Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry
Open accessAbstract
Because of the rise in atmospheric oxygen 2.3 billion years ago (Gya) and the subsequent changes in oceanic redox state over the last 2.3-1 Gya, trace metal bioavailability in marine environments has changed dramatically. Although theorized to have influenced the biological usage of metals leaving discernable genomic signals, a thorough and quantitative test of this hypothesis has been lacking. Using structural bioinformatics and whole-genome sequences, the Fe-, Zn-, Mn-, and Co-binding metallomes of 23 Archaea, 233 Bacteria, and 57 Eukarya were constructed. These metallomes reveal that the overall abundances of these metal-binding structures scale to proteome size as power laws with a unique set of slopes for each Superkingdom of Life. The differences in the power describing the abundances of Fe-, Mn-, Zn-, and Co-binding proteins in the proteomes of Prokaryotes and Eukaryotes are similar to the theorized changes in the abundances of these metals after the oxygenation of oceanic deep waters. This phenomenon suggests that Prokarya and Eukarya evolved in anoxic and oxic environments, respectively, a hypothesis further supported by structures and functions of Fe-binding proteins in each Superkingdom. Also observed is a proliferation in the diversity of Zn-binding protein structures involved in protein-DNA and protein-protein interactions within Eukarya, an event unlikely to occur in either an anoxic or euxinic environment where Zn concentrations would be vanishingly low. We hypothesize that these conserved trends are proteomic imprints of changes in trace metal bioavailability in the ancient ocean that highlight a major evolutionary shift in biological trace metal usage.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Based on eukaryotic cellular requirements, geochemical modeling, and late emergence of eukaryotic Zn metalloenzymes, it was believed that Zn concentrations in early oceans would have been a possible barrier to eukaryotic evolution.
“Similarly, based on eukaryotic cellular requirements, geochemical modeling, and the late emergence of eukaryotic Zn metalloenzymes, it was believed that Zn concentrations in the early oceans would have been a possible barrier to eukaryotic evolution (Williams and Frausto da Silva 2002;2003;Saito et al., 2003;Dupont et al., 2006;2010;Williams and Rickaby, 2012).”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2006
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., 2006
For proteins with metal-binding domains, it is possible to predict which metals occupy these domains, so evolutionary relationships between protein structures may reveal trends in metal acquisition.
“For families whose proteins contain metal-binding domains, it is possible to predict which metals occupy these domains, such that evolutionary relationships between protein structures may be used to reveal trends in metal acquisition in biological systems.”
From Trace elements at the intersection of marine biological and geochemical evolution (2016) · cites this paper as Dupont et al., 2006
Cites
Berman, H. M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.235 · Cited by 40,196 · see citing works
Murzin, A. G., Brenner, S. E., Hubbard, T., & Chothia, C. (1995) · Journal of Molecular Biology · doi:10.1016/s0022-2836(05)80134-2 · Cited by 6,412 · see citing works
The Chemical Evolution of the Atmosphere and Oceans
Holland, H. D. (1984) · doi:10.1515/9780691220239 · Cited by 1,836 · see citing works
Atmospheric Influence of Earth's Earliest Sulfur Cycle
Farquhar, J., Bao, H., & Thiemens, M. (2000) · Science · doi:10.1126/science.289.5480.756 · Cited by 1,805 · see citing works
Principles of bioinorganic chemistry
(1995) · Choice Reviews Online · doi:10.5860/choice.32-4515 · Cited by 1,538 · see citing works
Dating the rise of atmospheric oxygen
Bekker, A., Holland, H. D., Wang, P.-L., Rumble, D., Stein, H. J., Hannah, J. L., Coetzee, L. L., & Beukes, N. J. (2004) · Nature · doi:10.1038/nature02260 · Cited by 1,435 · see citing works
Archean Molecular Fossils and the Early Rise of Eukaryotes
Brocks, J. J., Logan, G. A., Buick, R., & Summons, R. E. (1999) · Science · doi:10.1126/science.285.5430.1033 · Cited by 1,275 · see citing works
A new model for Proterozoic ocean chemistry
Canfield, D. E. (1998) · Nature · doi:10.1038/24839 · Cited by 1,243 · see citing works
Gough, J., Karplus, K. J., Hughey, R., & Chothia, C. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.5080 · Cited by 1,200 · see citing works
Proterozoic Ocean Chemistry and Evolution: A Bioinorganic Bridge?
Anbar, A. D., & Knoll, A. H. (2002) · Science · doi:10.1126/science.1069651 · Cited by 1,191 · see citing works
Principles of bioinorganic chemistry
Chayen, J. (1995) · Cell Biochemistry and Function · doi:10.1002/cbf.290130214 · Cited by 1,062 · see citing works
One thousand families for the molecular biologist
Chothia, C. (1992) · Nature · doi:10.1038/357543a0 · Cited by 1,012 · see citing works
Canfield, D. E., & Teske, A. (1996) · Nature · doi:10.1038/382127a0 · Cited by 869 · see citing works
Eukaryotic organisms in Proterozoic oceans
Knoll, A. H., Javaux, E. J., Hewitt, D., & Cohen, P. (2006) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2006.1843 · Cited by 701 · see citing works
Molybdenum isotope evidence for widespread anoxia in mid-Proterozoic oceans
Arnold, G. L., Anbar, A. D., Barling, J., & Lyons, T. W. (2004) · Science · doi:10.1126/science.1091785 · Cited by 689 · see citing works
The timing of eukaryotic evolution: Does a relaxed molecular clock reconcile proteins and fossils?
