Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 3 March 2006:
Vol. 311. no. 5765, pp. 1283 - 1287
DOI: 10.1126/science.1123061
Prev | Table of Contents | Next

Reports

Toward Automatic Reconstruction of a Highly Resolved Tree of Life

Francesca D. Ciccarelli,1,2,3* Tobias Doerks,1* Christian von Mering,1 Christopher J. Creevey,1 Berend Snel,4 Peer Bork1,5{dagger}

We have developed an automatable procedure for reconstructing the tree of life with branch lengths comparable across all three domains. The tree has its basis in a concatenation of 31 orthologs occurring in 191 species with sequenced genomes. It revealed interdomain discrepancies in taxonomic classification. Systematic detection and subsequent exclusion of products of horizontal gene transfer increased phylogenetic resolution, allowing us to confirm accepted relationships and resolve disputed and preliminary classifications. For example, we place the phylum Acidobacteria as a sister group of {delta}-Proteobacteria, support a Gram-positive origin of Bacteria, and suggest a thermophilic last universal common ancestor.

1 European Molecular Biology Laboratory, Meyerhofstrasse 1, 69012 Heidelberg, Germany.
2 Department of Experimental Oncology, European Institute of Oncology, Via Ripamonti 435, 20141 Milan, Italy.
3 Institute of Molecular Oncology Foundation, Fondazione Italiana per la Ricerca sul Cancro, Via Adamello 16, 20139 Milan, Italy.
4 Center for Molecular and Biomolecular Informatics, Nijmegen Center for Molecular Life Sciences, Radboud University Nijmegen Medical Center, Toernooiveld 1, 6525 ED, Nijmegen, Netherlands.
5 Max Delbrück Centrum, 13092 Berlin-Buch, Germany.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: peer.bork{at}embl.de

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Getting a better picture of microbial evolution en route to a network of genomes.
T. Dagan and W. Martin (2009)
Phil Trans R Soc B 364, 2187-2196
   Abstract »    Full Text »    PDF »
Gene and genome trees conflict at many levels.
L. S. Haggerty, F. J. Martin, D. A. Fitzpatrick, and J. O. McInerney (2009)
Phil Trans R Soc B 364, 2209-2219
   Abstract »    Full Text »    PDF »
The practice of classification and the theory of evolution, and what the demise of Charles Darwin's tree of life hypothesis means for both of them.
W. F. Doolittle (2009)
Phil Trans R Soc B 364, 2221-2228
   Abstract »    Full Text »    PDF »
6-Pyruvoyltetrahydropterin Synthase Paralogs Replace the Folate Synthesis Enzyme Dihydroneopterin Aldolase in Diverse Bacteria.
A. Pribat, L. Jeanguenin, A. Lara-Nunez, M. J. Ziemak, J. E. Hyde, V. de Crecy-Lagard, and A. D. Hanson (2009)
J. Bacteriol. 191, 4158-4165
   Abstract »    Full Text »    PDF »
Identification of a Novel System for Boron Transport: Atr1 Is a Main Boron Exporter in Yeast.
A. Kaya, H. C. Karakaya, D. E. Fomenko, V. N. Gladyshev, and A. Koc (2009)
Mol. Cell. Biol. 29, 3665-3674
   Abstract »    Full Text »    PDF »
Genomic Analysis of "Elusimicrobium minutum," the First Cultivated Representative of the Phylum "Elusimicrobia" (Formerly Termite Group 1).
D. P. R. Herlemann, O. Geissinger, W. Ikeda-Ohtsubo, V. Kunin, H. Sun, A. Lapidus, P. Hugenholtz, and A. Brune (2009)
Appl. Envir. Microbiol. 75, 2841-2849
   Abstract »    Full Text »    PDF »
Three Genomes from the Phylum Acidobacteria Provide Insight into the Lifestyles of These Microorganisms in Soils.
