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

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 23, 2010, Pages 10567-10572

  Dupont, Christopher L ^a   Butcher, Andrew ^b   Valas, Ruben E ^c   Bourne, Philip E ^d   Caetano Anollés, Gustavo ^e  

^a J CRAIG VENTER INSTITUTE   (United States)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Archean Proterozoic; Biogeochemistry; Bioinorganic chemistry; Evolution; Metal homeostasis

Indexed keywords

CELL PROTEIN; COPPER; METAL; ZINC;

ARTICLE; CATALYSIS; ELECTRON TRANSPORT; EUKARYOTIC CELL; GENETIC ANALYSIS; HISTORY OF MEDICINE; PHYLOGENY; PRIORITY JOURNAL; PROTEIN STRUCTURE;

EVOLUTION, MOLECULAR; GENOMICS; METALLOPROTEINS; PHYLOGENY; PROTEOME;

EUKARYOTA;

EID: 77953778296     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0912491107     Document Type: Article

References (52)

1. Rosenzweig AC (2002) Metallochaperones: Bind and deliver. Chem Biol 9:673-677.
2. Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2008) Metal ions in biological catalysis: From enzyme databases to general principles. J Biol Inorg Chem 13:1205-1218.
3. Williams RJP, Frausto da Silva JJR (2006) The Chemistry of Evolution: The Development of Our Ecosystem (Elsevier, Amsterdam).
4. Irving H, Williams RJP (1948) Order of stability of metal complexes. Nature 162:746-747.
5. Tottey S, et al. (2008) Protein-folding location can regulate manganese-binding versus copper- or zinc-binding. Nature 455:1138-1142.
6. Waldron KJ, Robinson NJ (2009) How do bacterial cells ensure that metalloproteins get the correct metal? Nat Rev Microbiol 7:25-35.
7. Williams RJP, Fraústo Da Silva JJ (2003) Evolution was chemically constrained. J Theor Biol 220:323-343.
8. Anbar AD (2008) Oceans. Elements and evolution. Science 322:1481-1483.
9. Saito MA, Sigman DM, Morel FMM (2003) The bioinorganic chemistry of the ancient ocean: The co-evolution of cyanobacterial metal requirements and biogeochemical cycles at the Archean-Proterozoic boundary? Inorganica Chemica Acta 356:308-318.
10. Bekker A, et al. (2004) Dating the rise of atmospheric oxygen. Nature 427:117-120.
11. Arnold GL, Anbar AD, Barling J, Lyons TW (2004) Molybdenum isotope evidence for widespread anoxia in mid-Proterozoic oceans. Science 304:87-90. (Pubitemid 38451461)
12. Anbar AD, Knoll AH (2002) Proterozoic ocean chemistry and evolution: A bioinorganic bridge? Science 297:1137-1142.
13. Reinhard CT, Raiswell R, Scott C, Anbar AD, Lyons TW (2009) A late Archean sulfidic sea stimulated by early oxidative weathering of the continents. Science 326:713-716.
14. Lyons TW, Reinhard CT (2009) Early Earth: Oxygen for heavy-metal fans. Nature 461:179-181.
15. Williams RJP (1997) The natural selection of the chemical elements. Cell Mol Life Sci 53:816-829.
16. Ji H-F, Chen L, Jiang Y-Y, Zhang H-Y (2009) Evolutionary formation of new protein folds is linked to metallic cofactor recruitment. Bioessays 31:975-980.
17. Dupont CL, Yang S, Palenik B, Bourne PE (2006) Modern proteomes contain putative imprints of ancient shifts in trace metal geochemistry. Proc Natl Acad Sci USA 103:17822-17827. (Pubitemid 44852244)
18. Caetano-Anollés G, Caetano-Anollés D (2003) An evolutionarily structured universe of protein architecture. Genome Res 13:1563-1571.
19. Wang M, Yafremava LS, Caetano-Anollés D, Mittenthal JE, Caetano-Anollés G (2007) Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res 17:1572-1585. (Pubitemid 350074853)
20. Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP: A structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536-540.
21. Berman HM, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28:235-242.
22. Andreini C, Banci L, Bertini I, Rosato A (2008) Occurrence of copper proteins through the three domains of life: A bioinformatic approach. J Proteome Res 7:209-216. (Pubitemid 351171133)
23. Morgan RO, Martin-Almedina S, Iglesias JM, Gonzalez-Florez MI, Fernandez MP (2004) Evolutionary perspective on annexin calcium-binding domains. Biochim Biophys Acta 1742:133-140. (Pubitemid 39601773)
24. Shi W, et al. (2005) Metalloproteomics: High-throughput structural and functional annotation of proteins in structural genomics. Structure 13:1473-1486. (Pubitemid 41427587)