Douzery, E. J. P., Snell, E. A., Bapteste, E., Delsuc, F., & Philippe, H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403984101 · Cited by 638 · see citing works
Kopp, R. E., Kirschvink, J. L., Hilburn, I. A., & Nash, C. Z. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504878102 · Cited by 565 · see citing works
The structure of the protein universe and genome evolution
Koonin, E. V., Wolf, Y. I., & Karev, G. P. (2002) · Nature · doi:10.1038/nature01256 · Cited by 553 · see citing works
Trends between gene content and genome size in prokaryotic species with larger genomes
Konstantinidis, K. T., & Tiedje, J. M. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308653100 · Cited by 516 · see citing works
Molecular Evidence for the Early Evolution of Photosynthesis
Xiong, J., Fischer, W. M., Inoue, K., Nakahara, M., & Bauer, C. E. (2000) · Science · doi:10.1126/science.289.5485.1724 · Cited by 513 · see citing works
Domain combinations in archaeal, eubacterial and eukaryotic proteomes
Apic, G., Gough, J., & Teichmann, S. A. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2001.4776 · Cited by 496 · see citing works
The Effect of Oxygen on Biochemical Networks and the Evolution of Complex Life
Raymond, J., & Segrè, D. (2006) · Science · doi:10.1126/science.1118439 · Cited by 494 · see citing works
Saito, M. A., Sigman, D. M., & Morel, F. M. M. (2003) · Inorganica Chimica Acta · doi:10.1016/s0020-1693(03)00442-0 · Cited by 440 · see citing works
Morphological and ecological complexity in early eukaryotic ecosystems
Javaux, E. J., Knoll, A. H., & Walter, M. R. (2001) · Nature · doi:10.1038/35083562 · Cited by 418 · see citing works
The Impact of Structural Genomics: Expectations and Outcomes
Chandonia, J., & Brenner, S. E. (2006) · Science · doi:10.1126/science.1121018 · Cited by 377 · see citing works
Scaling laws in the functional content of genomes
van Nimwegen, E. (2003) · Trends in Genetics · doi:10.1016/s0168-9525(03)00203-8 · Cited by 316 · see citing works
Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment
Palenik, B. P., Ren, Q., Dupont, C. L., Myers, G. S. A., Heidelberg, J. F., Badger, J. H., Madupu, R., Nelson, W. C., Brinkac, L. M., Dodson, R. J., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602963103 · Cited by 266 · see citing works
Self-citationPhylogeny determined by protein domain content
Yang, S. Y., Doolittle, R. F., & Bourne, P. E. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408810102 · Cited by 237 · see citing works
Self-citationBiogeochemical signatures through time as inferred from whole microbial genomes
Zerkle, A. L. (2005) · American Journal of Science · doi:10.2475/ajs.305.6-8.467 · Cited by 223 · see citing works
Theißen, U. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg174 · Cited by 194 · see citing works
Evolution was Chemically Constrained
Williams, R. J. P., & da Silva, J. J. R. F. (2002) · Journal of Theoretical Biology · doi:10.1006/jtbi.2003.3152 · Cited by 143 · see citing works
Power Laws, Scale-Free Networks and Genome Biology
Koonin, E. V., Wolf, Y. I., & Karev, G. P. (2006) · Springer eBooks · doi:10.1007/0-387-33916-7 · Cited by 118 · see citing works
A limited universe of membrane protein families and folds
Oberai, A., Ihm, Y., Kim, S., et al. (2006) · Protein Science · doi:10.1110/ps.062109706 · Cited by 94 · see citing works
Shi, W., Zhan, C., Ignatov, A., et al. (2005) · Structure · doi:10.1016/j.str.2005.07.014 · Cited by 81 · see citing works
Evolutionary perspective on annexin calcium-binding domains
Morgan, R. O., Martin‐Almedina, S., Iglesias, J. M., Gonzalez-Florez, M. I., & Fernández, M. P. (2004) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2004.09.010 · Cited by 79 · see citing works
The chemistry of evolution: the development of our ecosystem
(2007) · Choice Reviews Online · doi:10.5860/choice.44-3881 · Cited by 77 · see citing works
Genomic scale sub-family assignment of protein domains
Gough, J. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl484 · Cited by 21 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Damo, S. M., Kehl-Fie, T. E., Sugitani, N., Holt, M. E., Rathi, S., Murphy, W. J., Zhang, Y., Betz, C., Hench, L., Fritz, G., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220341110 · Cited by 388 · see citing works
Tracking Euxinia in the Ancient Ocean: A Multiproxy Perspective and Proterozoic Case Study
Lyons, T. W., Anbar, A. D., Severmann, S., Scott, C., & Gill, B. C. (2009) · Annual Review of Earth and Planetary Sciences · doi:10.1146/annurev.earth.36.031207.124233 · Cited by 373 · see citing works
History of biological metal utilization inferred through phylogenomic analysis of protein structures
Dupont, C. L., Butcher, A., Valas, R. E., Bourne, P. E., & Caetano-Anollés, G. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0912491107 · Cited by 331 · see citing works
Self-citationTrace elements at the intersection of marine biological and geochemical evolution
Robbins, L. J., Lalonde, S. V., Planavsky, N. J., Partin, C. A., Reinhard, C. T., Kendall, B., Scott, C., Hardisty, D. S., Gill, B. C., Alessi, D. S., et al. (2016) · Earth-Science Reviews · doi:10.1016/j.earscirev.2016.10.013 · Cited by 227 · see citing works
Self-citationOxygenation, Life, and the Planetary System during Earth's Middle History: An Overview
Lyons, T. W., Diamond, C. W., Planavsky, N. J., Reinhard, C. T., & Li, C. (2021) · Astrobiology · doi:10.1089/ast.2020.2418 · Cited by 211 · see citing works
“, 2007) and geochemical archives of environmental change (Dupont et al., 2006; Magnabosco et al., 2018) have and will continue to yield essential fruit.”
