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Parallel adaptations to high temperatures in the Archaean eon

Nature volume 456, pages 942–945 (2008)Cite this article

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.

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

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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

Author notes

  1. Nicolas Lartillot

    Present address: Present address: Département de Biochimie, Université de Montréal, C.P. 6128, succursale Centre-Ville, Montréal QC H3C3J7, Canada.,

  2. Bastien Boussau and Samuel Blanquart: These authors contributed equally to this work.

Authors and Affiliations

  1. Laboratoire de Biométrie et Biologie Evolutive, CNRS, Université de Lyon, Université Lyon I, 43 Boulevard du 11 Novembre, 69622 Villeurbanne, France ,

    Bastien Boussau, Anamaria Necsulea & Manolo Gouy

  2. LIRMM, CNRS, 161 rue Ada, 34392 Montpellier, France ,

    Samuel Blanquart & Nicolas Lartillot

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  1. Bastien Boussau
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Correspondence to Manolo Gouy.

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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

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