Protein Superfamily Evolution and the Last Universal Common Ancestor (LUCA)
Abstract
By exploiting three-dimensional structure comparison, which is more sensitive than conventional sequence-based methods for detecting remote homology, we have identified a set of 140 ancestral protein domains using very restrictive criteria to minimize the potential error introduced by horizontal gene transfer. These domains are highly likely to have been present in the Last Universal Common Ancestor (LUCA) based on their universality in almost all of 114 completed prokaryotic (Bacteria and Archaea) and eukaryotic genomes. Functional analysis of these ancestral domains reveals a genetically complex LUCA with practically all the essential functional systems present in extant organisms, supporting the theory that life achieved its modern cellular status much before the main kingdom separation (Doolittle 2000). In addition, we have calculated different estimations of the genetic and functional versatility of all the superfamilies and functional groups in the prokaryote subsample. These estimations reveal that some ancestral superfamilies have been more versatile than others during evolution allowing more genetic and functional variation. Furthermore, the differences in genetic versatility between protein families are more attributable to their functional nature rather than the time that they have been evolving. These differences in tolerance to mutation suggest that some protein families have eroded their phylogenetic signal faster than others, hiding in many cases, their ancestral origin and suggesting that the calculation of 140 ancestral domains is probably an underestimate.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
There is good evidence that LUCA's genome was small but functionally fairly comprehensive.
“However, there is good evidence that LUCA's genome was small but functionally fairly comprehensive (Mirkin et al. 2003;Ranea et al. 2006;Koonin 2003).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Ranea et al. 2006
Compartmentation existed at the time of LUCA.
“Darwinian evolution at the organismal scale requires that both lineage and heredity-a specific line of evidence strongly suggesting compartmentation at the time of LUCA (Lombard et al. 2012;Ranea et al. 2006).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Ranea et al. 2006
LUCA had nearly all the essential functional systems present in modern organisms.
“functional analysis of these superfamilies indicates that LUCA had nearly all the essential functional systems present in modern organisms (Ranea et al. 2006).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Ranea et al. 2006
The pre-LUCA histories of some gene families can be examined.
“However, the pre-LUCA histories of some gene families can be examined (eg., Mirkin et al. 2003;Ranea et al. 2006;Gogarten and Taiz 1992;Fournier et al. 2015a;Fournier et al. 2015b).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Ranea et al. 2006
Cites
Nonparametric Statistics for the Behavioral Sciences
Guitton, H., & Siegel, S. (1958) · Revue économique · doi:10.2307/3498751 · Cited by 35,281 · see citing works
The Pfam Protein Families Database
Bateman, A. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.276 · Cited by 14,062 · see citing works
(1978) · Biochemical Education · doi:10.1016/0307-4412(78)90049-3 · Cited by 5,073 · see citing works
Lateral gene transfer and the nature of bacterial innovation
Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000) · Nature · doi:10.1038/35012500 · Cited by 3,816 · see citing works
A genomic perspective on protein families.
Tatusov, R., Koonin, E., & Lipman, D. (1997) · Science · doi:10.1126/science.278.5338.631 · Cited by 3,777 · see citing works
CATH – a hierarchic classification of protein domain structures
Orengo, C., Michie, A. D., Jones, S., Jones, D., Swindells, M. B., & Thornton, J. M. (1997) · Structure · doi:10.1016/s0969-2126(97)00260-8 · Cited by 2,608 · see citing works
Self-citationThe COG database: new developments in phylogenetic classification of proteins from complete genomes
Tatusov, R. L. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.1.22 · Cited by 1,873 · see citing works
Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS
Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y., & Ishikawa, H. (2000) · Nature · doi:10.1038/35024074 · Cited by 1,338 · see citing works
Genome Streamlining in a Cosmopolitan Oceanic Bacterium
Giovannoni, S. J., Tripp, H. J., Givan, S. A., Podar, M., Vergin, K. L., Baptista, D., Bibbs, L., Eads, J. R., Richardson, T. H., Noordewier, M. O., et al. (2005) · Science · doi:10.1126/science.1114057 · Cited by 1,212 · see citing works
Woese, C. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.12.6854 · Cited by 1,053 · see citing works
Deletional bias and the evolution of bacterial genomes.
Mira, A., Ochman, H., & Moran, N. (2001) · Trends in Genetics · doi:10.1016/s0168-9525(01)02447-7 · Cited by 850 · see citing works
The Pfam Protein Families Database
Bateman, A. G., Birney, E., Cerruti, L., Durbin, R. M., Etwiller, L., Eddy, S. R., Griffiths‐Jones, S., Howe, K., Marshall, M. S., & Sonnhammer, E. L. L. (2002) · PubMed Central · Cited by 764 · see citing works
Woese, C. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.132266999 · Cited by 762 · see citing works
Microbial minimalism: genome reduction in bacterial pathogens.
