The synergistic effect of concatenation in phylogenomics: the case in Pantoea

With the increased availability of genome sequences for bacteria, it has become routine practice to construct genome-based phylogenies. These phylogenies have formed the basis for various taxonomic decisions, especially for resolving problematic relationships between taxa. Despite the popularity of...

Full description

Bibliographic Details
Main Authors: Marike Palmer, Stephanus N. Venter, Alistair R. McTaggart, Martin P.A. Coetzee, Stephanie Van Wyk, Juanita R. Avontuur, Chrizelle W. Beukes, Gerda Fourie, Quentin C. Santana, Magriet A. Van Der Nest, Jochen Blom, Emma T. Steenkamp
Format: Article
Language:English
Published: PeerJ Inc. 2019-04-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/6698.pdf
_version_ 1797424234462445568
author Marike Palmer
Stephanus N. Venter
Alistair R. McTaggart
Martin P.A. Coetzee
Stephanie Van Wyk
Juanita R. Avontuur
Chrizelle W. Beukes
Gerda Fourie
Quentin C. Santana
Magriet A. Van Der Nest
Jochen Blom
Emma T. Steenkamp
author_facet Marike Palmer
Stephanus N. Venter
Alistair R. McTaggart
Martin P.A. Coetzee
Stephanie Van Wyk
Juanita R. Avontuur
Chrizelle W. Beukes
Gerda Fourie
Quentin C. Santana
Magriet A. Van Der Nest
Jochen Blom
Emma T. Steenkamp
author_sort Marike Palmer
collection DOAJ
description With the increased availability of genome sequences for bacteria, it has become routine practice to construct genome-based phylogenies. These phylogenies have formed the basis for various taxonomic decisions, especially for resolving problematic relationships between taxa. Despite the popularity of concatenating shared genes to obtain well-supported phylogenies, various issues regarding this combined-evidence approach have been raised. These include the introduction of phylogenetic error into datasets, as well as incongruence due to organism-level evolutionary processes, particularly horizontal gene transfer and incomplete lineage sorting. Because of the huge effect that this could have on phylogenies, we evaluated the impact of phylogenetic conflict caused by organism-level evolutionary processes on the established species phylogeny for Pantoea, a member of the Enterobacterales. We explored the presence and distribution of phylogenetic conflict at the gene partition and nucleotide levels, by identifying putative inter-lineage recombination events that might have contributed to such conflict. Furthermore, we determined whether smaller, randomly constructed datasets had sufficient signal to reconstruct the current species tree hypothesis or if they would be overshadowed by phylogenetic incongruence. We found that no individual gene tree was fully congruent with the species phylogeny of Pantoea, although many of the expected nodes were supported by various individual genes across the genome. Evidence of recombination was found across all lineages within Pantoea, and provides support for organism-level evolutionary processes as a potential source of phylogenetic conflict. The phylogenetic signal from at least 70 random genes recovered robust, well-supported phylogenies for the backbone and most species relationships of Pantoea, and was unaffected by phylogenetic conflict within the dataset. Furthermore, despite providing limited resolution among taxa at the level of single gene trees, concatenated analyses of genes that were identified as having no signal resulted in a phylogeny that resembled the species phylogeny of Pantoea. This distribution of signal and noise across the genome presents the ideal situation for phylogenetic inference, as the topology from a ≥70-gene concatenated species phylogeny is not driven by single genes, and our data suggests that this finding may also hold true for smaller datasets. We thus argue that, by using a concatenation-based approach in phylogenomics, one can obtain robust phylogenies due to the synergistic effect of the combined signal obtained from multiple genes.
first_indexed 2024-03-09T07:59:23Z
format Article
id doaj.art-2c738682cb524949bca2684dd192a902
institution Directory Open Access Journal
issn 2167-8359
language English
last_indexed 2024-03-09T07:59:23Z
publishDate 2019-04-01
publisher PeerJ Inc.
record_format Article
series PeerJ
spelling doaj.art-2c738682cb524949bca2684dd192a9022023-12-03T00:48:15ZengPeerJ Inc.PeerJ2167-83592019-04-017e669810.7717/peerj.6698The synergistic effect of concatenation in phylogenomics: the case in PantoeaMarike Palmer0Stephanus N. Venter1Alistair R. McTaggart2Martin P.A. Coetzee3Stephanie Van Wyk4Juanita R. Avontuur5Chrizelle W. Beukes6Gerda Fourie7Quentin C. Santana8Magriet A. Van Der Nest9Jochen Blom10Emma T. Steenkamp11Department of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaBioinformatics and Systems Biology, Justus Liebig Universität Gießen, Giessen, GermanyDepartment of Biochemistry, Genetics and Microbiology, DST-NRF Centre of Excellence in Tree Health Biotechnology (CTHB) and Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, Gauteng, South AfricaWith the increased availability of genome sequences for bacteria, it has become routine practice to construct genome-based phylogenies. These phylogenies have formed the basis for various taxonomic decisions, especially for resolving problematic relationships between taxa. Despite the popularity of