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Title: Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria

Abstract

Prokaryotic genomes are often considered to be mosaics of genes that do not necessarily share the same evolutionary history due to widespread horizontal gene transfers (HGTs). Consequently, representing evolutionary relationships of prokaryotes as bifurcating trees has long been controversial. However, studies reporting conflicts among gene trees derived from phylogenomic data sets have shown that these conflicts can be the result of artifacts or evolutionary processes other than HGT, such as incomplete lineage sorting, low phylogenetic signal, and systematic errors due to substitution model misspecification. Here, we present the results of an extensive exploration of phylogenetic conflicts in the cyanobacterial order Nostocales, for which previous studies have inferred strongly supported conflicting relationships when using different concatenated phylogenomic data sets. We found that most of these conflicts are concentrated in deep clusters of short internodes of the Nostocales phylogeny, where the great majority of individual genes have low resolving power. We then inferred phylogenetic networks to detect HGT events while also accounting for incomplete lineage sorting. Our results indicate that most conflicts among gene trees are likely due to incomplete lineage sorting linked to an ancient rapid radiation, rather than to HGTs. Moreover, the short internodes of this radiation fit the expectationsmore » of the anomaly zone, i.e., a region of the tree parameter space where a species tree is discordant with its most likely gene tree. In this work, we demonstrated that concatenation of different sets of loci can recover up to 17 distinct and well-supported relationships within the putative anomaly zone of Nostocales, corresponding to the observed conflicts among well-supported trees based on concatenated data sets from previous studies. Our findings highlight the important role of rapid radiations as a potential cause of strongly conflicting phylogenetic relationships when using phylogenomic data sets of bacteria. We propose that polytomies may be the most appropriate phylogenetic representation of these rapid radiations that are part of anomaly zones, especially when all possible genomic markers have been considered to infer these phylogenies.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [1]; ORCiD logo [1]
+ Show Author Affiliations
  1. Duke Univ., Durham, NC (United States)
  2. Univ. of Liege, (Belgium)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  4. Univ. of Liege, (Belgium); Sciensano, Brussels (Belgium)
  5. Botanical Research Institute of Texas, Fort Worth, TX (United States)
  6. North Carolina State University, Raleigh, NC (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE; National Science Foundation (NSF)
OSTI Identifier:
1972571
Grant/Contract Number:  
AC05-00OR22725; BEE 1929994
Resource Type:
Accepted Manuscript
Journal Name:
Systematic Biology
Additional Journal Information:
Journal Volume: 72; Journal Issue: 3; Journal ID: ISSN 1063-5157
Publisher:
Society of Systematic Biologists - Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; anomaly zone; bacteria; horizontal gene transfer; incomplete lineage sorting; Nostocales; phylogenomic conflict; rapid radiation; Rhizonema