N. L. Ward, J. F. Challacombe, P. H. Janssen, B. Henrissat, P. M. Coutinho, M. Wu, G. Xie, D. H. Haft, M. Sait, J. Badger, et al. (2009)
Appl. Envir. Microbiol. 75, 2046-2056
   Abstract »    Full Text »    PDF »
Biochemical Features and Functional Implications of the RNA-Based T-Box Regulatory Mechanism.
A. Gutierrez-Preciado, T. M. Henkin, F. J. Grundy, C. Yanofsky, and E. Merino (2009)
Microbiol. Mol. Biol. Rev. 73, 36-61
   Abstract »    Full Text »    PDF »
Detecting gene clusters under evolutionary constraint in a large number of genomes.
X. Ling, X. He, and D. Xin (2009)
Bioinformatics 25, 571-577
   Abstract »    Full Text »    PDF »
Functional Analysis of Free Methionine-R-sulfoxide Reductase from Saccharomyces cerevisiae.
D. T. Le, B. C. Lee, S. M. Marino, Y. Zhang, D. E. Fomenko, A. Kaya, E. Hacioglu, G.-H. Kwak, A. Koc, H.-Y. Kim, et al. (2009)
J. Biol. Chem. 284, 4354-4364
   Abstract »    Full Text »    PDF »
Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria.
B. Gao, R. Mohan, and R. S. Gupta (2009)
Int J Syst Evol Microbiol 59, 234-247
   Abstract »    Full Text »    PDF »
Phylogenomic analyses of clostridia and identification of novel protein signatures that are specific to the genus Clostridium sensu stricto (cluster I).
R. S. Gupta and B. Gao (2009)
Int J Syst Evol Microbiol 59, 285-294
   Abstract »    Full Text »    PDF »
A Major Clade of Prokaryotes with Ancient Adaptations to Life on Land.
F. U. Battistuzzi and S. B. Hedges (2009)
Mol. Biol. Evol. 26, 335-343
   Abstract »    Full Text »    PDF »
Discovering Functional Novelty in Metagenomes: Examples from Light-Mediated Processes.
A. H. Singh, T. Doerks, I. Letunic, J. Raes, and P. Bork (2009)
J. Bacteriol. 191, 32-41
   Abstract »    Full Text »    PDF »
metaTIGER: a metabolic evolution resource.
J. W. Whitaker, I. Letunic, G. A. McConkey, and D. R. Westhead (2009)
Nucleic Acids Res. 37, D531-D538
   Abstract »    Full Text »    PDF »
A likelihood framework to analyse phyletic patterns.
O. Cohen, N. D Rubinstein, A. Stern, U. Gophna, and T. Pupko (2008)
Phil Trans R Soc B 363, 3903-3911
   Abstract »    Full Text »    PDF »
A Bioinformatician's Guide to Metagenomics.
V. Kunin, A. Copeland, A. Lapidus, K. Mavromatis, and P. Hugenholtz (2008)
Microbiol. Mol. Biol. Rev. 72, 557-578
   Abstract »    Full Text »    PDF »
dnaJ is a useful phylogenetic marker for alphaproteobacteria.
A. Alexandre, M. Laranjo, J. P. W. Young, and S. Oliveira (2008)
Int J Syst Evol Microbiol 58, 2839-2849
   Abstract »    Full Text »    PDF »
The Proteomic Constraint and Its Role in Molecular Evolution.
S. E. Massey (2008)
Mol. Biol. Evol. 25, 2557-2565
   Abstract »    Full Text »    PDF »
Evolutionary origins of human apoptosis and genome-stability gene networks.
M. A. A. Castro, R. J. S. Dalmolin, J. C. F. Moreira, J. C. M. Mombach, and R. M. C. de Almeida (2008)
Nucleic Acids Res. 36, 6269-6283
   Abstract »    Full Text »    PDF »
Estimation of Phylogenetic Inconsistencies in the Three Domains of Life.
V. Soria-Carrasco and J. Castresana (2008)
Mol. Biol. Evol. 25, 2319-2329
   Abstract »    Full Text »    PDF »
Intraphylum Diversity and Complex Evolution of Cyanobacterial Aminoacyl-tRNA Synthetases.
