Comparative Analysis of RNA Families Reveals Distinct Repertoires for Each Domain of Life
Open accessAbstract
The RNA world hypothesis, that RNA genomes and catalysts preceded DNA genomes and genetically-encoded protein catalysts, has been central to models for the early evolution of life on Earth. A key part of such models is continuity between the earliest stages in the evolution of life and the RNA repertoires of extant lineages. Some assessments seem consistent with a diverse RNA world, yet direct continuity between modern RNAs and an RNA world has not been demonstrated for the majority of RNA families, and, anecdotally, many RNA functions appear restricted in their distribution. Despite much discussion of the possible antiquity of RNA families, no systematic analyses of RNA family distribution have been performed. To chart the broad evolutionary history of known RNA families, we performed comparative genomic analysis of over 3 million RNA annotations spanning 1446 families from the Rfam 10 database. We report that 99% of known RNA families are restricted to a single domain of life, revealing discrete repertoires for each domain. For the 1% of RNA families/clans present in more than one domain, over half show evidence of horizontal gene transfer (HGT), and the rest show a vertical trace, indicating the presence of a complex protein synthesis machinery in the Last Universal Common Ancestor (LUCA) and consistent with the evolutionary history of the most ancient protein-coding genes. However, with limited interdomain transfer and few RNA families exhibiting demonstrable antiquity as predicted under RNA world continuity, our results indicate that the majority of modern cellular RNA repertoires have primarily evolved in a domain-specific manner.
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Several RNA families have patterns of vertical inheritance consistent with their origin before LUCA.
“Comparative analysis of RNA families indicates that, while most RNA families are domain-specific, several RNA families have patterns of vertical inheritance consistent with their origin pre-LUCA.”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Hoeppner et al. 2012
Cellularity and cell membranes emerged prior to LUCA.
“By extension, this evidence, together with analysis indicating that signal recognition particle RNA was present in LUCA, strongly supports cellularity and cell membranes emerging prior to LUCA (Gogarten and Taiz 1992;Kawamura et al. 2005;Hoeppner et al. 2012;Harris et al. 2003;Jékely 2006).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Hoeppner et al. 2012
A fairly complex protein synthesis system existed before LUCA.
“This indicates a fairly complex protein synthesis system existed pre-LUCA (Hoeppner et al. 2012).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Hoeppner et al. 2012
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Olendzenski, L., & Gogarten, J. P. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04998.x · Cited by 34 · see citing works
3 The Genomic Tag Hypothesis: What Molecular Fossils Tell Us about the Evolution of tRNA
Maizels, N., & Weiner, A. M. (1999) · doi:10.1101/087969589.37.79 · Cited by 28 · see citing works
Chen, X. S., White, W. T. J., Collins, L. J., & Penny, D. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003106 · Cited by 23 · see citing works
Gaspin, C., Cavaillé, J., Erauso, G., et al. (2000) · HAL (Le Centre pour la Communication Scientifique Directe) · Cited by 19 · see citing works
Ribozyme Catalysis of Metabolism in the RNA World
Chen, X., Li, N., & Ellington, A. D. (2007) · ChemInform · doi:10.1002/chin.200726267 · Cited by 8 · see citing works
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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
- Authors
- Hoeppner, M. P., Gardner, P. P., & Poole, A. M.
- Affiliations
- Uppsala University (SE)
- University of Canterbury (NZ)
- Corresponding author
- Hoeppner, Marc P.
- Gardner, Paul P.
- Poole, Anthony M.
- Venue
- PLoS Computational Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-11-01
- Volume
- 8
- Issue
- 11
- Pages
- e1002752
- ISSN
- 1553-734X (ISSN-L)
- 1553-7358
- PMC
- PMC3486863
- OpenAlex
- W2100049196
- Cited by
- 62
- References
- 114
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 3 · 2023: 1 · 2022: 2 · 2021: 6 · 2020: 1 · 2019: 2 · 2018: 6 · 2017: 4 · 2016: 7 · 2015: 9 · 2014: 7 · 2013: 5 · 2012: 2
- FWCI
- 2.95
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Computational Biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- arXiv (Cornell University) (submittedVersion)
- KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- UC Research Repository (University of Canterbury) (submittedVersion)
- arXiv (Cornell University) (cc-by)
- Funders
- Wellcome Trust (WT077044/Z/05/Z)
- Royal Society
- Royal Society Te Apārangi
- Royal Swedish Academy of Sciences
- Knut och Alice Wallenbergs Stiftelse
- Stockholms Universitet
- Marsden Fund (09-UOC-013)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- RNA families, RNA world, domains of life, horizontal gene transfer, last universal common ancestor, origin of life, RNA evolution, Rfam, comparative genomics, protein synthesis machinery
- MeSH terms
- Archaea, Bacteria, Phylogeny, RNA, Genome, Evolution, Molecular, Genomics, Databases, Nucleic Acid, Eukaryota
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 ›
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