Citation Formats

Pardo-De la Hoz, Carlos J., Magain, Nicolas, Piatkowski, Bryan, Cornet, Luc, Dal Forno, Manuela, Carbone, Ignazio, Miadlikowska, Jolanta, and Lutzoni, François. Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria. United States: N. p., 2023. Web. doi:10.1093/sysbio/syad008.
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Pardo-De la Hoz, Carlos J., Magain, Nicolas, Piatkowski, Bryan, Cornet, Luc, Dal Forno, Manuela, Carbone, Ignazio, Miadlikowska, Jolanta, & Lutzoni, François. Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria. United States. https://doi.org/10.1093/sysbio/syad008
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Pardo-De la Hoz, Carlos J., Magain, Nicolas, Piatkowski, Bryan, Cornet, Luc, Dal Forno, Manuela, Carbone, Ignazio, Miadlikowska, Jolanta, and Lutzoni, François. Fri . "Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria". United States. https://doi.org/10.1093/sysbio/syad008. https://www.osti.gov/servlets/purl/1972571.
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@article{osti_1972571,
title = {Ancient Rapid Radiation Explains Most Conflicts Among Gene Trees and Well-Supported Phylogenomic Trees of Nostocalean Cyanobacteria},
author = {Pardo-De la Hoz, Carlos J. and Magain, Nicolas and Piatkowski, Bryan and Cornet, Luc and Dal Forno, Manuela and Carbone, Ignazio and Miadlikowska, Jolanta and Lutzoni, François},
abstractNote = {Prokaryotic genomes are often considered to be mosaics of genes that do not necessarily share the same evolutionary history due to widespread horizontal gene transfers (HGTs). Consequently, representing evolutionary relationships of prokaryotes as bifurcating trees has long been controversial. However, studies reporting conflicts among gene trees derived from phylogenomic data sets have shown that these conflicts can be the result of artifacts or evolutionary processes other than HGT, such as incomplete lineage sorting, low phylogenetic signal, and systematic errors due to substitution model misspecification. Here, we present the results of an extensive exploration of phylogenetic conflicts in the cyanobacterial order Nostocales, for which previous studies have inferred strongly supported conflicting relationships when using different concatenated phylogenomic data sets. We found that most of these conflicts are concentrated in deep clusters of short internodes of the Nostocales phylogeny, where the great majority of individual genes have low resolving power. We then inferred phylogenetic networks to detect HGT events while also accounting for incomplete lineage sorting. Our results indicate that most conflicts among gene trees are likely due to incomplete lineage sorting linked to an ancient rapid radiation, rather than to HGTs. Moreover, the short internodes of this radiation fit the expectations of the anomaly zone, i.e., a region of the tree parameter space where a species tree is discordant with its most likely gene tree. In this work, we demonstrated that concatenation of different sets of loci can recover up to 17 distinct and well-supported relationships within the putative anomaly zone of Nostocales, corresponding to the observed conflicts among well-supported trees based on concatenated data sets from previous studies. Our findings highlight the important role of rapid radiations as a potential cause of strongly conflicting phylogenetic relationships when using phylogenomic data sets of bacteria. We propose that polytomies may be the most appropriate phylogenetic representation of these rapid radiations that are part of anomaly zones, especially when all possible genomic markers have been considered to infer these phylogenies.},
doi = {10.1093/sysbio/syad008},
journal = {Systematic Biology},
number = 3,
volume = 72,
place = {United States},
year = {Fri Feb 24 00:00:00 EST 2023},
month = {Fri Feb 24 00:00:00 EST 2023}
}
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  • The ISME Journal, Vol. 13, Issue 12
  • DOI: 10.1038/s41396-019-0481-1

To Tree or Not to Tree? Genome-Wide Quantification of Recombination and Reticulate Evolution during the Diversification of Strict Intracellular Bacteria
journal, November 2013

  • Hernández-López, Antonio; Chabrol, Olivier; Royer-Carenzi, Manuela
  • Genome Biology and Evolution, Vol. 5, Issue 12
  • DOI: 10.1093/gbe/evt178

A renaissance for the pioneering 16S rRNA gene
journal, October 2008

TreeShrink: fast and accurate detection of outlier long branches in collections of phylogenetic trees
journal, May 2018

Modeling Site Heterogeneity with Posterior Mean Site Frequency Profiles Accelerates Accurate Phylogenomic Estimation
journal, August 2017

  • Wang, Huai-Chun; Minh, Bui Quang; Susko, Edward
  • Systematic Biology, Vol. 67, Issue 2
  • DOI: 10.1093/sysbio/syx068

Metagenome Sequencing to Explore Phylogenomics of Terrestrial Cyanobacteria
journal, June 2021

  • Ward, Ryan D.; Stajich, Jason E.; Johansen, Jeffrey R.
  • Microbiology Resource Announcements, Vol. 10, Issue 22
  • DOI: 10.1128/MRA.00258-21

trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009

Empirical profile mixture models for phylogenetic reconstruction
journal, August 2008

Ancient Yersinia pestis genomes from across Western Europe reveal early diversification during the First Pandemic (541–750)
journal, June 2019