I. Luque, M. L. Riera-Alberola, A. Andujar, and J. A. G. Ochoa de Alda (2008)
Mol. Biol. Evol. 25, 2369-2389
   Abstract »    Full Text »    PDF »
A Phylogenomic Analysis of the Shikimate Dehydrogenases Reveals Broadscale Functional Diversification and Identifies One Functionally Distinct Subclass.
S. Singh, J. Stavrinides, D. Christendat, and D. S. Guttman (2008)
Mol. Biol. Evol. 25, 2221-2232
   Abstract »    Full Text »    PDF »
Large-scale reconstruction and phylogenetic analysis of metabolic environments.
E. Borenstein, M. Kupiec, M. W. Feldman, and E. Ruppin (2008)
PNAS 105, 14482-14487
   Abstract »    Full Text »    PDF »
The Deep Archaeal Roots of Eukaryotes.
N. Yutin, K. S. Makarova, S. L. Mekhedov, Y. I. Wolf, and E. V. Koonin (2008)
Mol. Biol. Evol. 25, 1619-1630
   Abstract »    Full Text »    PDF »
Signature Genes as a Phylogenomic Tool.
B. E. Dutilh, B. Snel, T. J. G. Ettema, and M. A. Huynen (2008)
Mol. Biol. Evol. 25, 1659-1667
   Abstract »    Full Text »    PDF »
Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment.
J. F. Biddle, S. Fitz-Gibbon, S. C. Schuster, J. E. Brenchley, and C. H. House (2008)
PNAS 105, 10583-10588
   Abstract »    Full Text »    PDF »
Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution.
T. Dagan, Y. Artzy-Randrup, and W. Martin (2008)
PNAS 105, 10039-10044
   Abstract »    Full Text »    PDF »
Signature, a web server for taxonomic characterization of sequence samples using signature genes.
B. E. Dutilh, Y. He, M. L. Hekkelman, and M. A. Huynen (2008)
Nucleic Acids Res. 36, W470-W474
   Abstract »    Full Text »    PDF »
High-Resolution Crystal Structure and In Vivo Function of a Kinesin-2 Homologue in Giardia intestinalis.
J. C. Hoeng, S. C. Dawson, S. A. House, M. S. Sagolla, J. K. Pham, J. J. Mancuso, J. Lowe, and W. Z. Cande (2008)
Mol. Biol. Cell 19, 3124-3137
   Abstract »    Full Text »    PDF »
The PhyLoTA Browser: Processing GenBank for Molecular Phylogenetics Research.
M. J. Sanderson, D. Boss, D. Chen, K. A. Cranston, and A. Wehe (2008)
Syst Biol 57, 335-346
   Abstract »    Full Text »    PDF »
The evolution of modularity in bacterial metabolic networks.
A. Kreimer, E. Borenstein, U. Gophna, and E. Ruppin (2008)
PNAS 105, 6976-6981
   Abstract »    Full Text »    PDF »
The evolution of the Ecdysozoa.
M. J Telford, S. J Bourlat, A. Economou, D. Papillon, and O. Rota-Stabelli (2008)
Phil Trans R Soc B 363, 1529-1537
   Abstract »    Full Text »    PDF »
The genome of Bacillus coahuilensis reveals adaptations essential for survival in the relic of an ancient marine environment.
L. D. Alcaraz, G. Olmedo, G. Bonilla, R. Cerritos, G. Hernandez, A. Cruz, E. Ramirez, C. Putonti, B. Jimenez, E. Martinez, et al. (2008)
PNAS 105, 5803-5808
   Abstract »    Full Text »    PDF »
Cell Cycle Synchrony in Giardia intestinalis Cultures Achieved by Using Nocodazole and Aphidicolin.
