Payoffs, Not Tradeoffs, in the Adaptation of a Virus to Ostensibly Conflicting Selective Pressures

PLoS Genetics

Volumn 10, Issue 10, 2014, Pages

  McGee, Lindsey W ^a   Aitchison, Erick W ^a   Caudle, S Brian ^a   Morrison, Anneliese J ^a   Zheng, Lianqing ^a   Yang, Wei ^a   Rokyta, Darin R ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; HEAT SHOCK PROTEIN; SINGLE STRANDED DNA; VIRAL PROTEIN;

ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; BINDING SITE; BIOPHYSICS; EVOLUTIONARY ADAPTATION; GENETIC TRAIT; GROWTH RATE; HIGH TEMPERATURE; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NONHUMAN; PH MEASUREMENT; PLEIOTROPY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; THERMOSTABILITY; VIRUS GENOME; ADAPTATION; CHEMISTRY; GENETIC SELECTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT SHOCK RESPONSE; METABOLISM; MICROVIRUS; MUTATION; PH; PHYSIOLOGY; REPRODUCTIVE FITNESS; TEMPERATURE; VIRUS CAPSID;

ADAPTATION, PHYSIOLOGICAL; CAPSID; GENETIC FITNESS; HEAT-SHOCK RESPONSE; HYDROGEN-ION CONCENTRATION; MICROVIRUS; MUTATION; SELECTION, GENETIC; TEMPERATURE; VIRAL PROTEINS;

EID: 84908324093     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004611     Document Type: Article

References (65)

