The molecular signal for the adaptation to cold temperature during early life on Earth
Open accessAbstract
Several lines of evidence such as the basal location of thermophilic lineages in large-scale phylogenetic trees and the ancestral sequence reconstruction of single enzymes or large protein concatenations support the conclusion that the ancestors of the bacterial and archaeal domains were thermophilic organisms which were adapted to hot environments during the early stages of the Earth. A parsimonious reasoning would therefore suggest that the last universal common ancestor (LUCA) was also thermophilic. Various authors have used branch-wise non-homogeneous evolutionary models that better capture the variation of molecular compositions among lineages to accurately reconstruct the ancestral G + C contents of ribosomal RNAs and the ancestral amino acid composition of highly conserved proteins. They confirmed the thermophilic nature of the ancestors of Bacteria and Archaea but concluded that LUCA, their last common ancestor, was a mesophilic organism having a moderate optimal growth temperature. In this letter, we investigate the unknown nature of the phylogenetic signal that informs ancestral sequence reconstruction to support this non-parsimonious scenario. We find that rate variation across sites of molecular sequences provides information at different time scales by recording the oldest adaptation to temperature in slow-evolving regions and subsequent adaptations in fast-evolving ones.
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Reconstructions of LUCA rRNA have shown a G + C content consistent with mesophily.
“Reconstructions of LUCA rRNA have shown a G + C content consistent with mesophily (Galtier et al. 1999;Groussin et al. 2013).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Groussin et al. 2013
G + C nucleotides are present more frequently in the rRNA of thermophiles and hyperthermophiles than in the rRNA of mesophiles.
“Due to their additional thermostability, G + C nucleotides are present more frequently in the rRNA of thermophiles and hyperthermophiles than in the rRNA of mesophiles (Galtier et al. 1999;Groussin et al. 2013).”
From Environmental Adaptation from the Origin of Life to the Last Universal Common Ancestor (2018) · cites this paper as Groussin et al. 2013
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Cites
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010) · Systematic Biology · doi:10.1093/sysbio/syq010 · Cited by 18,376 · see citing works
APE: Analyses of Phylogenetics and Evolution in R language
Paradis, E., Claude, J., & Strimmer, K. (2004) · Bioinformatics · doi:10.1093/bioinformatics/btg412 · Cited by 12,037 · see citing works
Phylogenies and the Comparative Method
Felsenstein, J. (1985) · The American Naturalist · doi:10.1086/284325 · Cited by 9,793 · see citing works
A Nonhyperthermophilic Common Ancestor to Extant Life Forms
Galtier, N., Tourasse, N., & Gouy, M. (1999) · Science · doi:10.1126/science.283.5399.220 · Cited by 442 · see citing works
Self-citationGaltier, N., & Lobry, J. R. (1997) · Journal of Molecular Evolution · doi:10.1007/pl00006186 · Cited by 441 · see citing works
Palaeotemperature trend for Precambrian life inferred from resurrected proteins
Gaucher, E. A., Govindarajan, S., & Ganesh, O. K. (2008) · Nature · doi:10.1038/nature06510 · Cited by 397 · see citing works
The archaebacterial origin of eukaryotes
Cox, C. J., Foster, P. G., Hirt, R. P., Harris, S. R., & Embley, T. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810647105 · Cited by 381 · see citing works
Galtier, N., & Gouy, M. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a025991 · Cited by 335 · see citing works
Self-citationProtein and DNA Sequence Determinants of Thermophilic Adaptation