M. K. Poxleitner, S. C. Dawson, and W. Z. Cande (2008)
Eukaryot. Cell 7, 569-574
   Abstract »    Full Text »    PDF »
Integrating Markov Clustering and Molecular Phylogenetics to Reconstruct the Cyanobacterial Species Tree from Conserved Protein Families.
W. D. Swingley, R. E. Blankenship, and J. Raymond (2008)
Mol. Biol. Evol. 25, 643-654
   Abstract »    Full Text »    PDF »
Nanoarchaeum equitans and Ignicoccus hospitalis: New Insights into a Unique, Intimate Association of Two Archaea.
U. Jahn, M. Gallenberger, W. Paper, B. Junglas, W. Eisenreich, K. O. Stetter, R. Rachel, and H. Huber (2008)
J. Bacteriol. 190, 1743-1750
   Abstract »    Full Text »    PDF »
Coevolution of gene families in prokaryotes.
O. X. Cordero, B. Snel, and P. Hogeweg (2008)
Genome Res. 18, 462-468
   Abstract »    Full Text »    PDF »
Codon choice in genes depends on flanking sequence information--implications for theoretical reverse translation.
K. Sivaraman, A. Seshasayee, P. M. Tarwater, and A. M. Cole (2008)
Nucleic Acids Res. 36, e16
   Abstract »    Full Text »    PDF »
Testing Congruence in Phylogenomic Analysis.
J. W. Leigh, E. Susko, M. Baumgartner, and A. J. Roger (2008)
Syst Biol 57, 104-115
   Abstract »    Full Text »    PDF »
Networks of genomic co-occurrence capture characteristics of human influenza A (H3N2) evolution.
X. Du, Z. Wang, A. Wu, L. Song, Y. Cao, H. Hang, and T. Jiang (2008)
Genome Res. 18, 178-187
   Abstract »    Full Text »    PDF »
Alternative Methods for Concatenation of Core Genes Indicate a Lack of Resolution in Deep Nodes of the Prokaryotic Phylogeny.
E. Bapteste, E. Susko, J. Leigh, I. Ruiz-Trillo, J. Bucknam, and W.F. Doolittle (2008)
Mol. Biol. Evol. 25, 83-91
   Abstract »    Full Text »    PDF »
Kinesin-13 Regulates Flagellar, Interphase, and Mitotic Microtubule Dynamics in Giardia intestinalis.
S. C. Dawson, M. S. Sagolla, J. J. Mancuso, D. J. Woessner, S. A. House, L. Fritz-Laylin, and W. Z. Cande (2007)
Eukaryot. Cell 6, 2354-2364
   Abstract »    Full Text »    PDF »
Accurate gene-tree reconstruction by learning gene- and species-specific substitution rates across multiple complete genomes.
M. D. Rasmussen and M. Kellis (2007)
Genome Res. 17, 1932-1942
   Abstract »    Full Text »    PDF »
Crystal Structure of Nucleoporin Nic96 Reveals a Novel, Intricate Helical Domain Architecture.
S. Jeudy and T. U. Schwartz (2007)
J. Biol. Chem. 282, 34904-34912
   Abstract »    Full Text »    PDF »
Genome-Wide Experimental Determination of Barriers to Horizontal Gene Transfer.
R. Sorek, Y. Zhu, C. J. Creevey, M. P. Francino, P. Bork, and E. M. Rubin (2007)
Science 318, 1449-1452
   Abstract »    Full Text »    PDF »
Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world.
M. Wang, L. S. Yafremava, D. Caetano-Anolles, J. E. Mittenthal, and G. Caetano-Anolles (2007)
Genome Res. 17, 1572-1585
   Abstract »    Full Text »    PDF »
Support for the Coelomata Clade of Animals from a Rigorous Analysis of the Pattern of Intron Conservation.
J. Zheng, I. B. Rogozin, E. V. Koonin, and T. M. Przytycka (2007)
Mol. Biol. Evol. 24, 2583-2592
   Abstract »    Full Text »    PDF »
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions.
S. S. Merchant, S. E. Prochnik, O. Vallon, E. H. Harris, S. J. Karpowicz, G. B. Witman, A. Terry, A. Salamov, L. K. Fritz-Laylin, L. Marechal-Drouard, et al. (2007)
Science 318, 245-250
   Abstract »    Full Text »    PDF »
Origins of Flagellar Gene Operons and Secondary Flagellar Systems.
R. Liu and H. Ochman (2007)
J. Bacteriol. 189, 7098-7104
   Abstract »    Full Text »    PDF »
New Approaches to Phylogenetic Tree Search and Their Application to Large Numbers of Protein Alignments.
S. Whelan (2007)
Syst Biol 56, 727-740
   Abstract »    Full Text »    PDF »
Phylogeny and shared conserved inserts in proteins provide evidence that Verrucomicrobia are the closest known free-living relatives of chlamydiae.
E. Griffiths and R. S. Gupta (2007)
Microbiology 153, 2648-2654
   Abstract »    Full Text »    PDF »
Phylogenomic Analysis Supports the Monophyly of Cryptophytes and Haptophytes and the Association of Rhizaria with Chromalveolates.
J. D. Hackett, H. S. Yoon, S. Li, A. Reyes-Prieto, S. E. Rummele, and D. Bhattacharya (2007)
Mol. Biol. Evol. 24, 1702-1713
   Abstract »    Full Text »    PDF »
Supertrees Disentangle the Chimerical Origin of Eukaryotic Genomes.
D. Pisani, J. A. Cotton, and J. O. McInerney (2007)
Mol. Biol. Evol. 24, 1752-1760
   Abstract »    Full Text »    PDF »
Bioinformatics software for biologists in the genomics era.
S. Kumar and J. Dudley (2007)
Bioinformatics 23, 1713-1717
   Abstract »    Full Text »    PDF »
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization.
N. H. Putnam, M. Srivastava, U. Hellsten, B. Dirks, J. Chapman, A. Salamov, A. Terry, H. Shapiro, E. Lindquist, V. V. Kapitonov, et al. (2007)
Science 317, 86-94
   Abstract »    Full Text »    PDF »
A Robust Species Tree for the Alphaproteobacteria.
K. P. Williams, B. W. Sobral, and A. W. Dickerman (2007)
J. Bacteriol. 189, 4578-4586
   Abstract »    Full Text »    PDF »
Reconstruction of highly heterogeneous gene-content evolution across the three domains of life.
W. Iwasaki and T. Takagi (2007)
Bioinformatics 23, i230-i239
   Abstract »    Full Text »    PDF »
Targeted Access to the Genomes of Low-Abundance Organisms in Complex Microbial Communities.
M. Podar, C. B. Abulencia, M. Walcher, D. Hutchison, K. Zengler, J. A. Garcia, T. Holland, D. Cotton, L. Hauser, and M. Keller (2007)
Appl. Envir. Microbiol. 73, 3205-3214
   Abstract »    Full Text »    PDF »
The mode and tempo of genome size evolution in eukaryotes.
M. J. Oliver, D. Petrov, D. Ackerly, P. Falkowski, and O. M. Schofield (2007)
Genome Res. 17, 594-601
   Abstract »    Full Text »    PDF »
A Tree of Life Based on Protein Domain Organizations.
K. Fukami-Kobayashi, Y. Minezaki, Y. Tateno, and K. Nishikawa (2007)
Mol. Biol. Evol. 24, 1181-1189
   Abstract »    Full Text »    PDF »
Stepwise formation of the bacterial flagellar system.
R. Liu and H. Ochman (2007)
PNAS 104, 7116-7121
   Abstract »    Full Text »    PDF »
Highly Tolerated Amino Acid Substitutions Increase the Fidelity of Escherichia coli DNA Polymerase I.
E. Loh, J. Choe, and L. A. Loeb (2007)
J. Biol. Chem. 282, 12201-12209
   Abstract »    Full Text »    PDF »
High-resolution species trees without concatenation.
