Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Parallel adaptations to high temperatures in the Archaean eon

Abstract

Fossils of organisms dating from the origin and diversification of cellular life are scant and difficult to interpret1, for this reason alternative means to investigate the ecology of the last universal common ancestor (LUCA) and of the ancestors of the three domains of life are of great scientific value. It was recently recognized that the effects of temperature on ancestral organisms left ‘genetic footprints’ that could be uncovered in extant genomes2,3,4. Accordingly, analyses of resurrected proteins predicted that the bacterial ancestor was thermophilic and that Bacteria subsequently adapted to lower temperatures3,4. As the archaeal ancestor is also thought to have been thermophilic5, the LUCA was parsimoniously inferred as thermophilic too. However, an analysis of ribosomal RNAs supported the hypothesis of a non-hyperthermophilic LUCA2. Here we show that both rRNA and protein sequences analysed with advanced, realistic models of molecular evolution6,7 provide independent support for two environmental-temperature-related phases during the evolutionary history of the tree of life. In the first period, thermotolerance increased from a mesophilic LUCA to thermophilic ancestors of Bacteria and of Archaea–Eukaryota; in the second period, it decreased. Therefore, the two lineages descending from the LUCA and leading to the ancestors of Bacteria and Archaea–Eukaryota convergently adapted to high temperatures, possibly in response to a climate change of the early Earth1,8,9, and/or aided by the transition from an RNA genome in the LUCA to organisms with more thermostable DNA genomes10,11. This analysis unifies apparently contradictory results2,3,4 into a coherent depiction of the evolution of an ecological trait over the entire tree of life.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Correlations between sequence compositions and OGT, and estimates of key ancestral compositions.
Figure 2: Evolution of thermophily over the tree of life.

References

  1. 1

    Nisbet, E. G. & Sleep, N. H. The habitat and nature of early life. Nature 409, 1083–1091 (2001)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Galtier, N., Tourasse, N. & Gouy, M. A nonhyperthermophilic common ancestor to extant life forms. Science 283, 220–221 (1999)

    CAS  Article  Google Scholar 

  3. 3

    Gaucher, E. A., Thomson, J. M., Burgan, M. F. & Benner, S. A. Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425, 285–288 (2003)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Gaucher, E. A. Govindara jan, S. & Ganesh, O. K. Palaeotemperature trend for precambrian life inferred from resurrected proteins. Nature 451, 704–707 (2008)

    ADS  CAS  Article  Google Scholar 

  5. 5

    Gribaldo, S. & Brochier-Armanet, C. The origin and evolution of archaea: a state of the art. Phil. Trans. R. Soc. Lond. B 361, 1007–1022 (2006)

    CAS  Article  Google Scholar 

  6. 6

    Blanquart, S. & Lartillot, N. A site- and time-heterogeneous model of amino-acid replacement. Mol. Biol. Evol. 25, 842–858 (2008)

    CAS  Article  Google Scholar 

  7. 7

    Boussau, B. & Gouy, M. Efficient likelihood computations with nonreversible models of evolution. Syst. Biol. 55, 756–768 (2006)

    Article  Google Scholar 

  8. 8

    Sleep, N. H., Zahnle, K. J., Kasting, J. F. & Morowitz, H. J. Annihilation of ecosystems by large asteroid impacts on the early Earth. Nature 342, 139–142 (1989)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Gogarten-Boekels, M., Hilario, E. & Gogarten, J. P. The effects of heavy meteorite bombardment on the early evolution–the emergence of the three domains of life. Orig. Life Evol. Biosph. 25, 251–264 (1995)

    ADS  CAS  Article  Google Scholar 

  10. 10

    Mushegian, A. R. & Koonin, E. V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl Acad. Sci. USA 93, 10268–10273 (1996)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Forterre, P. The origin of DNA genomes and DNA replication proteins. Curr. Opin. Microbiol. 5, 525–532 (2002)

    CAS  Article  Google Scholar 

  12. 12

    Galtier, N. & Lobry, J. R. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J. Mol. Evol. 44, 632–636 (1997)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Di Giulio, M. The universal ancestor and the ancestor of bacteria were hyperthermophiles. J. Mol. Evol. 57, 721–730 (2003)

    ADS  Article  Google Scholar 

  14. 14

    Brooks, D. J., Fresco, J. R. & Singh, M. A novel method for estimating ancestral amino acid composition and its application to proteins of the Last Universal Ancestor. Bioinformatics 20, 2251–2257 (2004)

    CAS  Article  Google Scholar 

  15. 15

    Zeldovich, K. B., Berezovsky, I. N. & Shakhnovich, E. I. Protein and DNA sequence determinants of thermophilic adaptation. PLoS Comput. Biol. 3, 62–72 (2007)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Gowri-Shankar, V. & Rattray, M. On the correlation between composition and site-specific evolutionary rate: implications for phylogenetic inference. Mol. Biol. Evol. 23, 352–364 (2005)

    Article  Google Scholar 

  17. 17

    Blanquart, S. & Lartillot, N. A Bayesian compound stochastic process for modeling nonstationary and nonhomogeneous sequence evolution. Mol. Biol. Evol. 23, 2058–2071 (2006)

    CAS  Article  Google Scholar 

  18. 18

    Lartillot, N. & Philippe, H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095–1109 (2004)

    CAS  Article  Google Scholar 

  19. 19

    Zhaxybayeva, O., Lapierre, P. & Gogarten, J. P. Ancient gene duplications and the root(s) of the tree of life. Protoplasma 227, 53–64 (2005)

    Article  Google Scholar 

  20. 20

    Fournier, G. P. & Gogarten, J. P. Signature of a primitive genetic code in ancient protein lineages. J. Mol. Evol. 65, 425–436 (2007)