  • Keller, Marcel; Spyrou, Maria A.; Scheib, Christiana L.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 25
  • DOI: 10.1073/pnas.1820447116

GUNC: detection of chimerism and contamination in prokaryotic genomes
journal, June 2021

The Past Sure is Tense: On Interpreting Phylogenetic Divergence Time Estimates
journal, September 2017

Approximate Likelihood Calculation on a Phylogeny for Bayesian Estimation of Divergence Times
journal, February 2011

ASTRAL-Pro: Quartet-Based Species-Tree Inference despite Paralogy
journal, September 2020

  • Zhang, Chao; Scornavacca, Celine; Molloy, Erin K.
  • Molecular Biology and Evolution, Vol. 37, Issue 11
  • DOI: 10.1093/molbev/msaa139

Cyanocohniella calida gen. et sp. nov. (Cyanobacteria: Aphanizomenonaceae) a new cyanobacterium from the thermal springs from Karlovy Vary, Czech Republic
journal, October 2014

Irrational exuberance for resolved species trees: COMMENTARY
journal, December 2015

Extensive Genome-Wide Phylogenetic Discordance Is Due to Incomplete Lineage Sorting and Not Ongoing Introgression in a Rapidly Radiated Bryophyte Genus
journal, March 2021

  • Meleshko, Olena; Martin, Michael D.; Korneliussen, Thorfinn Sand
  • Molecular Biology and Evolution, Vol. 38, Issue 7
  • DOI: 10.1093/molbev/msab063

Specialized bacteriome uncovered in the coralloid roots of the epiphytic gymnosperm, Zamia pseudoparasitica
journal, January 2020

  • Bell‐Doyon, Philip; Laroche, Jérôme; Saltonstall, Kristin
  • Environmental DNA, Vol. 2, Issue 4
  • DOI: 10.1002/edn3.66

Assessing the fit of the multi-species network coalescent to multi-locus data
journal, December 2020

The All-Species Living Tree project: A 16S rRNA-based phylogenetic tree of all sequenced type strains
journal, September 2008

  • Yarza, Pablo; Richter, Michael; Peplies, Jörg
  • Systematic and Applied Microbiology, Vol. 31, Issue 4
  • DOI: 10.1016/j.syapm.2008.07.001

RAD sequencing resolves the phylogeny, taxonomy and biogeography of Trichophoreae despite a recent rapid radiation (Cyperaceae)
journal, April 2020

  • Léveillé-Bourret, Étienne; Chen, Bing-Hua; Garon-Labrecque, Marie-Ève
  • Molecular Phylogenetics and Evolution, Vol. 145
  • DOI: 10.1016/j.ympev.2019.106727

Whole-Genome Analyses Resolve the Phylogeny of Flightless Birds (Palaeognathae) in the Presence of an Empirical Anomaly Zone
journal, April 2019

  • Cloutier, Alison; Sackton, Timothy B.; Grayson, Phil
  • Systematic Biology, Vol. 68, Issue 6
  • DOI: 10.1093/sysbio/syz019

Phylogenetic analyses of cyanobacterial genomes: Quantification of horizontal gene transfer events
journal, August 2006

APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004

MAFFT version 5: improvement in accuracy of multiple sequence alignment
journal, January 2005

The Relative Importance of Modeling Site Pattern Heterogeneity Versus Partition-Wise Heterotachy in Phylogenomic Inference
journal, April 2019

  • Wang, Huai-Chun; Susko, Edward; Roger, Andrew J.
  • Systematic Biology, Vol. 68, Issue 6
  • DOI: 10.1093/sysbio/syz021

More Genes or More Taxa? The Relative Contribution of Gene Number and Taxon Number to Phylogenetic Accuracy
journal, March 2005

  • Rokas, Antonis; Carroll, Sean B.
  • Molecular Biology and Evolution, Vol. 22, Issue 5
  • DOI: 10.1093/molbev/msi121

ClipKIT: A multiple sequence alignment trimming software for accurate phylogenomic inference
journal, December 2020

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