Zeldovich, K. B., Berezovsky, I. N., & Shakhnovich, E. I. (2007) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0030005 · Cited by 325 · see citing works
Hyperthermophiles in the history of life
STETTER, K. O. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1907 · Cited by 291 · see citing works
Parallel adaptations to high temperatures in the Archaean eon
Boussau, B., Blanquart, S., Necsulea, A., Lartillot, N., & Gouy, M. (2008) · Nature · doi:10.1038/nature07393 · Cited by 242 · see citing works
Self-citationNon-homogeneous models of sequence evolution in the Bio++ suite of libraries and programs
Dutheil, J. Y., & Boussau, B. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-255 · Cited by 131 · see citing works
Self-citationGroussin, M., & Gouy, M. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr098 · Cited by 119 · see citing works
Self-citationA Branch-Heterogeneous Model of Protein Evolution for Efficient Inference of Ancestral Sequences
Groussin, M., Boussau, B., & Gouy, M. (2013) · Systematic Biology · doi:10.1093/sysbio/syt016 · Cited by 56 · see citing works
Self-citationBrooks, D. J., Fresco, J. R., & Singh, M. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth235 · Cited by 35 · see citing works
Gowri-Shankar, V., & Rattray, M. (2005) · Molecular Biology and Evolution · doi:10.1093/molbev/msj040 · Cited by 32 · see citing works
Signature of a Primitive Genetic Code in Ancient Protein Lineages
Fournier, G. P., & Gogarten, J. P. (2007) · Journal of Molecular Evolution · doi:10.1007/s00239-007-9024-x · Cited by 24 · see citing works
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Williams, T. A., Szöllősi, G. J., Spang, A., Foster, P. G., Heaps, S. E., Boussau, B., Ettema, T. J. G., & Embley, T. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1618463114 · Cited by 233 · see citing works
Self-citationThe nature of the last universal common ancestor and its impact on the early Earth system
Moody, E. R. R., Álvarez-Carretero, S., Mahendrarajah, T., Clark, J., Betts, H. C., Dombrowski, N., Szánthó, L. L., Boyle, R. A., Daines, S. J., Chen, X., et al. (2024) · Nature Ecology & Evolution · doi:10.1038/s41559-024-02461-1 · Cited by 256 · see citing works
Chemistry of Abiotic Nucleotide Synthesis
Yadav, M., Kumar, R., & Krishnamurthy, R. (2020) · Chemical Reviews · doi:10.1021/acs.chemrev.9b00546 · Cited by 225 · see citing works
The universal tree of life: an update
Forterre, P. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00717 · Cited by 186 · see citing works
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Osinski, G. R., Cockell, C., Pontefract, A., & Sapers, H. (2020) · Astrobiology · doi:10.1089/ast.2019.2203 · Cited by 179 · see citing works
Bacterial gene import and mesophilic adaptation in archaea
López‐García, P., Zivanovic, Y., Deschamps, P., & Moreira, D. (2015) · Nature Reviews Microbiology · doi:10.1038/nrmicro3485 · Cited by 112 · 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
Protein Thermodynamics Can Be Predicted Directly from Biological Growth Rates
Corkrey, R., McMeekin, T. A., Bowman, J. P., Ratkowsky, D. A., Olley, J. N., & Ross, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096100 · Cited by 50 · see citing works
Robustness of predictions of extremely thermally stable proteins in ancient organisms
Akanuma, S., Yokobori, S., Nakajima, Y., Bessho, M., & Yamagishi, A. (2015) · Evolution · doi:10.1111/evo.12779 · Cited by 43 · see citing works
Akanuma, S. (2017) · Life · doi:10.3390/life7030033 · Cited by 39 · see citing works
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Maurel, M., Leclerc, F., & Hervé, G. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.9b00457 · Cited by 25 · see citing works
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The Archean–Hadean Earth: Modern paradigms and ancient processes
Mueller, P. A., & Nutman, A. P. (2017) · Geological Society of America eBooks · doi:10.1130/2017.2523(03 · Cited by 10 · see citing works
Rao, Y.-Z., Li, Y.-X., Li, Z.-W., Qu, Y.-N., Qi, Y.-L., Jiao, J., Shu, W., Hua, Z., & Li, W. (2023) · mSystems · doi:10.1128/msystems.01252-22 · Cited by 9 · see citing works
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Zhao, F., & Akanuma, S. (2022) · Journal of Molecular Evolution · doi:10.1007/s00239-022-10078-w · Cited by 6 · see citing works
Abiotic and biotic constraints on Earth’s ancient colonisers in the Proterozoic
Mukherjee, I., Corkrey, R., Large, R. R., & Danyushevsky, L. V. (2023) · Precambrian Research · doi:10.1016/j.precamres.2023.107089 · Cited by 5 · see citing works
Radványi, Á., & Kun, Á. (2021) · Life · doi:10.3390/life11080773 · Cited by 5 · see citing works
Chu, X., Chen, S.-M., Zhao, K., Tian, T., Gao, J., & Zhang, H. (2021) · Life · doi:10.3390/life11080738 · Cited by 4 · see citing works
Was LUCA a Hyperthermophilic Prokaryote? The Impact-Bottleneck Hypothesis Revisited
Pérez-Morales, G., & Delaye, L. (2020) · Cuatro ciénegas basin: an endangered hyperdiverse oasis · doi:10.1007/978-3-030-46087-7_3 · Cited by 3 · see citing works
Learning About Protein Stability and Functional Activity From Ancestral Reconstruction
Akanuma, S. (2025) · Journal of Molecular Biology · doi:10.1016/j.jmb.2025.169435 · Cited by 2 · see citing works
Immobilized Ancient Lipase for Waste-to-Fuel Biocatalysis: Toward Sustainable Biodiesel Production
Saad, A. H. M., Kamarudin, N. H. A., Leow, T. C., Mohamed, M. S., & Ali, M. S. M. (2025) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-025-05392-0 · Cited by 2 · see citing works
Reconstructing the Last Common Ancestor: Epistemological and Empirical Challenges
Estrada, A., Suárez‐Díaz, E., & Becerra, A. (2022) · Acta Biotheoretica · doi:10.1007/s10441-022-09439-1 · Cited by 3 · see citing works
Chemosynthetic carbon metabolism in thermophiles
Urschel, M. R. (2015) · Montana State University ScholarWorks (Montana State University)
Rao, Y.-Z., Li, Y.-X., Li, Z.-W., Qu, Y.-N., Qi, Y.-L., Jiao, J., Shu, W., Hua, Z., & Li, W. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.14.520523
Assessing the Earliest Evidence for Life in the Geologic and Genomic Records
Bell, E. A., & Fournier, G. P. (2026) · Astrobiology · doi:10.1177/15311074261454242
Lv, Z., Wang, Y., & Wang, Y. (2026) · The Innovation Life · doi:10.59717/j.xinn-life.2026.100235
- Authors
- Groussin, M., Boussau, B., Charles, S., Blanquart, S., & Gouy, M.
- Affiliations
- Lyon 1 Université (FR)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Groussin, Mathieu
- Venue
- Biology Letters
- Publisher
- The Royal Society
- Published
- 2013-10-23
- Volume
- 9
- Issue
- 5
- Pages
- 20130608-20130608
- ISSN
- 1744-9561 (ISSN-L)
- 1744-957X
- PMC
- PMC3971708
- OpenAlex
- W1991171677
- Cited by
- 29
- References
- 17
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 3 · 2019: 1 · 2017: 4 · 2016: 1 · 2015: 4 · 2014: 1
- FWCI
- 0.90
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Biology Letters (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- LillOA (Université de Lille (University Of Lille)) (submittedVersion, other-oa)
- Funders
- Agence Nationale de la Recherche
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- 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
- Keywords
- last universal common ancestor, cold adaptation, ancestral sequence reconstruction, ribosomal RNA, amino acid composition, early life on Earth, phylogenetic signal
- MeSH terms
- Adaptation, Physiological, Cold Temperature, Models, Theoretical, Phylogeny, Earth, Planet, Life
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