Thermodynamic System Drift in Protein Evolution

PLoS Biology

Volumn 12, Issue 11, 2014, Pages

  Hart, Kathryn M ^a,b   Harms, Michael J ^c   Schmidt, Bryan H ^a,b,e   Elya, Carolyn ^a,b   Thornton, Joseph W ^d   Marqusee, Susan ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF OREGON   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE H; BACTERIAL PROTEIN; RIBONUCLEASE HI;

AMINO ACID SEQUENCE; ARTICLE; BIODIVERSITY; CONTROLLED STUDY; ENZYME STABILITY; ENZYME STRUCTURE; ESCHERICHIA COLI; MELTING POINT; MOLECULAR EVOLUTION; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN UNFOLDING; SEQUENCE ANALYSIS; THERMODYNAMIC SYSTEM DRIFT; THERMODYNAMICS; THERMUS THERMOPHILUS; GENETICS; PROTEIN STABILITY; TRANSITION TEMPERATURE;

BACTERIAL PROTEINS; ESCHERICHIA COLI; EVOLUTION, MOLECULAR; PROTEIN STABILITY; RIBONUCLEASE H; THERMUS THERMOPHILUS; TRANSITION TEMPERATURE;

EID: 84912544160     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001994     Document Type: Article

References (61)

1. Counago R, Chen S, Shamoo Y, (2006) In vivo molecular evolution reveals biophysical origins of organismal fitness. Mol Cell 22: 441–449.
2. Gromiha MM, Oobatake M, Sarai A, (1999) Important amino acid properties for enhanced thermostability from mesophilic to thermophilic proteins. Biophys Chem 82: 51–67.
3. Taverna DM, Goldstein RA, (2002) Why are proteins marginally stable? Proteins 46: 105–109.
4. Kumar S, Nussinov R, (2001) How do thermophilic proteins deal with heat? Cell Mol Life Sci 58: 1216–1233.
5. Razvi A, Scholtz JM, (2006) Lessons in stability from thermophilic proteins. Protein Sci 15: 1569–1578.
6. Kumar S, Tsai CJ, Nussinov R, (2001) Thermodynamic differences among homologous thermophilic and mesophilic proteins. Biochemistry 40: 14152–14165.
7. Gould SJ, Lewontin RC, (1979) The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc R Soc Lond B Biol Sci 205: 581–598.
8. Akanuma S, Nakajima Y, Yokobori S, Kimura M, Nemoto N, et al. (2013) Experimental evidence for the thermophilicity of ancestral life. Proc Natl Acad Sci U S A 110: 11067–11072.
9. Gaucher EA, Govindarajan S, Ganesh OK, (2008) Palaeotemperature trend for Precambrian life inferred from resurrected proteins. Nature 451: 704–707.
10. Gaucher EA, Thomson JM, Burgan MF, Benner SA, (2003) Inferring the palaeoenvironment of ancient bacteria on the basis of resurrected proteins. Nature 425: 285–288.
11. Hobbs JK, Shepherd C, Saul DJ, Demetras NJ, Haaning S, et al. (2012) On the origin and evolution of thermophily: reconstruction of functional precambrian enzymes from ancestors of Bacillus. Mol Biol Evol 29: 825–835.
12. Perez-Jimenez R, Ingles-Prieto A, Zhao ZM, Sanchez-Romero I, Alegre-Cebollada J, et al. (2011) Single-molecule paleoenzymology probes the chemistry of resurrected enzymes. Nat Struct Mol Biol 18: 592–596.
13. Risso VA, Gavira JA, Mejia-Carmona DF, Gaucher EA, Sanchez-Ruiz JM, (2013) Hyperstability and substrate promiscuity in laboratory resurrections of precambrian beta-lactamases. J Am Chem Soc 135: 2899–2902.
14. Harms MJ, Thornton JW, (2010) Analyzing protein structure and function using ancestral gene reconstruction. Curr Opin Struct Biol 20: 360–366.
15. Tadokoro T, Kanaya S, (2009) Ribonuclease H: molecular diversities, substrate binding domains, and catalytic mechanism of the prokaryotic enzymes. FEBS J 276: 1482–1493.
16. Hollien J, Marqusee S, (1999) Structural distribution of stability in a thermophilic enzyme. Proc Natl Acad Sci U S A 96: 13674–13678.
17. Hollien J, Marqusee S, (1999) A thermodynamic comparison of mesophilic and thermophilic ribonucleases H. Biochemistry 38: 3831–3836.
18. Hollien J, Marqusee S, (2002) Comparison of the folding processes of T. thermophilus and E. coli ribonucleases H. J Mol Biol 316: 327–340.
19. Robic S, Berger JM, Marqusee S, (2002) Contributions of folding cores to the thermostabilities of two ribonucleases H. Protein Sci 11: 381–389.
20. Tadokoro T, You DJ, Abe Y, Chon H, Matsumura H, et al. (2007) Structural, thermodynamic, and mutational analyses of a psychrotrophic RNase HI. Biochemistry 46: 7460–7468.
21. Ratcliff K, Corn J, Marqusee S, (2009) Structure, stability, and folding of ribonuclease H1 from the moderately thermophilic Chlorobium tepidum: comparison with thermophilic and mesophilic homologues. Biochemistry 48: 5890–5898.
22. Parte A (2012) Bergey's manual of systematic bacteriology. New York: Springer.
23. Iversen C, Mullane N, McCardell B, Tall BD, Lehner A, et al. (2008) Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., Cronobacter malonaticus sp. nov., Cronobacter turicensis sp. nov., Cronobacter muytjensii sp. nov., Cronobacter dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies, Cronobacter dublinensis subsp. dublinensis subsp. nov., Cronobacter dublinensis subsp. lausannensis subsp. nov. and Cronobacter dublinensis subsp. lactaridi subsp. nov. Int J Syst Evol Microbiol 58: 1442–1447.