    ADS  CAS  Article  Google Scholar 

  21. 21

    Lanave, C., Preparata, G., Saccone, C. & Serio, G. A new method for calculating evolutionary substitution rates. J. Mol. Evol. 20, 86–93 (1984)

    ADS  CAS  Article  Google Scholar 

  22. 22

    Williams, P. D., Pollock, D. D., Blackburne, B. P. & Goldstein, R. A. Assessing the accuracy of ancestral protein reconstruction methods. PLoS Comput. Biol. 2, 598–605 (2006)

    CAS  Article  Google Scholar 

  23. 23

    Graur, D. & Martin, W. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet. 20, 80–86 (2004)

    CAS  Article  Google Scholar 

  24. 24

    Robert, F. & Chaussidon, M. A palaeotemperature curve for the Precambrian oceans based on silicon isotopes in cherts. Nature 443, 969–972 (2006)

    ADS  CAS  Article  Google Scholar 

  25. 25

    Shields, G. A. & Kasting, J. F. Evidence for hot early oceans? Nature 447, E1 (2007)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Kasting, J. F. & Ono, S. Palaeoclimates: the first two billion years. Phil. Trans. R. Soc. Lond. B 361, 917–929 (2006)

    CAS  Article  Google Scholar 

  27. 27

    Gomes, R., Levison, H. F., Tsiganis, K. & Morbidelli, A. Origin of the cataclysmic Late Heavy Bombardment period of the terrestrial planets. Nature 435, 466–469 (2005)

    ADS  CAS  Article  Google Scholar 

  28. 28

    Rosing, M. T. 13C-depleted carbon microparticles in >3700-Ma sea-floor sedimentary rocks from West Greenland. Science 283, 674–676 (1999)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Islas, S., Velasco, A. M., Becerra, A., Delaye, L. & Lazcano, A. Hyperthermophily and the origin and earliest evolution of life. Int. Microbiol. 6, 87–94 (2003)

    CAS  Article  Google Scholar 

  30. 30

    Naya, H., Romero, H., Zavala, A., Alvarez, B. & Musto, H. Aerobiosis increases the genomic guanine plus cytosine content (GC%) in prokaryotes. J. Mol. Evol. 55, 260–264 (2002)

    ADS  CAS  Article  Google Scholar 

  31. 31

    Moreira, D. et al. Global eukaryote phylogeny: Combined small- and large-subunit ribosomal DNA trees support monophyly of Rhizaria, Retaria and Excavata. Mol. Phylogenet. Evol. 44, 255–266 (2007)

    CAS  Article  Google Scholar 

  32. 32

    Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004)

    Article  Google Scholar 

  33. 33

    Philippe, H. MUST, a computer package of management utilities for sequences and trees. Nucleic Acids Res. 21, 5264–5272 (1993)

    CAS  Article  Google Scholar 

  34. 34

    Felsenstein, J. PHYLIP (Phylogeny Inference Package) version 3.6. (Department of Genome Sciences, 2005)

    Google Scholar 

  35. 35

    Wuyts, J., Perrière, G. & Van De Peer, Y. The European ribosomal RNA database. Nucleic Acids Res. 32, D101–D103 (2004)

    CAS  Article  Google Scholar 

  36. 36

    Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402 (1997)

    CAS  Article  Google Scholar 

  37. 37

    Saitou, N. & Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425 (1987)

    CAS  PubMed  Google Scholar 

  38. 38

    Galtier, N., Gouy, M. & Gautier, C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput. Appl. Biosci. 12, 543–548 (1996)

    CAS  PubMed  Google Scholar 

  39. 39

    Wolf, Y. I., Aravind, L., Grishin, N. V. & Koonin, E. V. Evolution of aminoacyl-trna synthetases–analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res. 9, 689–710 (1999)

    CAS  PubMed  Google Scholar 

  40. 40

    Roure, B., Rodriguez-Ezpeleta, N. & Philippe, H. SCaFoS: a tool for selection, concatenation and fusion of sequences for phylogenomics. BMC Evol. Biol. 7 (Suppl 1). S2 (2007)

    Article  Google Scholar 

  41. 41

    Hill, M. O. Correspondence analysis: a neglected multivariate method. Appl. Statist. 23, 340–354 (1974)

    MathSciNet  Article  Google Scholar 

  42. 42

    Chessel, D., Dufour, A. B. & Thioulouse, J. The ade4 package -I- one-table methods. R. News 4, 5–10 (2004)

    Google Scholar 

  43. 43

    Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

    Article  Google Scholar 

  44. 44

    Anisimova, M. & Gascuel, O. Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst. Biol. 55, 539–552 (2006)

    Article  Google Scholar 

  45. 45

    Huelsenbeck, J. P. & Ronquist, F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755 (2001)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by Action Concertée Incitative IMPBIO-MODELPHYLO and ANR PlasmoExplore. We thank C. Brochier-Armanet and A. Lazcano for help and suggestions, the LIRMM Bioinformatics platform ATGC and the computing facilities of IN2P3.

Author Contributions B.B. and S.B. contributed equally to this study, designing and conducting experiments. A.N. performed statistical analyses and retrieved optimal growth temperatures. N.L. and M.G. provided guidance throughout the study, and M.G. gave the original idea. All authors participated in manuscript writing.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Manolo Gouy.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-36 with Legends, Supplementary Tables 1 – 3, Supplementary Discussion, and additional references. (PDF 1691 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Boussau, B., Blanquart, S., Necsulea, A. et al. Parallel adaptations to high temperatures in the Archaean eon. Nature 456, 942–945 (2008). https://doi.org/10.1038/nature07393

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing