History of biological metal utilization inferred through phylogenomic analysis of protein structures
Open accessAbstract
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.
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Loss or gain of FF or FSF can be viewed as key evolutionary events that in many cases appear to track fundamental shifts in paleomarine redox chemistry.
“The loss or gain of these FF or FSF can be viewed as key evolutionary events that in many cases appear to track fundamental shifts in paleomarine redox chemistry (Dupont et al., 2006;2010).”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2010
This drawdown would have presented a challenge for many microbial clades because Fe is the most common metal co-factor for both prokaryotes and eukaryotes.
“This would have presented a challenge for many microbial clades, as Fe is the most common metal co-factor for both prokaryotes and eukaryotes (Dupont et al., 2010).”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2010
The updated view of a relatively static paleomarine Zn reservoir contradicts earlier geochemical models that linked low Zn requirements of cyanobacteria to low Precambrian total Zn and linked eukaryotic proliferation to a Phanerozoic Zn increase.
“The updated view of a relatively static paleomarine Zn reservoir (Fig. 7) contradicts the findings of earlier geochemical models that linked (1) the low Zn requirements of cyanobacteria to the predicted low levels of total Zn in the Precambrian oceans, and also (2) the proliferation of eukaryotes to an increase in total Zn during the Phanerozoic”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2010
This modeling was consistent with the emergence of eukaryotic metalloenzymes and rapid diversification of eukaryotes in the Neoproterozoic following a transition from a widely anoxic ocean with expanded euxinia to a well-oxygenated ocean.
“This modeling work was consistent with the emergence of eukaryotic metalloenzymes and rapid diversification of eukaryotes in the Neoproterozoic following a transition from a widely anoxic ocean with expanded euxinia to a well-oxygenated ocean”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2010
The emergence of Cu-metalloproteins is thought to have been quite late.
“The emergence of Cumetalloproteins is thought to have been quite late (Dupont et al., 2010).”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2010
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- Authors
- Dupont, C. L., Butcher, A., Valas, R. E., Bourne, P. E., & Caetano-Anollés, G.
- Affiliations
- J. Craig Venter Institute (US)
- University of York (GB)
- University of California San Diego (US)
- University of California System (US)
- Evolutionary Bioinformatics Laboratory, Department of Crop Sciences, University of Illinois, Urbana–Champaign, IL 61801
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-05-24
- Volume
- 107
- Issue
- 23
- Pages
- 10567-10572
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2890839
- OpenAlex
- W2010985843
- Cited by
- 331
- References
- 53
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 22 · 2023: 21 · 2022: 18 · 2021: 27 · 2020: 17 · 2019: 17 · 2018: 19 · 2017: 18 · 2016: 14 · 2015: 26 · 2014: 18 · 2013: 16 · 2012: 32
- FWCI
- 13.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0749836)
- National Aeronautics and Space Administration
- U.S. Department of Agriculture (MCB-0749836)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- metal-binding proteins, trace elements, metal homeostasis, protein structure evolution, zinc-binding proteins, iron-binding proteins, copper-binding proteins, calcium-binding proteins, Archean ocean, early life, eukaryotic evolution, biogeochemical cycles, comparative genomics, phylogenomics
- MeSH terms
- Metalloproteins, Phylogeny, Evolution, Molecular, Proteome, Genomics
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