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A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group

BACKGROUND: Dictyostelia are a well-studied group of organisms with colonial multicellularity, which are members of the mostly unicellular Amoebozoa. A phylogeny based on SSU rDNA data subdivided all Dictyostelia into four major groups, but left the position of the root and of six group-intermediate...

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Autores principales: Singh, Reema, Schilde, Christina, Schaap, Pauline
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5114724/
https://www.ncbi.nlm.nih.gov/pubmed/27855631
http://dx.doi.org/10.1186/s12862-016-0825-7
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author Singh, Reema
Schilde, Christina
Schaap, Pauline
author_facet Singh, Reema
Schilde, Christina
Schaap, Pauline
author_sort Singh, Reema
collection PubMed
description BACKGROUND: Dictyostelia are a well-studied group of organisms with colonial multicellularity, which are members of the mostly unicellular Amoebozoa. A phylogeny based on SSU rDNA data subdivided all Dictyostelia into four major groups, but left the position of the root and of six group-intermediate taxa unresolved. Recent phylogenies inferred from 30 or 213 proteins from sequenced genomes, positioned the root between two branches, each containing two major groups, but lacked data to position the group-intermediate taxa. Since the positions of these early diverging taxa are crucial for understanding the evolution of phenotypic complexity in Dictyostelia, we sequenced six representative genomes of early diverging taxa. RESULTS: We retrieved orthologs of 47 housekeeping proteins with an average size of 890 amino acids from six newly sequenced and eight published genomes of Dictyostelia and unicellular Amoebozoa and inferred phylogenies from single and concatenated protein sequence alignments. Concatenated alignments of all 47 proteins, and four out of five subsets of nine concatenated proteins all produced the same consensus phylogeny with 100% statistical support. Trees inferred from just two out of the 47 proteins, individually reproduced the consensus phylogeny, highlighting that single gene phylogenies will rarely reflect correct species relationships. However, sets of two or three concatenated proteins again reproduced the consensus phylogeny, indicating that a small selection of genes suffices for low cost classification of as yet unincorporated or newly discovered dictyostelid and amoebozoan taxa by gene amplification. CONCLUSIONS: The multi-locus consensus phylogeny shows that groups 1 and 2 are sister clades in branch I, with the group-intermediate taxon D. polycarpum positioned as outgroup to group 2. Branch II consists of groups 3 and 4, with the group-intermediate taxon Polysphondylium violaceum positioned as sister to group 4, and the group-intermediate taxon Dictyostelium polycephalum branching at the base of that whole clade. Given the data, the approximately unbiased test rejects all alternative topologies favoured by SSU rDNA and individual proteins with high statistical support. The test also rejects monophyletic origins for the genera Acytostelium, Polysphondylium and Dictyostelium. The current position of Acytostelium ellipticum in the consensus phylogeny indicates that somatic cells were lost twice in Dictyostelia. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0825-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-51147242016-11-25 A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group Singh, Reema Schilde, Christina Schaap, Pauline BMC Evol Biol Research Article BACKGROUND: Dictyostelia are a well-studied group of organisms with colonial multicellularity, which are members of the mostly unicellular Amoebozoa. A phylogeny based on SSU rDNA data subdivided all Dictyostelia into four major groups, but left the position of the root and of six group-intermediate taxa unresolved. Recent phylogenies inferred from 30 or 213 proteins from sequenced genomes, positioned the root between two branches, each containing two major groups, but lacked data to position the group-intermediate taxa. Since the positions of these early diverging taxa are crucial for understanding the evolution of phenotypic complexity in Dictyostelia, we sequenced six representative genomes of early diverging taxa. RESULTS: We retrieved orthologs of 47 housekeeping proteins with an average size of 890 amino acids from six newly sequenced and eight published genomes of Dictyostelia and unicellular Amoebozoa and inferred phylogenies from single and concatenated protein sequence alignments. Concatenated alignments of all 47 proteins, and four out of five subsets of nine concatenated proteins all produced the same consensus phylogeny with 100% statistical support. Trees inferred from just two out of the 47 proteins, individually reproduced the consensus phylogeny, highlighting that single gene phylogenies will rarely reflect correct species relationships. However, sets of two or three concatenated proteins again reproduced the consensus phylogeny, indicating that a small selection of genes suffices for low cost classification of as yet unincorporated or newly discovered dictyostelid and amoebozoan taxa by gene amplification. CONCLUSIONS: The multi-locus consensus phylogeny shows that groups 1 and 2 are sister clades in branch I, with the group-intermediate taxon D. polycarpum positioned as outgroup to group 2. Branch II consists of groups 3 and 4, with the group-intermediate taxon Polysphondylium violaceum positioned as sister to group 4, and the group-intermediate taxon Dictyostelium polycephalum branching at the base of that whole clade. Given the data, the approximately unbiased test rejects all alternative topologies favoured by SSU rDNA and individual proteins with high statistical support. The test also rejects monophyletic origins for the genera Acytostelium, Polysphondylium and Dictyostelium. The current position of Acytostelium ellipticum in the consensus phylogeny indicates that somatic cells were lost twice in Dictyostelia. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-016-0825-7) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-17 /pmc/articles/PMC5114724/ /pubmed/27855631 http://dx.doi.org/10.1186/s12862-016-0825-7 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Singh, Reema
Schilde, Christina
Schaap, Pauline
A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
title A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
title_full A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
title_fullStr A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
title_full_unstemmed A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
title_short A core phylogeny of Dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
title_sort core phylogeny of dictyostelia inferred from genomes representative of the eight major and minor taxonomic divisions of the group
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5114724/
https://www.ncbi.nlm.nih.gov/pubmed/27855631
http://dx.doi.org/10.1186/s12862-016-0825-7
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