25. Caetano-Anollés G, Wang M, Caetano-Anollés D, Mittenthal JE (2009) The origin, evolution and structure of the protein world. Biochem J 417:621-637.
26. Knoll AH, Javaux EJ, Hewitt D, Cohen P (2006) Euykaryotic organisms in Proterozoic oceans. Philos Trans R Soc Lond B Biol Sci 361:1023-1038.
27. Caetano-Anollés G, et al. (2009) The origin and evolution of modern metabolism. Int J Biochem Cell Biol 41:285-297.
28. Ji H-F, Chen L, Zhang H-Y (2008) Organic cofactors participated more frequently than transition metals in redox reactions of primitive proteins. Bioessays 30:766-771.
29. Kump LR (2004) Scientists Debate Gaia, eds Schneider SH, Miller JR, Crist E, Boston PJ (MIT press, Cambridge), pp 93-100.
30. Falkowski PG, Fenchel T, Delong EF (2008) The microbial engines that drive Earth's biogeochemical cycles. Science 320:1034-1039. (Pubitemid 351929518)
31. Volk T (2004) Scientists Debate Gaia, eds Schneider SH, Miller JR, Crist E, Boston PJ (MIT press, Cambridge), pp 27-36.
32. Embley TM, Martin W (2006) Eukaryotic evolution, changes and challenges. Nature 440:623-630.
33. Twining BS, Baines SB, Vogt S, de Jonge MD (2008) Exploring ocean biogeochemistry by single-cell microprobe analysis of protist elemental composition. J Eukaryot Microbiol 55:151-162. (Pubitemid 351629913)
34. Johnston DT, Wolfe-Simon F, Pearson A, Knoll AH (2009) Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth's middle age. Proc Natl Acad Sci USA 106:16925-16929.
35. Brocks JJ, Logan GA, Buick R, Summons RE (1999) Archean molecular fossils and the early rise of eukaryotes. Science 285:1033-1036. (Pubitemid 129515441)
36. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455:1101-1104.
37. John SG, Geis RW, Saito MA, Boyle EA (2007) Zinc isotopic fractionation during high-affinity and low-affinity zinc transport by the marine diatom Thalassiosira oceanica. Limnol Oceanogr 52:2710-2714.
38. Vardi A, et al. (2006) A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol 4:e60.
39. Scott C, et al. (2008) Tracing the stepwise oxygenation of the Proterozoic ocean. Nature 452:456-459. (Pubitemid 351450847)
40. Glass JB, Wolfe-Simon F, Anbar AD (2009) Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology 7:100-123.
41. Mulkidjanian A, Galperin M (2009) On the origin of life in the Zinc world. 2. Validation of the hypothesis on the photosynthesizing zinc sulfide edifices as cradles of life on Earth. Biol Direct 4:27.
42. Sunda WG, Huntsman SA (1995) Co and Zn interreplacement in marine phytoplankton: Evolutionary and ecological implications. Limnol Oceanogr 40:1404-1417. (Pubitemid 3027065)
43. Saito MA, Moffett JW, Chisholm SW, Waterbury JB (2002) Cobalt limitation and uptake in Prochlorococcus. Limnol Oceanogr 47:1629-1636.
44. Heese D, Berger S, Röhm K-H (1990) Nuclear magnetic relaxation studies of the role of the metal ion in Mn2(+)-substituted aminoacylase I. Eur J Biochem 188:175-180. (Pubitemid 20076272)
45. Maric S, et al. (2009) The M17 leucine aminopeptidase of the malaria parasite Plasmodium falciparum: Importance of active site metal ions in the binding of substrates and inhibitors. Biochemistry 48:5435-5439.
46. Speckhard DC, Wu FY-H, Wu C-W (1977) Role of the intrinsic metal in RNA polymerase from Escherichia coli. In vivo substitution of tightly bound zinc with cobalt. Biochemistry 16:5228-5234.
47. Predki PF, Sarkar B (1994) Metal replacement in "zinc finger" and its effect on DNA binding. Environ Health Perspect 102(Suppl 3):195-198. (Pubitemid 24316382)
48. Aravind L, Iyer LM, Koonin EV (2006) Comparative genomics and structural biology of the molecular innovations of eukaryotes. Curr Opin Struct Biol 16:409-419. (Pubitemid 43831642)
49. Price NM, Morel FMM (1990) Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344:658-660. (Pubitemid 20426771)
50. Gough J (2006) Genomic scale sub-family assignment of protein domains. Nucleic Acids Res 34:3625-3633.
51. Gough J, Karplus K, Hughey R, Chothia C (2001) Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 313:903-919. (Pubitemid 33063435)
52. Yang S, Doolittle RF, Bourne PE (2005) Phylogeny determined by protein domain content. Proc Natl Acad Sci USA 102:373-378. (Pubitemid 40116774)