A universal molecular clock of protein folds and its power in tracing the early history of aerobic metabolism and planet oxygenation

Molecular Biology and Evolution

Volumn 28, Issue 1, 2011, Pages 567-582

  Wang, Minglei ^a   Jiang, Ying Ying ^b,c   Kim, Kyung Mo ^a   Qu, Ge ^c   Ji, Hong Fang ^c   Mittenthal, Jay E ^d   Zhang, Hong Yu ^b   Caetano Anollés, Gustavo ^a  

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

^b HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^c SHANDONG UNIVERSITY OF TECHNOLOGY   (China)

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

Author keywords

aerobic metabolism; enzyme; evolution; function; structure

Indexed keywords

AEROBIC METABOLISM; ARTICLE; ENZYME ACTIVITY; MOLECULAR CLOCK; MOLECULAR EVOLUTION; NONHUMAN; OXYGENATION; PLANET OXYGENATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEOMICS;

AEROBIOSIS; EVOLUTION, MOLECULAR; LIFE; OXYGEN; PHYLOGENY; PLANETS; PROTEIN FOLDING; PROTEINS; PROTEOME; TIME FACTORS;

EID: 78650476811     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq232     Document Type: Article

References (100)

1. Anbar AD, Duan Y, Lyons TW, et al. 2007. A whiff of oxygen before the great oxidation event? Science 317(5846):1903-1906.
2. Andreeva A, Howorth D, Chandonia J-M, Brenner SE, Hubbard TJP, Chothia C, Murzin AG. 2008. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res. 36(Data-base issue):D419-D425.
3. Bengtson S, Belivanova V, Rasmussen B, Whitehouse M. 2009. The controversial "Cambrian" fossils of the Vindhyan are real but more than a billion years older. Proc Natl Acad Sci USA. 106(19): 7729-7734.
4. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The Protein Data Bank. Nucleic Acids Res. 28(1):235-242.
5. Bhattacharya D, Yoon HS, Hedges SB, Hackett JD. 2009. Eukaryotes (Eukaryota). In: Hedges SB, Kumar S, editors. The timetree of life. New York: Oxford University Press. p. 116-120.
6. Blank CE. 2009. Not so old Archaea-the antiquity of biogeo-chemical processes in the archaeal domain of life. Geobiology 7(5):495-514.
7. Bloom JD, Silberg JJ, Wilke CO, Drummond DA, Adami C, Arnold FH. 2005. Thermodynamic prediction of protein neutrality. Proc Natl Acad Sci USA. 102(3):606-611.
8. Boca SM. 2006. A dynamical model for the evolution of protein folds [mathematics honors thesis]. [Urbana (IL)]: University of Illinois.
9. Brocks JJ, Logan GA, Buick R, Summons RE. 1999. Archean molecular fossils and the early rise of eukaryotes. Science 285(5430): 1033-1036.
10. Bromham L, Penny D. 2003. The modern molecular clock. Nat Rev Genet. 4(3):216-224.
11. Butterfield NJ. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleo-biology 26(3):386-404.
12. Caetano-Anollés G, Caetano-Anollés D. 2003. An evolutionarily structured universe of protein architecture. Genome Res. 13(7): 1563-1571.
13. Caetano-Anollés G, Mittenthal JE. 2010. Exploring the interplay of stability and function in protein evolution. BioEssays 32(8): 655-658.
14. Caetano-Anollés G, Kim HS, Mittenthal JE. 2007. The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc Natl Acad Sci USA. 104(22): 9358-9363.
15. Caetano-Anollés G, Wang M, Caetano-Anollés D, Mittenthal JE. 2009. The origin, evolution and structure of the protein world. Biochem J. 417(3):621-637.
16. Caetano-Anollés G, Yafremava LS, Mittenthal JE. 2010. Modularity and dissipation in evolution of macromolecular structures, functions, and networks. In: Caetano-Anollés G, editor. Evolutionary genomics and systems biology. Hoboken (NJ): Wiley-Blackwell. p. 431-450.
17. Catling DC, Glein CR, Zahnle KJ, McKay CP. 2005. Why O2 is required by complex life on habitable planets and the concept of planetary "oxygenation time". Astrobiology 5(3): 415-438.