1. Otto SP, (2004) Two steps forward, one step back: the pleiotropic effects of favoured alleles. Proceedings of the Royal Society of London B Biological Sciences 271: 705–714.
2. Ostman B, Hintze A, Adami C, (2012) Impact of epistasis and pleiotropy on evolutionary adaptation. Proceedings of the Royal Society of London B Biological Sciences 279: 247–256.
3. Mather K, Harrison B, (1949) The manifold effect of selection. Heredity 23: 131–162.
4. Cooper VS, Lenski RE, (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739.
5. Magwire M, Yamamoto A, Carbone M, Roshina N, Symonenko A, et al. (2010) Quantitative and molecular genetic analyses of mutations increasing drosophila life span. PLoS Genetics 6: e1001037.
6. Wenger J, Piotrowski J, Nagarajan S, Chiotti K, Sherlock G, et al. (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genetics 7: e1002202.
7. Bull JJ, Badgett MR, Wichman HA, (2000) Big-benefit mutations in a bacteriophage inhibited with heat. Molecular Biology and Evolution 17: 942–950.
8. 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.
9. Cooper VS, Lenski RE, (2001) Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment populations. Evolution 55: 889–896.
10. Williams GC, (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11: 398–411.
11. Hughes K, Alipaz J, Drnevich J, Reynolds R, (2002) A test of evolutionary theories of aging. Proceedings of the National Academy of Sciences of the USA 99: 14286–14291.
12. Promislow DEL, (2004) Protein networks, pleiotropy and the evolution of senescence. Proceedings of the Royal Society of London B Biological Sciences 271: 1225–1234.
13. Orr HA, (2000) Adaptation and the cost of complexity. Evolution 54: 13–20.
14. Kassen R, (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15: 173–190.
15. MacLean RC, Bell G, Rainey PB, (2004) The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proceedings of the National Academy of Sciences of the USA 101: 8072–8077.
16. Remold SK, (2012) Understanding specialism when the jack of all trades can be the master of all. Proceedings of the National Academy of Sciences of the USA 98: 11388–11393.
17. Turner P, Morales N, Alto B, Remold S, (2010) Role of evolved host breadth in the initial emergence of an RNA virus. Evolution 64: 3273–3286.
18. Elena SF, Agudelo-Romero P, Lalic J, (2009) The evolution of viruses in multi-host fitness landscapes. The Open Virology Journal 3: 1–6.
19. Caraco T, Wang IN, (2008) Free-living pathogens: life-history constraints and strain competition. Journal of Theoretical Biology 250: 569–579.
20. Handel A, Bennett MR, (2008) Surviving the bottleneck: transmission mutants and the evolution of microbial populations. Genetics 180: 2193–2200.
21. Bonhoeffer S, Lenski RE, Ebert D, (1996) The curse of the pharaoh: the evolution of virulence in pathogens with long living propagules. Proceedings of the Royal Society of London B Biological Sciences 263: 715–721.
22. Gandon S, (1998) The curse of the pharaoh hypothesis. Proceedings of the Royal Society of London B Biological Sciences 265: 1545–1552.
23. De Paepe M, Taddei F, (2006) Viruses' life history: towards a mechanistic basis of a trade-off between survival and reproduction among phages. PLoS Biology 4: e193.
24. Ewens WJ, (1967) The probability of survival of a new mutant in a fluctuating environment. Heredity 43: 438–443.
25. Wahl LM, Gerrish PJ, (2001) The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55: 2606–2610.
26. Heffernan JM, Wahl LM, (2002) The effects of genetic drift in experimental evolution. Theoretical Population Biology 62: 349–356.
27. Wahl LM, Gerrish PJ, Saika-Voivod I, (2002) Evaluating the impact of population bottlenecks in experimental evolution. Genetics 162: 961–971.
28. DePristo MA, Weinreich DM, Hartl DL, (2005) Missense meanderings in sequence space: a biophysical view of protein evolution. Nature Reviews Genetics 6: 678–687.
29. Zlotnick A, (1994) To build a virus capsid: an equilibrium model of the self assembly of polyhedral protein complexes. Journal of Molelcular Biology 241: 59–67.
30. Zlotnick A, (2003) Are weak protein-protein interactions the general rule in capsid assembly? Virology 315: 269–274.
31. Zlotnick A, (2005) Theoretical aspects of virus capsid assembly. Journal of Molecular Recognition 18: 479–490.
32. Ceres P, Zlotnick A, (2002) Weak protein-protein interactions are sufficient to drive assembly of hepatitis B virus capsids. Biochemistry 41: 11525–11531.
33. Crill WD, Wichman HA, Bull JJ, (2000) Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154: 27–37.
34. Inagaki M, Kawaura T, Wakashima H, Kato M, Nishikawa S, et al. (2003) Different contributions of the outer and inner R-core residues of lipopolysaccharide to the recognition by spike H and G proteins of bacteriophage φX174. FEMS Microbiol Lett 226: 221–227.
35. Sun L, Young L, Zhang X, Boudko S, Fokine A, et al. (2014) Icosahedral bacteriophage φX174 forms a tail for DNA transport during infection. Nature 505: 432–443.