concatenating shared genes to obtain well-supported phylogenies, various issues regarding this combined-evidence approach have been raised. These include the introduction of phylogenetic error into datasets, as well as incongruence due to organism-level evolutionary processes, particularly horizontal gene transfer and incomplete lineage sorting. Because of the huge effect that this could have on phylogenies, we evaluated the impact of phylogenetic conflict caused by organism-level evolutionary processes on the established species phylogeny for Pantoea, a member of the Enterobacterales. We explored the presence and distribution of phylogenetic conflict at the gene partition and nucleotide levels, by identifying putative inter-lineage recombination events that might have contributed to such conflict. Furthermore, we determined whether smaller, randomly constructed datasets had sufficient signal to reconstruct the current species tree hypothesis or if they would be overshadowed by phylogenetic incongruence. We found that no individual gene tree was fully congruent with the species phylogeny of Pantoea, although many of the expected nodes were supported by various individual genes across the genome. Evidence of recombination was found across all lineages within Pantoea, and provides support for organism-level evolutionary processes as a potential source of phylogenetic conflict. The phylogenetic signal from at least 70 random genes recovered robust, well-supported phylogenies for the backbone and most species relationships of Pantoea, and was unaffected by phylogenetic conflict within the dataset. Furthermore, despite providing limited resolution among taxa at the level of single gene trees, concatenated analyses of genes that were identified as having no signal resulted in a phylogeny that resembled the species phylogeny of Pantoea. This distribution of signal and noise across the genome presents the ideal situation for phylogenetic inference, as the topology from a ≥70-gene concatenated species phylogeny is not driven by single genes, and our data suggests that this finding may also hold true for smaller datasets. We thus argue that, by using a concatenation-based approach in phylogenomics, one can obtain robust phylogenies due to the synergistic effect of the combined signal obtained from multiple genes.https://peerj.com/articles/6698.pdfPhylogenomicsConcatenateSuper treesPhylogeneticsPhylogenetic signalPhylogenetic conflict
spellingShingle Marike Palmer
Stephanus N. Venter
Alistair R. McTaggart
Martin P.A. Coetzee
Stephanie Van Wyk
Juanita R. Avontuur
Chrizelle W. Beukes
Gerda Fourie
Quentin C. Santana
Magriet A. Van Der Nest
Jochen Blom
Emma T. Steenkamp
The synergistic effect of concatenation in phylogenomics: the case in Pantoea
PeerJ
Phylogenomics
Concatenate
Super trees
Phylogenetics
Phylogenetic signal
Phylogenetic conflict
title The synergistic effect of concatenation in phylogenomics: the case in Pantoea
title_full The synergistic effect of concatenation in phylogenomics: the case in Pantoea
title_fullStr The synergistic effect of concatenation in phylogenomics: the case in Pantoea
title_full_unstemmed The synergistic effect of concatenation in phylogenomics: the case in Pantoea
title_short The synergistic effect of concatenation in phylogenomics: the case in Pantoea
title_sort synergistic effect of concatenation in phylogenomics the case in pantoea
topic Phylogenomics
Concatenate
Super trees
Phylogenetics
Phylogenetic signal
Phylogenetic conflict
url https://peerj.com/articles/6698.pdf
work_keys_str_mv AT marikepalmer thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT stephanusnventer thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT alistairrmctaggart thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT martinpacoetzee thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT stephanievanwyk thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT juanitaravontuur thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT chrizellewbeukes thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT gerdafourie thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT quentincsantana thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT magrietavandernest thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT jochenblom thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT emmatsteenkamp thesynergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT marikepalmer synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT stephanusnventer synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT alistairrmctaggart synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT martinpacoetzee synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT stephanievanwyk synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT juanitaravontuur synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT chrizellewbeukes synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT gerdafourie synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT quentincsantana synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT magrietavandernest synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT jochenblom synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea
AT emmatsteenkamp synergisticeffectofconcatenationinphylogenomicsthecaseinpantoea