18. Chang A, Scheer M, Grote A, Schomburg I, Schomburg D. 2009. BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res. 37(Database issue):D588-D592.
19. Chapman DJ, Schopf JW. 1983. Biological and biochemical effects of the development of an aerobic environment. In: Schopf JW, editor. Earth's earliest biosphere: its origin and evolution. Princeton (NJ): Princeton University Press. p. 302-320 and references therein.
20. Chen LL, Wang GZ, Zhang HY. 2007. Sterol biosynthesis and prokaryotes-to-eukaryotes evolution. Biochem Biophys Res Commun. 363(4):885-888.
21. Chothia C, Gough J. 2009. Genomic and structural aspects of protein evolution. Biochem J. 419(1):15-28.
22. Claire MW, Catling DC, Zahnle KJ. 2006. Biogeochemical modelling of the rise in atmospheric oxygen. Geobiology 4(4):239-269.
23. 8 barrels: implications for the evolution of metabolic pathways. J Mol Biol. 303:627-640.
24. de Pinna MCC. 1991. Concepts and tests of homology in the cladistic paradigm. Cladistics 7:367-394.
25. Doolittle RF. 2005. Evolutionary aspects of whole-genome biology. Curr Opin Struct Biol. 15(3):248-253.
26. Doolittle RF, Feng DF, Tsang S, Cho G, Little E. 1996. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science 271(5248):470-477.
27. 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(47):17822-17827.
28. Dupont CL, Butcher A, Valas RE, Bourne PE, Caetano-Anollés G. 2010. History of biological metal utilization inferred through phylogenomic analysis of protein structure. Proc Natl Acad Sci USA. 107:10567-10572.
29. Dym O, Pratt EA, Ho C, Eisenberg D. 2000. The crystal structure of D-lactate dehydrogenase, a peripheral membrane respiratory enzyme. Proc Natl Acad Sci USA. 97(17):9413-9418.
30. 2. Science 322(5901):540-542.
31. Feng DF, Cho G, Doolittle RF. 1997. Determining divergence times with a protein clock: update and reevaluation. Proc Natl Acad Sci USA. 94(24):13028-13033.
32. Fischer WW. 2008. Life before the rise of oxygen. Nature 455: 1051-1052.
33. Forslund K, Henricson A, Hollich V, Sonnhammer E. 2008. Domain tree-based analysis of protein architecture evolution. Mol Biol Evol. 25:254-264.
34. Garvin J, Buick R, Anbar AD, Arnold GL, Kaufman AJ. 2009. Isotopic evidence for an aerobic nitrogen cycle in the latest Archean. Science 323(5917):1045-1048.
35. Glass JB, Wolfe-Simon F, Anbar AD. 2009. Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology 7(2):100-123.
36. Godfrey LV, Falkowski PG. 2009. The cycling and redox state of nitrogen in the Archaean ocean. Nat Geosci. 2(10): 725-729.
37. Gough J. 2005. Convergent evolution of domain structures (is rare). Bioinformatics 21:1464-1471.
38. 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(4):903-919.
39. Gourier D, Delpoux O, Bonduelle A, Binet L, Ciofini I, Vezin H. 2010. EPR, ENDOR, and HYSCORE study of the structure and the stability of vanadyl-porphyrin complexes encapsulated in silica: potential paramagnetic biomarkers for the origin of life. J Phys Chem B. 114(10):3714-3725.
40. Hall BG, Barlow M. 2004. Evolution of the serine b-lactamases: past, present and future. Drug Resist Updat. 7(2):111-123.
41. Harris TA. 1963. The theory of branching processes. New York: Dover Publications.
42. Hedges SB, Dudley J, Kumar S. 2006. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22(23):2971-2972.
43. Hermann TN, Podkovyrov VN. 2008. On the nature of the Precambrian microfossils Arctacellularia and Glomovertella. Paleontol J. 42(6):655-664.
44. Hoashi M, David C, Bevacqua DC, Otake T, Watanabe Y, Hickman AH, Utsunomiya S, Ohmoto H. 2009. Primary haematite formation in an oxygenated sea 3.46 billion years ago. Nat Geosci. 2(4):301-306.
45. Hofmann HJ. 1976. Precambrian microflora, Belcher Islands, Canada: significance and systematics. J Paleontol. 50(6):1040-1073.
46. Holland HD. 2006. The oxygenation of the atmosphere and oceans. Philos Trans R Soc Lond B Biol Sci. 361(1470):903-915.
47. Holland LZ, Albalat R, Azumi K, et al. 2008. The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18(7):1100-1111.
48. Javaux EJ, Knoll AH, Walter MR. 2004. TEM evidence for eukaryotic diversity in mid-Proterozoic oceans. Geobiology 2(3):121-132.
49. Jez JM, Bowman ME, Dixon RA, Noel JP. 2000. Structure and mechanism of the evolutionarily unique plant enzyme chalcone isomerase. Nat Struct Biol. 7:786-791.
50. Ji HF, Chen L, Jiang YY, Zhang HY. 2009. Evolutionary formation of new protein folds is linked to metallic cofactor recruitment. BioEssays 31(9):975-980.
51. Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28(1):27-30.
52. Kato Y, Suzuki K, Nakamura K, Hickman Ah, Nedachi M, Kusakabe M, Bevacqua DC, Ohmoto H. 2009. Hematite formation by oxygenated groundwater more than 2.76 billion years ago. Earth Planet Sci Lett. 278(1-2):40-49.
53. Kaufman AJ, Johnston DT, Farquhar J, et al. 2007. Late Archean biospheric oxygenation and atmospheric evolution. Science 317(5846):1900-1903.
54. Kim HS, Mittenthal JE, Caetano-Anollés G. 2006. MANET: tracing evolution of protein architecture in metabolic networks. BMC Bioinformatics 7:351.
55. Kim KM, Caetano-Anollés G. 2010. Emergence and evolution of modern molecular functions inferred from phylogenomic analysis of ontological data. Mol Biol Evol. 27(7):1710-1733.
56. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge: Cambridge University Press.
57. Kirkpatrick M, Slatkin M. 1993. Searching for evolutionary patterns in the shape of phylogenetic trees. Evolution 47:1171-1181.
58. Kumar S. 2005. Molecular clocks: four decades of evolution. Nat Rev Genet. 6(8):654-662.
59. Lane DP, Cheok CF, Brown C, Madhumalar A, Ghadessy FJ, Verma C. 2010. Mdm2 and p53 are highly conserved from placozoans to man. Cell Cycle. 9(3):1-8.
60. Levitt M. 2007. Growth of novel protein structural data. Proc Natl Acad Sci USA. 104:3183-3188.
61. Ma BG, Chen L, Ji HF, et al. 2008. Characters of very ancient proteins. Biochem Biophys Res Commun. 366(3):607-611.
62. McKenzie A, Steel M . 2000. Distributions of cherries for two models of trees. Math Biosci. 164:81-92.
63. Margoliash E. 1963. Primary structure and evolution of cytochrome c. Proc Natl Acad Sci USA. 50(4):672-679.
64. Michael EB, David JC. 2009. 3D model of amphioxus steroid receptor complexed with estradiol. Biochem Biophys Res Commun. 386(3):516-520.
65. Mojzsis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP, Friend CR. 1996. Evidence for life on Earth before 3,800 million years ago. Nature 384(6604):55-59.
66. 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(4):536-540.
67. Nagano N, Orengo CA, Thornton JM. 2000. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol. 321:741-765.
68. Nisbet EG, Grassineau NV, Howe CJ, Abell PI, Regelous M, Nisbet RER. 2007. The age of Rubisco: the evolution of oxygenic photosynthesis. Geobiology 5(4):311-335.
69. Nixon KC. 1999. The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15(4):407-414.
70. Payne JL, Boyer AG, Brown JH, et al. 2009. Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity. Proc Natl Acad Sci USA. 106(1):24-27.
71. Porter CT, Bartlett GJ, Thornton JM. 2004. The Catalytic Site Atlas: a resource of catalytic sites and residues identified in enzymes using structural data. Nucleic Acids Res. 32(Database issue): D129-D133.
72. Porter SM. 2004. The fossil record of early eukaryotic diversification. Paleontol Soc Paper. 10:35-50.
73. Rasmussen B, Fletcher IR, Brocks JJ, Kilburn MR. 2008. Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455(7216):1101-1104.
74. Raymond J, Segrè D. 2006. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311(5768): 1764-1767.
75. Römpler H, Stäubert C, Thor D, Schulz A, Hofreiter M, Schöneberg T. 2007. G protein-coupled time travel: evolutionary aspects of GPCR research. Mol Interv. 7(1):17-25.
76. Saito MA. 2009. Less nickel for more oxygen. Nature 458(7239):714-715.
77. 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? Inorg Chim Acta. 356: 308-318.
78. Schuster P. 2010. Genotypes and phenotypes in the evolution of molecules. In: Caetano-Anollés G, editor. Evolutionary genomics and systems biology. Hoboken (NJ): Wiley-Blackwell. p. 123-152.
79. Serrano LAG, Day G, Fersht AR. 1993. Step-wise mutation of barnase to binase: a procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability. J Mol Biol. 233(2):305-312.
80. Sessions AL, Doughty DM, Welander PV, Summons RE, Newman DK. 2009. The continuing puzzle of the great oxidation event. Curr Biol. 19(14):R567-R574.
81. Summons RE, Bradley AS, Jahnke LL, Waldbauer JR. 2006. Steroids, triterpenoids and molecular oxygen. Phil Trans R Soc B. 361(1470):951-968.
82. Sun F-J, Caetano-Anollés G. 2008. The origin and evolution of tRNA inferred from phylogenetic analysis of structure. J Mol Biol. 66:1-35.
83. Sun F-J, Caetano-Anollés G. 2009. The evolutionary history of the structure of 5S ribosomal RNA. J Mol Evol. 69:430-443.
84. Sun F-J, Caetano-Anollés G. 2010. The ancient history of the structure of ribonuclease P and the early origins of Archaea. BMC Bioinformatics. 11:153.
85. Swofford DL. 2002. Phylogenetic analysis using parsimony and other programs (PAUP*), version 4. Sunderland (MA): Sinauer Associates.
86. Theobald DL. 2010. A formal test of the theory of common ancestry. Nature 465:219-222.
87. Thornton JW. 2001. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci USA. 98(10):5671-5676.
88. Tomitani A, Knoll AH, Cavanaugh CM, Ohno T. 2006. The evolutionary diversification of cyanobacteria: molecular- phylogenetic and paleontological perspectives. Proc Natl Acad Sci USA. 103(14):5442-5447.
89. van Berkel WJ, Kamerbeek NM, Fraaije MW. 2006. Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. J Biotechnol. 124(4):670-689.
90. van Holde KE, Miller KI, Decker H. 2001. Hemocyanins and invertebrate evolution. J Biol Chem. 276(19):15563-15566.
91. Ventura GT, Kenig F, Reddy CM, Schieber J, Frysinger GS, Nelson RK, Dinel E, Gaines RB, Schaeffer P. 2007. Molecular evidence of Late Archean archaea and the presence of a subsurface hydrothermal biosphere. Proc Natl Acad Sci USA. 104(36):14260-14265.
92. Wang M, Boca SM, Kalelkar R, Mittenthal JE, Caetano-Anollés G. 2006. A phylogenomic reconstruction of the protein world based on a genomic census of protein fold architecture. Complexity 12(1):27-40.
93. Wang M, Caetano-Anollés G. 2009. The evolutionary mechanics of domain organization in proteomes and the rise of modularity in the protein world. Structure 17(1):66-78.
94. Wang M, Yafremava LS, Caetano-Anolles D, Mittenthal JE, Caetano-Anolles G. 2007. Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res. 17(11):1572-1585.
95. Webster AJ, Payne RJH, Pagel M. 2003. Molecular phylogenies link rates of evolution and speciation. Science 301:478.
96. Williams RJ. 2003. Fraústo Da Silva JJ. Evolution was chemically constrained. J Theor Biol. 220(3):323-343.
97. Yang S, Bourne PE. 2009. The evolutionary history of protein domains viewed by species phylogeny. PLoS One. 4:e8378.
98. Yang S, Doolittle RF, Bourne PE. 2005. Phylogeny determined by protein domain content. Proc Natl Acad Sci USA. 102:373-378.
99. Yumiko Y-S, Ya-Pei H, Takeshi S. 2003. Distribution of flavonoids and related compounds from seaweeds in Japan. J Tokyo Univ Fish. 89:1-6.
100. Zuckerkandl E, Pauling LB. 1962. Molecular disease, evolution, and genetic heterogeneity. In: Kasha M, Pullman B, editors. Horizons in biochemistry. New York: Academic Press. p. 189-225.