Rapid evolutionary innovation during an Archaean genetic expansion

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Abstract

The natural history of Precambrian life is still unknown because of the rarity of microbial fossils and biomarkers1,2. However, the composition of modern-day genomes may bear imprints of ancient biogeochemical events3,4,5,6. Here we use an explicit model of macroevolution including gene birth, transfer, duplication and loss events to map the evolutionary history of 3,983 gene families across the three domains of life onto a geological timeline. Surprisingly, we find that a brief period of genetic innovation during the Archaean eon, which coincides with a rapid diversification of bacterial lineages, gave rise to 27% of major modern gene families. A functional analysis of genes born during this Archaean expansion reveals that they are likely to be involved in electron-transport and respiratory pathways. Genes arising after this expansion show increasing use of molecular oxygen (P = 3.4 × 10−8) and redox-sensitive transition metals and compounds, which is consistent with an increasingly oxygenating biosphere.

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Figure 1: Rates of macroevolutionary events over time.
Figure 2: Genome utilization of redox-sensitive compounds over time.

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Acknowledgements

We thank M. Polz, E. Delong, J. Waldbauer and T. Lyons for suggestions to improve this manuscript. This work is supported by the US Department of Energy ENIGMA project through contract DE-AC02-05CH11231, the National Science Foundation under an Assembling the Tree of Life Award, and a National Defense Science and Engineering Graduate Fellowship.

Author information

L.D. and E.A. designed the analysis. L.D. performed the analysis. L.D. and E.A. wrote the manuscript.

Correspondence to Eric J. Alm.

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The authors declare no competing financial interests.

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The file contains Supplementary Methods, Supplementary Figures 1-15 with legends, Supplementary Tables 1-2 and additional references. (PDF 2466 kb)

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