24. Darby AC, Chandler SM, Welburn SC, Douglas AE, (2005) Aphid-symbiotic bacteria cultured in insect cell lines. Appl Environ Microbiol 71: 4833–4839.
25. Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, et al. (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6: e1000943.
26. Hedges SB, Dudley J, Kumar S, (2006) TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22: 2971–2972.
27. Yang W, Hendrickson WA, Crouch RJ, Satow Y, (1990) Structure of ribonuclease H phased at 2 A resolution by MAD analysis of the selenomethionyl protein. Science 249: 1398–1405.
28. Ishikawa K, Okumura M, Katayanagi K, Kimura S, Kanaya S, et al. (1993) Crystal structure of ribonuclease H from Thermus thermophilus HB8 refined at 2.8 A resolution. J Mol Biol 230: 529–542.
29. Haruki M, Noguchi E, Akasako A, Oobatake M, Itaya M, et al. (1994) A novel strategy for stabilization of Escherichia coli ribonuclease HI involving a screen for an intragenic suppressor of carboxyl-terminal deletions. J Biol Chem 269: 26904–26911.
30. Keck JL, Goedken ER, Marqusee S, (1998) Activation/attenuation model for RNase H. A one-metal mechanism with second-metal inhibition. J Biol Chem 273: 34128–34133.
31. Crooke ST, Lemonidis KM, Neilson L, Griffey R, Lesnik EA, et al. (1995) Kinetic characteristics of Escherichia coli RNase H1: cleavage of various antisense oligonucleotide-RNA duplexes. Biochem J 312 (Pt 2): 599–608.
32. Guzman-Casado M, Parody-Morreale A, Robic S, Marqusee S, Sanchez-Ruiz JM, (2003) Energetic evidence for formation of a pH-dependent hydrophobic cluster in the denatured state of Thermus thermophilus ribonuclease H. J Mol Biol 329: 731–743.
33. Robic S, Guzman-Casado M, Sanchez-Ruiz JM, Marqusee S, (2003) Role of residual structure in the unfolded state of a thermophilic protein. Proc Natl Acad Sci U S A 100: 11345–11349.
34. Baldwin RL, (1986) Temperature dependence of the hydrophobic interaction in protein folding. Proc Natl Acad Sci U S A 83: 8069–8072.
35. Haruki M, Tanaka M, Motegi T, Tadokoro T, Koga Y, et al. (2007) Structural and thermodynamic analyses of Escherichia coli RNase HI variant with quintuple thermostabilizing mutations. FEBS J 274: 5815–5825.
36. True JR, Haag ES, (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3: 109–119.
37. Gong LI, Suchard MA, Bloom JD, (2013) Stability-mediated epistasis constrains the evolution of an influenza protein. Elife 2: e00631.
38. Taverna DM, Goldstein RA, (2002) Why are proteins so robust to site mutations? J Mol Biol 315: 479–484.
39. Wagner A, (2008) Neutralism and selectionism: a network-based reconciliation. Nat Rev Genet 9: 965–974.
40. Bloom JD, Gong LI, Baltimore D, (2010) Permissive secondary mutations enable the evolution of influenza oseltamivir resistance. Science 328: 1272–1275.
41. Lunzer M, Golding GB, Dean AM, (2010) Pervasive cryptic epistasis in molecular evolution. PLoS Genet 6: e1001162.
42. Harms MJ, Thornton JW, (2013) Evolutionary biochemistry: revealing the historical and physical causes of protein properties. Nat Rev Genet 14: 559–571.
43. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
44. Pruitt KD, Tatusova T, Maglott DR, (2005) NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 33: D501–504.
45. Huang Y, Niu B, Gao Y, Fu L, Li W, (2010) CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26: 680–682.
46. Abascal F, Zardoya R, Posada D, (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.
47. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–321.
48. Jones DT, Taylor WR, Thornton JM, (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275–282.
49. Anisimova M, Gascuel O, (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55: 539–552.
50. Yang Z, Kumar S, Nei M, (1995) A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141: 1641–1650.
51. Yang Z, (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591.
52. Edelhoch H, (1967) Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6: 1948–1954.
53. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307–326.
54. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658–674.
55. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486–501.
56. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213–221.
57. Chen VB, Arendall WB, 3rdHeadd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12–21.
58. Schrodinger LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1.
59. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
60. Fletcher R, Reeves CM, (1964) Function minimization by conjugate gradients. The Computer Journal 7: 149–154.
61. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188–1190.