BackgroundUndocumented water column sink for cadmium in open ocean oxygen-deficient zones
Janssen, D. J., Conway, T. M., John, S. G., Christian, J. R., Kramer, D. I., Pedersen, T. F., & Cullen, J. T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402388111 · Cited by 154 · see citing works
Evolutionary inheritance of elemental stoichiometry in phytoplankton
Quigg, A., Irwin, A. J., & Finkel, Z. V. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.1356 · Cited by 144 · see citing works
Cycles of nutrient trace elements in the Phanerozoic ocean
Large, R. R., Halpin, J. A., Lounejeva, E., Danyushevsky, L. V., Maslennikov, V. V., Gregory, D., Sack, P. J., Haines, P. W., Long, J. A., Makoundi, C., et al. (2015) · Gondwana Research · doi:10.1016/j.gr.2015.06.004 · Cited by 145 · see citing works
Cobalt and marine redox evolution
Swanner, E. D., Planavsky, N. J., Lalonde, S. V., Robbins, L. J., Bekker, A., Rouxel, O. J., Saito, M. A., Kappler, A., Mojzsis, S. J., & Konhauser, K. O. (2014) · Earth and Planetary Science Letters · doi:10.1016/j.epsl.2014.01.001 · Cited by 127 · see citing works
Bioavailability of zinc in marine systems through time
Scott, C., Planavsky, N. J., Dupont, C. L., Kendall, B., Gill, B. C., Robbins, L. J., Husband, K. F., Arnold, G. L., Wing, B. A., Poulton, S. W., et al. (2013) · Nature Geoscience · doi:10.1038/ngeo1679 · Cited by 120 · see citing works
Self-citationRobbins, L. J., Lalonde, S. V., Saito, M. A., Planavsky, N. J., Mloszewska, A. M., Pecoits, E., Scott, C., Dupont, C. L., Kappler, A., & Konhauser, K. O. (2013) · Geobiology · doi:10.1111/gbi.12036 · Cited by 79 · see citing works
Self-citation
- Authors
- Dupont, C. L., Yang, S., Palenik, B., & Bourne, P. E.
- Affiliations
- Scripps Institution of Oceanography (US)
- Departments of ‡Chemistry and Biochemistry and
- Marine Biology Research Division,
- San Diego Supercomputer Center (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-11-21
- Volume
- 103
- Issue
- 47
- Pages
- 17822-17827
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC1635651
- OpenAlex
- W2134705864
- Cited by
- 236
- References
- 37
- Citations by year
- 2026: 6 · 2025: 9 · 2024: 8 · 2023: 12 · 2022: 19 · 2021: 12 · 2020: 8 · 2019: 10 · 2018: 13 · 2017: 18 · 2016: 13 · 2015: 5 · 2014: 15 · 2013: 9 · 2012: 11
- FWCI
- 6.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of General Medical Sciences (GM63208, P01GM063208)
- Topics
- Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Paleontology and Stratigraphy of Fossils
- Health Sciences › Nursing › Nutrition and Dietetics › Trace Elements in Health
- Keywords
- trace metal bioavailability, metallome, metal-binding proteins, iron-binding proteins, zinc-binding proteins, Great Oxidation Event, ocean redox state, anoxic oceans, protein-DNA interactions, protein-protein interaction, power law, proteome evolution
- MeSH terms
- Animals, Bacterial Proteins, Eukaryotic Cells, Metals, Oxidation-Reduction, Seawater, Trace Elements, Geologic Sediments, Evolution, Molecular, Computational Biology, Archaeal Proteins, Proteome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
