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Research Article

History of biological metal utilization inferred through phylogenomic analysis of protein structures

Christopher L. Dupont, Andrew Butcher, Ruben E. Valas, Philip E. Bourne, and Gustavo Caetano-Anollés
PNAS June 8, 2010 107 (23) 10567-10572; https://doi.org/10.1073/pnas.0912491107
Christopher L. Dupont
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  • For correspondence: cdupont@jcvi.org gca@illinois.edu
Andrew Butcher
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Ruben E. Valas
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Philip E. Bourne
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Gustavo Caetano-Anollés
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  • For correspondence: cdupont@jcvi.org gca@illinois.edu
  1. Edited by Paul G. Falkowski, Rutgers, The State University of New Jersey, New Brunswick, NJ, and approved May 3, 2010 (received for review October 28, 2009)

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Abstract

The fundamental chemistry of trace elements dictates the molecular speciation and reactivity both within cells and the environment at large. Using protein structure and comparative genomics, we elucidate several major influences this chemistry has had upon biology. All of life exhibits the same proteome size-dependent scaling for the number of metal-binding proteins within a proteome. This fundamental evolutionary constant shows that the selection of one element occurs at the exclusion of another, with the eschewal of Fe for Zn and Ca being a defining feature of eukaryotic proteomes. Early life lacked both the structures required to control intracellular metal concentrations and the metal-binding proteins that catalyze electron transport and redox transformations. The development of protein structures for metal homeostasis coincided with the emergence of metal-specific structures, which predominantly bound metals abundant in the Archean ocean. Potentially, this promoted the diversification of emerging lineages of Archaea and Bacteria through the establishment of biogeochemical cycles. In contrast, structures binding Cu and Zn evolved much later, providing further evidence that environmental availability influenced the selection of the elements. The late evolving Zn-binding proteins are fundamental to eukaryotic cellular biology, and Zn bioavailability may have been a limiting factor in eukaryotic evolution. The results presented here provide an evolutionary timeline based on genomic characteristics, and key hypotheses can be tested by alternative geochemical methods.

  • Archean-Proterozoic
  • biogeochemistry
  • bioinorganic chemistry
  • evolution
  • metal homeostasis

Footnotes

  • 1To whom correspondence may be addressed. E-mail: cdupont{at}jcvi.org or gca{at}illinois.edu.
  • Author contributions: C.L.D., P.E.B., and G.C.-A. designed research; C.L.D., R.E.V., and G.C.-A. performed research; A.B. contributed new reagents/analytic tools; C.L.D., R.E.V., P.E.B., and G.C.-A. analyzed data; and C.L.D., P.E.B., and G.C.-A. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.0912491107/-/DCSupplemental.

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    History of biological metal utilization inferred through phylogenomic analysis of protein structures
    Christopher L. Dupont, Andrew Butcher, Ruben E. Valas, Philip E. Bourne, Gustavo Caetano-Anollés
    Proceedings of the National Academy of Sciences Jun 2010, 107 (23) 10567-10572; DOI: 10.1073/pnas.0912491107

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    History of biological metal utilization inferred through phylogenomic analysis of protein structures
    Christopher L. Dupont, Andrew Butcher, Ruben E. Valas, Philip E. Bourne, Gustavo Caetano-Anollés
    Proceedings of the National Academy of Sciences Jun 2010, 107 (23) 10567-10572; DOI: 10.1073/pnas.0912491107
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    Proceedings of the National Academy of Sciences: 107 (23)
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