36. Dessau M, Goldhill D, McBride R, Turner P, Modis Y, (2012) Selective pressure causes an rna virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme. PLoS Genetics 8: e1003102.
37. Goldman RP, Travisano M, (2011) Experimental evolution of ultraviolet radiation resistance in Escherichia coli. Evolution 65: 3486–3498.
38. Leiby N, Marx C, (2014) Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biology 12: 1–10.
39. Rokyta DR, Abdo Z, Wichman HA, (2009) The genetics of adaptation for eight microvirid bacteriophages. Journal of Molecular Evolution 69: 229–239.
40. Rokyta DR, Joyce P, Caudle SB, Wichman HA, (2005) An empirical test of the mutational landscape model of adaptation using a single-stranded DNA virus. Nature Genetics 37: 441–444.
41. Travisano M, Vasi F, Lenski RE, (1995) Long-term experimental evolution in Escherichia coli. III. variation among replicate populations in correlated responses to novel environments. Evolution 49: 189–200.
42. Ostrowski E, Rozen D, Lenski R, (2005) Pleiotropic effects of beneficial mutations in Escherichia coli. Evolution 59: 2343–2352.
43. Fisher RA (1930) The genetical theory of natural selection. Oxford (UK): Oxford University Press.
44. Sniegowski P, Gerrish P, Lenski R, (1997) Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387: 703–705.
45. Rosche W, Foster P, Cairns J, (1999) The role of transient hypermutators in adaptive mutation in Escherichia coli. Proceedings of the National Academy of Sciences of the USA 96: 6862–6867.
46. Wielgoss S, Barrick JE, Tenaillon O, Wiser MJ, Dittmar WJ, et al. (2013) Mutation rate dynamics in a bacterial population reflect tension between adaptation and genetic load. Proceedings of the National Academy of Sciences of the USA 110: 222–227.
47. Cuevas JM, Duffy S, Sanjuán R, (2009) Point mutation rate of bacteriophage?x174. Genetics 183: 747–749.
48. Zheng L, Yang W, (2012) Practically efficient and robust free energy calculations: double-integration orthogonal space tempering. Journal of Chemical Theory and Computation 8: 810–823.
49. McKenna R, Bowman BR, Ilag LL, Rossmann MG, Fane BA, (1996) Atomic structure of the degraded procapsid particle of the bacteriophage G4: induced structural changes in the presence of calcium ions and functional implications. Journal of Molelcular Biology 256: 736–750.
50. Zheng L, Chen M, Yang W, (2008) Random walk in orthogonal space to achieve efficient free-energy simulation of complex systems. Proceedings of the National Academy of Sciences of the USA 105: 20227–20232.
51. Zheng L, Chen M, Yang W, (2009) Simultaneous escaping of explicit and hidden free energy barriers: application of the orthogonal space random walk strategy in generalized ensemble based conformational sampling. Journal of Chemical Physics 130: 234105.
52. Berezovsky IN, Shakhnovich EI, (2005) Physics and evolution of thermophilic adaptation. Proceedings of the National Academy of Sciences of the USA 102: 12742–12747.
53. Aharoni A, Gaidukov L, Khersonsky O, Gould SM, Roodveldt C, et al. (2004) The 'evolvability' of promiscuous protein functions. Nature Genetics 37: 73–76.
54. Bloom JD, Labthavikul ST, Otey CR, Arnold FH, (2006) Protein stability promotes evolvability. Proceedings of the National Academy of Sciences of the USA 103: 5869–5874.
55. Tokuriki N, Tawfik D, (2009) Stability effects of mutations and protein evolvability. Current Opinion in Structural Biology 19: 1–9.
56. Besenmatter W, Kast P, Hilvert D, (2007) Relative tolerance of mesostable and thermostable protein homologs to extensive mutation. Proteins 66: 500–506.
57. Domingo-Calap P, Pereira-Gómez M, Sanjuá R, (2010) Selection for thermostability can lead to the emergence of mutational robustness in an RNA virus. Journal of Evolutionary Biology 23: 2453–2460.
58. Tembe B, McCammon J, (1984) Ligand receptor interactions. Journal of Computational Chemistry 8: 281–283.
59. Jorgensen W, Ravimohan C, (1985) Monte-carlo simulation of differences in free-energies of hydration. Journal of the American Chemical Society 83: 3050–3054.
60. Straatsman T, McCammon J, (1992) Computational alchemy. Annual Review of Physical Chemistry 43: 407–435.
61. Jorgensen W, Thomas L, (2008) Perspective on free-energy perturbation calculations for chemical equilibria. Journal of Chemical Theory and Computation 4: 869–876.
62. AD MacKerell J, Bashford D, Bellott M, Jr RD, Evanseck J, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. Journal of Physical Chemistry B 102: 3586–3616.
63. Jorgensen W, Chandrasekhar J, Madura J, Impey R, Klein M, (1983) Comparison of simple potential functions for simulating liquid water. Journal of Chemical Physics 79: 926–935.
64. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. Journal of Chemical Physics 98: 10089–10092.
65. Zacharias M, Straatsma T, McCammon J, (1994) Separation-shifted scaling: A new scaling method for lennard-jones interactions in thermodynamic integration. Journal of Chemical Physics 100: 9025–9031.