S. V. Edwards, L. Liu, and D. K. Pearl (2007)
PNAS 104, 5936-5941
   Abstract »    Full Text »    PDF »
Deciphering RNA structural diversity and systematic phylogeny from microbial metagenomes.
Y. Zhu, D. K. Pulukkunat, and Y. Li (2007)
Nucleic Acids Res. 35, 2283-2294
   Abstract »    Full Text »    PDF »
Assessment of phylogenomic and orthology approaches for phylogenetic inference.
B. E. Dutilh, V. van Noort, R. T. J. M. van der Heijden, T. Boekhout, B. Snel, and M. A. Huynen (2007)
Bioinformatics 23, 815-824
   Abstract »    Full Text »    PDF »
Ecdysozoan Clade Rejected by Genome-Wide Analysis of Rare Amino Acid Replacements.
I. B. Rogozin, Y. I. Wolf, L. Carmel, and E. V. Koonin (2007)
Mol. Biol. Evol. 24, 1080-1090
   Abstract »    Full Text »    PDF »
Surprising Arginine Biosynthesis: a Reappraisal of the Enzymology and Evolution of the Pathway in Microorganisms.
Y. Xu, B. Labedan, and N. Glansdorff (2007)
Microbiol. Mol. Biol. Rev. 71, 36-47
   Abstract »    Full Text »    PDF »
Quantitative Phylogenetic Assessment of Microbial Communities in Diverse Environments.
C. von Mering, P. Hugenholtz, J. Raes, S. G. Tringe, T. Doerks, L. J. Jensen, N. Ward, and P. Bork (2007)
Science 315, 1126-1130
   Abstract »    Full Text »    PDF »
Inaugural Article: Pattern pluralism and the Tree of Life hypothesis.
W. F. Doolittle and E. Bapteste (2007)
PNAS 104, 2043-2049
   Abstract »    Full Text »    PDF »
Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution.
T. Dagan and W. Martin (2007)
PNAS 104, 870-875
   Abstract »    Full Text »    PDF »
STRING 7--recent developments in the integration and prediction of protein interactions.
C. von Mering, L. J. Jensen, M. Kuhn, S. Chaffron, T. Doerks, B. Kruger, B. Snel, and P. Bork (2007)
Nucleic Acids Res. 35, D358-D362
   Abstract »    Full Text »    PDF »
Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation.
I. Letunic and P. Bork (2007)
Bioinformatics 23, 127-128
   Abstract »    Full Text »    PDF »
Nitrogen Fixation at 92{degrees}C by a Hydrothermal Vent Archaeon.
M. P. Mehta and J. A. Baross (2006)
Science 314, 1783-1786
   Abstract »    Full Text »    PDF »
Three-dimensional analysis of mitosis and cytokinesis in the binucleate parasite Giardia intestinalis.
M. S. Sagolla, S. C. Dawson, J. J. Mancuso, and W. Z. Cande (2006)
J. Cell Sci. 119, 4889-4900
   Abstract »    Full Text »    PDF »
Global Phylogeny Determined by the Combination of Protein Domains in Proteomes.
M. Wang and G. Caetano-Anolles (2006)
Mol. Biol. Evol. 23, 2444-2454
   Abstract »    Full Text »    PDF »
Non-canonical CRP sites control competence regulons in Escherichia coli and many other {gamma}-proteobacteria.
A. D. S. Cameron and R. J. Redfield (2006)
Nucleic Acids Res. 34, 6001-6014
   Abstract »    Full Text »    PDF »
Toward a More Robust Assessment of Intraspecies Diversity, Using Fewer Genetic Markers.
K. T. Konstantinidis, A. Ramette, and J. M. Tiedje (2006)
Appl. Envir. Microbiol. 72, 7286-7293
   Abstract »    Full Text »    PDF »
Phylogenetic Supermatrix Analysis of GenBank Sequences from 2228 Papilionoid Legumes.
M. M. McMahon and M. J. Sanderson (2006)
Syst Biol 55, 818-836
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)