Selective Pressure Causes an RNA Virus to Trade Reproductive Fitness for Increased Structural and Thermal Stability of a Viral Enzyme

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Dessau, Moshe ^a   Goldhill, Daniel ^a   McBride, Robert L ^a,b   Turner, Paul E ^a   Modis, Yorgo ^a  

^a YALE UNIVERSITY   (United States)

^b Sapphire Energy   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCAN; PROTEIN P5; UNCLASSIFIED DRUG; VIRUS ENZYME;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIOPHAGE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOLYSIS; ENVIRONMENTAL TEMPERATURE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME STABILITY; HEAT SHOCK; HYDROPHOBICITY; NONHUMAN; PLEIOTROPY; PROTEIN FOLDING; PROTEIN FUNCTION; REPRODUCTIVE FITNESS; STRUCTURE ACTIVITY RELATION; THERMOSTABILITY; VIRUS MORPHOLOGY; VIRUS MUTATION; VIRUS REPLICATION; VIRUS SURVIVAL; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIOPHAGES; BIOLOGICAL EVOLUTION; CAPSID; CRYSTALLOGRAPHY, X-RAY; ENZYME STABILITY; GENETIC FITNESS; RNA VIRUSES; SELECTION, GENETIC; VIRAL PROTEINS;

MIRIDAE; PSEUDOMONAS PHAGE PHI-6; RNA VIRUSES;

EID: 84870678336     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003102     Document Type: Article

References (48)