Moran, N. (2002) · Cell · doi:10.1016/s0092-8674(02)00665-7 · Cited by 746 · see citing works
Biochemistry — The chemical reactions of living cells
(1978) · Biochemical Education · doi:10.1016/0307-4412(78)90043-2 · Cited by 707 · see citing works
Todd, A. E., Orengo, C. A., & Thornton, J. M. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4513 · Cited by 681 · see citing works
Self-citationTaylor, W. R., & Orengo, C. A. (1989) · Journal of Molecular Biology · doi:10.1016/0022-2836(89)90084-3 · Cited by 667 · see citing works
Self-citationComparative genomics, minimal gene-sets and the last universal common ancestor
Koonin, E. V. (2003) · Nature Reviews Microbiology · doi:10.1038/nrmicro751 · Cited by 661 · see citing works
Valdar, W. S. J. (2002) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.10146 · Cited by 633 · see citing works
Mirkin, B. G., Fenner, T. I., Galperin, M. Y., & Koonin, E. V. (2003) · BMC Evolutionary Biology · doi:10.1186/1471-2148-3-2 · Cited by 368 · see citing works
Wood, E. J. (2004) · Biochemistry and Molecular Biology Education · doi:10.1002/bmb.2004.494032069994 · Cited by 363 · see citing works
Accelerated evolution associated with genome reduction in a free-living prokaryote
Dufresne, A., Garczarek, L., & Partensky, F. (2005) · Genome biology · doi:10.1186/gb-2005-6-2-r14 · Cited by 353 · see citing works
Did DNA replication evolve twice independently?
Leipe, D. D., Aravind, L., & Koonin, E. V. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.17.3389 · Cited by 351 · see citing works
Scaling laws in the functional content of genomes
van Nimwegen, E. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00203-8 · Cited by 316 · see citing works
Whole genome plasticity in pathogenic bacteria
Dobrindt, U. (2001) · Current Opinion in Microbiology · doi:10.1016/s1369-5274(00)00250-2 · Cited by 212 · see citing works
The chemical reactions of living cells
Dagley, S. (1978) · Biochemical Education · doi:10.1016/0307-4412(78)90056-0 · Cited by 153 · see citing works
The nature of the universal ancestor and the evolution of the proteome
Doolittle, W. F. (2000) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(00)00096-8 · Cited by 134 · see citing works
Systematic discovery of analogous enzymes in thiamin biosynthesis
Morett, E., Korbel, J. O., Rajan, E., et al. (2003) · Nature Biotechnology · doi:10.1038/nbt834 · Cited by 130 · see citing works
Evolution of Protein Superfamilies and Bacterial Genome Size
Ranea, J. A. G., Buchan, D. W. A., Thornton, J. M., & Orengo, C. A. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.12.044 · Cited by 108 · see citing works
Self-citationCORA—Topological fingerprints for protein structural families
Orengo, C. A. (1999) · Protein Science · doi:10.1110/ps.8.4.699 · Cited by 63 · see citing works
Self-citationComparative genomics and bioenergetics
Castresana, J. (2001) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(01)00227-4 · Cited by 61 · see citing works
Whitfield, J. (2004) · Nature · doi:10.1038/427674a · Cited by 56 · see citing works
McGuffin, L. J. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh043 · Cited by 44 · see citing works
Gene3D: structural assignments for the biologist and bioinformaticist alike
Buchan, D. W. A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg051 · Cited by 29 · see citing works
A structural perspective on genome evolution
Lee, D. K., Grant, A., Buchan, D. W. A., et al. (2003) · Current Opinion in Structural Biology · doi:10.1016/s0959-440x(03)00079-4 · Cited by 25 · see citing works
Assessing strategies for improved superfamily recognition
Sillitoe, I., Dibley, M., Bray, J. E., et al. (2005) · Protein Science · doi:10.1110/ps.041056105 · Cited by 23 · see citing works
Pentose phosphate and calvin cycles: Similarities and three‐dimensional views*
Sillero, A., Selivanov, V. A., & Cascante, M. (2006) · Biochemistry and Molecular Biology Education · doi:10.1002/bmb.2006.494034042627 · Cited by 13 · see citing works
Self-citationGenome evolution: Micro(be)-economics
Ranea, J. A. G. (2005) · Heredity · doi:10.1038/sj.hdy.6800766 · Cited by 8 · see citing works
Self-citationMicroeconomic principles explain an optimal genome size in bacteria
Ranea, J. G., Grant, A., Thornton, J. M., et al. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.11.014 · Cited by 3 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Becerra, A., Delaye, L., Islas, S., & Lazcano, A. (2007) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.38.091206.095825 · Cited by 115 · see citing works
Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor
Cantine, M. D., & Fournier, G. P. (2018) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-017-9542-5 · Cited by 54 · see citing works
Scaling laws in enzyme function reveal a new kind of biochemical universality
Gagler, D. C., Karas, B., Kempes, C. P., Malloy, J., Mierzejewski, V., Goldman, A. D., Kim, H., & Walker, S. I. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2106655119 · Cited by 34 · see citing works
- Authors
- Ranea, J. A. G., Sillero, A., Thornton, J. M., & Orengo, C. A.
- Affiliations
- University College London (GB)
- Consejo Superior de Investigaciones Científicas (ES)
- European Bioinformatics Institute (GB)
- Corresponding author
- Ranea, Juan A. G.
- Venue
- Journal of Molecular Evolution
- Published
- 2006-10
- Volume
- 63
- Issue
- 4
- Pages
- 513-525
- ISSN
- 0022-2844 (ISSN-L)
- 1432-1432
- OpenAlex
- W1973481154
- Cited by
- 122
- References
- 39
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 7 · 2023: 5 · 2022: 7 · 2021: 8 · 2020: 6 · 2019: 6 · 2018: 9 · 2017: 5 · 2016: 8 · 2015: 3 · 2014: 2 · 2013: 5 · 2012: 7
- FWCI
- 2.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Molecular Evolution (publishedVersion)
- PubMed (publishedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Keywords
- protein superfamilies, last universal common ancestor, remote homology detection, horizontal gene transfer, prokaryotic genomes, eukaryotic genomes, mutation tolerance, origin of cellular life
- MeSH terms
- Proteins, Temperature, Genetic Variation, Genome, Protein Structure, Tertiary, Evolution, Molecular, Gene Duplication
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
