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Rapid evolutionary innovation during an Archaean genetic expansion

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.

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

    Rasmussen, B., Fletcher, I. R., Brocks, J. J. & Kilburn, M. R. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455, 1101–1104 (2008)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Dupont, C. L., Yang, S., Palenik, B. & Bourne, P. E. Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry. Proc. Natl Acad. Sci. USA 103, 17822–17827 (2006)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. 4

    Dupont, C. L., Butcher, A., Valas, R. E., Bourne, P. E. & Caetano-Anollés, G. History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc. Natl Acad. Sci. USA 107, 10567–10572 (2010)

    ADS  CAS  Article  Google Scholar 

  5. 5

    Saito, M. A., Sigman, D. M. & Morel, F. M. M. The bioinorganic chemistry of the ancient ocean: the co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean–Proterozoic boundary? Inorg. Chim. Acta 356, 308–318 (2003)

    CAS  Article  Google Scholar 

  6. 6

    Zerkle, A. L., House, C. H. & Brantley, S. L. Biogeochemical signatures through time as inferred from whole microbial genomes. Am. J. Sci. 305, 467–502 (2005)

    ADS  CAS  Article  Google Scholar 

  7. 7

    De Marais, D. J. When did photosynthesis emerge on Earth? Science 289, 1703–1705 (2000)

    CAS  PubMed  Google Scholar 

  8. 8

    Brocks, J. J., Logan, G. A., Buick, R. & Summons, R. E. Archean molecular fossils and the early rise of eukaryotes. Science 285, 1033–1036 (1999)

    CAS  Article  Google Scholar 

  9. 9

    Gogarten, J. P., Doolittle, W. F. & Lawrence, J. G. Prokaryotic evolution in light of gene transfer. Mol. Biol. Evol. 19, 2226–2238 (2002)

    CAS  Article  Google Scholar 

  10. 10

    Jain, R., Rivera, M. C. & Lake, J. A. Horizontal gene transfer among genomes: the complexity hypothesis. Proc. Natl Acad. Sci. USA 96, 3801–3806 (1999)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Ragan, M. A. & Beiko, R. G. Lateral genetic transfer: open issues. Phil. Trans. R. Soc. Lond. B 364, 2241–2251 (2009)

    CAS  Article  Google Scholar 

  12. 12

    Ochman, H., Lawrence, J. G. & Groisman, E. A. Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304 (2000)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Fischer, D. & Eisenberg, D. Finding families for genomic ORFans. Bioinformatics 15, 759–762 (1999)

    CAS  Article  Google Scholar 

  14. 14

    Yang, D., Oyaizu, Y., Oyaizu, H., Olsen, G. J. & Woese, C. R. Mitochondrial origins. Proc. Natl Acad. Sci. USA 82, 4443–4447 (1985)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Giovannoni, S. J. et al. Evolutionary relationships among cyanobacteria and green chloroplasts. J. Bacteriol. 170, 3584–3592 (1988)

    CAS  Article  Google Scholar 

  16. 16

    Scott, C. et al. Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452, 456–459 (2008)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Konhauser, K. O. et al. Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event. Nature 458, 750–753 (2009)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Garvin, J., Buick, R., Anbar, A. D., Arnold, G. L. & Kaufman, A. J. Isotopic evidence for an aerobic nitrogen cycle in the latest Archean. Science 323, 1045–1048 (2009)

    ADS  CAS  Article  Google Scholar 

  19. 19

    Canfield, D. E. A new model for Proterozoic ocean chemistry. Nature 396, 450–453 (1998)

    ADS  CAS  Article  Google Scholar 

  20. 20

    Waldbauer, J. R., Sherman, L. S., Sumner, D. Y. & Summons, R. E. Late Archean molecular fossils from the Transvaal Supergroup record the antiquity of microbial diversity and aerobiosis. Precambr. Res. 169, 28–47 (2009)

    ADS  CAS  Article  Google Scholar 

  21. 21

    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 

  22. 22

    Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302 (2003)

    CAS  Article  Google Scholar 

  23. 23

    Ciccarelli, F. D. et al. Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283–1287 (2006)

    ADS  CAS  Article  Google Scholar 

  24. 24

    Alm, E., Huang, K. & Arkin, A. The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLOS Comput. Biol. 2, e143 (2006)

    ADS  Article  Google Scholar 

  25. 25

    Kunin, V. & Ouzounis, C. A. The balance of driving forces during genome evolution in prokaryotes. Genome Res. 13, 1589–1594 (2003)

    CAS  Article  Google Scholar 

  26. 26

    Snel, B., Bork, P. & Huynen, M. A. Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res. 12, 17–25 (2002)

    CAS  Article  Google Scholar 

  27. 27

    Kanehisa, M. & Goto, S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28, 27–30 (2000)

    CAS  Article  Google Scholar 

  28. 28

    Alm, E. J. et al. The MicrobesOnline Web site for comparative genomics. Genome Res. 15, 1015–1022 (2005)

    CAS  Article  Google Scholar 

Download references

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.

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

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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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David, L., Alm, E. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469, 93–96 (2011). https://doi.org/10.1038/nature09649

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