1. Crill WD, Wichman HA, Bull JJ, (2000) Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154: 27-37.
2. Duffy S, Burch CL, Turner PE, (2007) Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution 61: 2614-22.
3. Dean AM, Thornton JW, (2007) Mechanistic approaches to the study of evolution: the functional synthesis. Nat Rev Genet 8: 675-88.
4. Golding GB, Dean AM, (1998) The structural basis of molecular adaptation. Mol Biol Evol 15: 355-69.
5. Newcomb RD, Campbell PM, Ollis DL, Cheah E, Russell RJ, et al. (1997) A single amino acid substitution converts a carboxylesterase to an organophosphorus hydrolase and confers insecticide resistance on a blowfly. Proc Natl Acad Sci U S A 94: 7464-8.
6. Weinreich DM, Delaney NF, Depristo MA, Hartl DL, (2006) Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312: 111-4.
7. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP, (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science 313: 101-4.
8. Darwin C (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray.
9. Hamilton WD, (1964) The genetical evolution of social behaviour. I. J Theor Biol 7: 1-16.
10. Stearns SC (1992) The Evolution of Life Histories. Oxford, UK.: Oxford University Press.
11. Mindich L, (1988) Bacteriophage phi 6: a unique virus having a lipid-containing membrane and a genome composed of three dsRNA segments. Adv Virus Res 35: 137-76.
12. Young R, (1992) Bacteriophage lysis: mechanism and regulation. Microbiol Rev 56: 430-81.
13. Fokine A, Miroshnikov KA, Shneider MM, Mesyanzhinov VV, Rossmann MG, (2008) Structure of the bacteriophage phi KZ lytic transglycosylase gp144. J Biol Chem 283: 7242-50.
14. Wei H, Cheng RH, Berriman J, Rice WJ, Stokes DL, et al. (2009) Three-dimensional structure of the enveloped bacteriophage phi12: an incomplete T = 13 lattice is superposed on an enclosed T = 1 shell. PLoS ONE 4: e6850 doi: 10.1371/journal.pone.0006850.
15. McBride RC, Ogbunugafor CB, Turner PE, (2008) Robustness promotes evolvability of thermotolerance in an RNA virus. BMC Evol Biol 8: 231.
16. Caldentey J, Bamford DH, (1992) The lytic enzyme of the Pseudomonas phage phi 6. Purification and biochemical characterization. Biochim Biophys Acta 1159: 44-50.
17. Pei J, Grishin NV, (2005) The P5 protein from bacteriophage phi-6 is a distant homolog of lytic transglycosylases. Protein Sci 14: 1370-4.
18. Chothia C, (1974) Hydrophobic bonding and accessible surface area in proteins. Nature 248: 338-9.
19. Richards FM, (1977) Areas, volumes, packing and protein structure. Annu Rev Biophys Bioeng 6: 151-76.
20. Eriksson AE, Baase WA, Wozniak JA, Matthews BW, (1992) A cavity-containing mutant of T4 lysozyme is stabilized by buried benzene. Nature 355: 371-3.
21. Leung AK, Duewel HS, Honek JF, Berghuis AM, (2001) Crystal structure of the lytic transglycosylase from bacteriophage lambda in complex with hexa-N-acetylchitohexaose. Biochemistry-Us 40: 5665-73.
22. van Asselt EJ, Dijkstra AJ, Kalk KH, Takacs B, Keck W, et al. (1999) Crystal structure of Escherichia coli lytic transglycosylase Slt35 reveals a lysozyme-like catalytic domain with an EF-hand. Structure 7: 1167-80.
23. van Asselt EJ, Thunnissen AM, Dijkstra BW, (1999) High resolution crystal structures of the Escherichia coli lytic transglycosylase Slt70 and its complex with a peptidoglycan fragment. J Mol Biol 291: 877-98.
24. Blake CC, Fenn RH, North AC, Phillips DC, Poljak RJ, (1962) Structure of lysozyme. A Fourier map of the electron density at 6 angstrom resolution obtained by x-ray diffraction. Nature 196: 1173-6.
25. Grutter MG, Weaver LH, Matthews BW, (1983) Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes? Nature 303: 828-31.
26. Thunnissen AM, Rozeboom HJ, Kalk KH, Dijkstra BW, (1995) Structure of the 70-kDa soluble lytic transglycosylase complexed with bulgecin A. Implications for the enzymatic mechanism. Biochemistry-Us 34: 12729-37.
27. De Paepe M, Taddei F, (2006) Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biol 4: e193 doi:10.1371/journal.pbio.0040193.
28. Bull JJ, Badgett MR, Wichman HA, (2000) Big-benefit mutations in a bacteriophage inhibited with heat. Mol Biol Evol 17: 942-50.
29. Lee KH, Miller CR, Nagel AC, Wichman HA, Joyce P, et al. (2011) First-step mutations for adaptation at elevated temperature increase capsid stability in a virus. PLoS ONE 6: e25640 doi:10.1371/journal.pone.0025640.
30. Holtje JV, Mirelman D, Sharon N, Schwarz U, (1975) Novel type of murein transglycosylase in Escherichia coli. J Bacteriol 124: 1067-76.
31. Scheurwater E, Reid CW, Clarke AJ, (2008) Lytic transglycosylases: bacterial space-making autolysins. Int J Biochem Cell Biol 40: 586-91.
32. Matthews BW, Remington SJ, Grutter MG, Anderson WF, (1981) Relation between hen egg white lysozyme and bacteriophage T4 lysozyme: evolutionary implications. J Mol Biol 147: 545-58.
33. Anderson WF, Grutter MG, Remington SJ, Weaver LH, Matthews BW, (1981) Crystallographic determination of the mode of binding of oligosaccharides to T4 bacteriophage lysozyme: implications for the mechanism of catalysis. J Mol Biol 147: 523-43.
34. Blake CC, Koenig DF, Mair GA, North AC, Phillips DC, et al. (1965) Structure of hen egg-white lysozyme. A three-dimensional Fourier synthesis at 2 Angstrom resolution. Nature 206: 757-61.
35. Matthews BW, Remington SJ, (1974) The three dimensional structure of the lysozyme from bacteriophage T4. Proc Natl Acad Sci U S A 71: 4178-82.
36. Blackburn NT, Clarke AJ, (2000) Assay for lytic transglycosylases: a family of peptidoglycan lyases. Anal Biochem 284: 388-93.
37. Baase WA, Liu L, Tronrud DE, Matthews BW, (2010) Lessons from the lysozyme of phage T4. Protein Sci 19: 631-41.
38. Karpusas M, Baase WA, Matsumura M, Matthews BW, (1989) Hydrophobic packing in T4 lysozyme probed by cavity-filling mutants. Proc Natl Acad Sci U S A 86: 8237-41.
39. Haber PS, Young MM, Dorrington L, Jones A, Kaldor J, et al. (2007) Transmission of hepatitis C virus by needle-stick injury in community settings. J Gastroenterol Hepatol 22: 1882-5.
40. Stallknecht DE, Shane SM, Kearney MT, Zwank PJ, (1990) Persistence of avian influenza viruses in water. Avian Dis 34: 406-11.
41. Alto BW, Turner PE, (2010) Consequences of host adaptation for performance of vesicular stomatitis virus in novel thermal environments. Evol Ecol 24: 299-315.
42. Turner PE, Chao L, (1998) Sex and the evolution of intrahost competition in RNA virus phi6. Genetics 150: 523-32.
43. Chao L, (1990) Fitness of RNA virus decreased by Muller's ratchet. Nature 348: 454-5.
44. Pape T, Schneider TR, (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J Appl Crystallogr 37: 843-4.
45. Langer G, Cohen SX, Lamzin VS, Perrakis A, (2008) Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 3: 1171-9.
46. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-32.
47. Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, et al. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-54.
48. Kleywegt GJ, Jones TA, (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D Biol Crystallogr 50: 178-85.