see main text and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s006\" target=\"_blank\">Figure S4</a>). The external branch indicates the position of the flagellum sequences and was inferred with the “rooted” dataset (“rooted” tree is in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s007\" target=\"_blank\">Figure S5</a>). “Chlamy” stands for Chlamydiales, “Desulfo” for Desulfovibrionales, “Myxo” for Myxococcales, and “Rhizo” for Rhizobiales. The scale of the tree is given in substitutions per site.</p>", "links"=>[], "tags"=>["phylogeny", "nf-t3ss", "proteins", "flagellar"], "article_id"=>238509, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Concatenate_phylogeny_of_the_core_NF_T3SS_proteins_with_flagellar_homologs_/238509", "title"=>"Concatenate phylogeny of the core NF-T3SS proteins with flagellar homologs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:21:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/568122"], "description"=>"<p>The gene contents of the “short” and “long” Myxo NF-T3SSs are displayed on the 16S rRNA phylogeny of the group. The 16S rRNA maximum likelihood tree was built with RAxML <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983-Stamatakis1\" target=\"_blank\">[96]</a> (General time-reversible model + 4-categories-discretized Gamma distribution for rate variations among sites) and chosen from the best of 200 starting trees. The numbers in the tree nodes refer to bootstrap values out of 100 replicates. The identified NF-T3SS genes are represented by boxes containing the last letter of the “<i>sct</i>” gene name, and colored according to the color code of <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen-1002983-g001\" target=\"_blank\">Figure 1A</a>. Dashed transparent boxes correspond to genes showing hits for Hmmer sequence profiles with i-evalue above the 10<sup>−3</sup> threshold. Empty boxes correspond to genes not annotated in our analysis, and boxes with three dots correspond to several (4 to 16) consecutive non-annotated genes. Proteins encoded in the loci are colored on the NF-T3SS structure drawings, whereas parts of the structure whose corresponding gene could not be found remain unfilled.</p>", "links"=>[], "tags"=>["myxo"], "article_id"=>238620, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_organization_of_the_Myxo_NF_T3SS_/238620", "title"=>"Genomic organization of the Myxo NF-T3SS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:23:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/568178"], "description"=>"<p>(A) Phylogeny of the secretin family. The numbers represent bootstrap support values for branches separating the different types of secretins found in NF-T3SSs (highlighted by colored bars). Gray boxes indicate the main secretin groups. The two genes encoding the Rhizo secretin are indicated in orange and yellow boxes (see panel B). NF-T3SS types are named as in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen-1002983-g004\" target=\"_blank\">Figure 4</a>. (B) Domain architecture of the secretins related to NF-T3SS secretins. PFAM domains were identified using InterProScan <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983-Quevillon1\" target=\"_blank\">[140]</a>, except for the Chlamy-specific N-terminal domain of the NF-T3SS secretin CdsC (burgundy box), and the dashed box “N-domain”, which were identified by sequence similarity with the other secretins using Blast. Signal peptides were detected with InterProScan and PsortB <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983-Yu1\" target=\"_blank\">[141]</a>. Dotted lines correspond to the boundaries of the alignments of Blast hits. See <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s017\" target=\"_blank\">Text S4</a> for more analyses of Rhizo secretins. (C) Analysis of the genetic organization of the Rhizo loci mapped on their phylogeny. The phylogeny was inferred from the concatenation of the eight NF-T3SS core genes (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen-1002983-g004\" target=\"_blank\">Figure 4</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983.s006\" target=\"_blank\">Figure S4</a>). Conventions are the same as in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen-1002983-g005\" target=\"_blank\">Figure 5</a>. Numbers in white boxes correspond to the number of genes separating the block of genes with conserved order (light green box) from the RhcC2 secretin (outside the box), or to the number of consecutive genes not annotated in this study (inside the box).</p>", "links"=>[], "tags"=>["nf-t3ss"], "article_id"=>238681, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_history_domain_architecture_and_genetic_organization_of_the_NF_T3SS_secretins_/238681", "title"=>"Evolutionary history, domain architecture, and genetic organization of the NF-T3SS secretins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:24:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/568290"], "description"=>"<p>We propose that genes common to the flagellum and the NF-T3SS were present in the flagellar ancestor of NF-T3SS. They are designated as “T3SS genes”. Then we detail the evolution of this system to the extant NF-T3SSs. First, the loss of flagellum-specific genes resulted in loss of the motility function. Presumably this system kept the ability to translocate or secrete proteins. The ancestral NF-T3SS experienced a series of gene losses and gains while diversifying to the ancestor of all extant NF-T3SSs. One early lineage derived into the Myxo systems by loss of some genes, notably SctF. Acquisition of secretins and of a few other genes allowed the formation of ancestral contact-dependent protein secretion systems, and the concomitant ability to subvert eukaryotic cells by direct delivery of effectors in their cytosol. Secretins were recruited to the NF-T3SS at least three times from three different cell machineries. Finally, the NF-T3SS quickly diversified and adapted to different host cells. Some components of NF-T3SS, such as the translocon proteins (YopB/YopD), the needle length determinant (SctP) or the needle tip (LcrV), cannot yet be integrated in this schema because of low or undetectable sequence similarity among T3SSs. Structural and sequence similarities were previously noted between translocon proteins of <i>Chlamydia</i> (CopB) and <i>Salmonella</i> (SipB) <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983-Fields1\" target=\"_blank\">[142]</a>. In contrast, we found no more than 28% identity over less than half of the protein when aligning CopB with all complete genomes in GenBank after excluding Chlamy proteins (Blastp, e-value>0.05). We also did not find significant sequence homologs of YopB/YopD in the NF-T3SS of Myxo or plant-associated bacteria. Since the translocon is required for protein delivery but not for secretion <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen.1002983-Hakansson1\" target=\"_blank\">[35]</a>, it might have been acquired after the secretin. Balloons indicate gene losses and accretions. Only genes mentioned in the main text are shown. Abbreviated names of taxa are as in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002983#pgen-1002983-g004\" target=\"_blank\">Figure 4</a>.</p>", "links"=>[], "tags"=>["microbiology", "Computational biology", "Evolutionary biology"], "article_id"=>238784, "categories"=>["Biological Sciences", "Microbiology", "Evolutionary Biology"], "users"=>["Sophie S. Abby", "Eduardo P. C. Rocha"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1002983.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_scenario_for_the_evolution_of_NF_T3SS_/238784", "title"=>"Proposed scenario for the evolution of NF-T3SS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-27 02:26:24"}

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Relative Metric

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