Adaptive regulatory substitutions affect multiple stages in the life cycle of the bacteriophage φx174

BMC Evolutionary Biology

Volumn 13, Issue 1, 2013, Pages

  Brown, Celeste J ^a   Stancik, Amber D ^a   Roychoudhury, Pavitra ^a   Krone, Stephen M ^a  

^a UNIVERSITY OF IDAHO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BACTERIOPHAGE; FITNESS; GENE EXPRESSION; HIGH TEMPERATURE; PHENOTYPE; PLEIOTROPY; TRADE-OFF;

ENTEROBACTERIA PHAGE PHIX174;

ARTICLE; BACTERIOPHAGE PHI X 174; BIOLOGICAL MODEL; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; MUTATION; PHYSIOLOGY; REPRODUCTIVE FITNESS; VIROLOGY; VIRUS ASSEMBLY;

BACTERIOPHAGE PHI X 174; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, VIRAL; GENETIC FITNESS; MODELS, BIOLOGICAL; MUTATION; TRANSCRIPTION, GENETIC; VIRUS ASSEMBLY;

MLCS; MLOWN;

EID: 84875058100     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-13-66     Document Type: Article

References (50)

1. Positive selection at high temperature reduces gene transcription in the bacteriophage φ X174. Brown CJ, Zhao L, Evans KJ, Ally D, Stancik AD, BMC Evol Biol 2010 10 378 10.1186/1471-2148-10-378 21129199
2. Differential transcription of bacteriophage φ X174 genes at 37°C and 42°C. Zhao L, Stancik AD, Brown CJ, PLoS One 2012 7 4 35909 10.1371/journal.pone.0035909 22540010
3. Mapping of in vivo messenger RNAs for bacteriophage phiX-174. Hayashi M, Fujimura FK, Hayashi M, Proc Natl Acad Sci USA 1976 73 10 3519 3523 10.1073/pnas.73.10.3519 1068463
4. Experimental evolution of viruses: Microviridae as a model system. Wichman HA, Brown CJ, Philos Trans R Soc Lond B Biol Sci 2010 365 2495 2501 10.1098/rstb.2010.0053 20643739
5. Exceptional convergent evolution in a virus. Bull JJ, Badgett MR, Wichman HA, Huelsenbeck JP, Hillis DM, Gulati A, Ho C, Molineux IJ, Genetics 1997 147 4 1497 1507 9409816 (Pubitemid 27525448)
6. Evolutionary reversals during viral adaptation to alternating hosts. Crill WD, Wichman HA, Bull JJ, Genetics 2000 154 1 27 37 10628966 (Pubitemid 30045898)
7. Different trajectories of parallel evolution during viral adaptation. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ, Science 1999 285 5426 422 424 10.1126/science.285.5426.422 10411508 (Pubitemid 29343967)
8. Experimental evolution recapitulates natural evolution. Wichman HA, Scott LA, Yarber CD, Bull JJ, Philos Trans R Soc Lond B Biol Sci 2000 355 1403 1677 1684 10.1098/rstb.2000.0731 11127915
9. Mapping the B and D gene promoters of bacteriophage S13 by footprinting and exonuclease III analysis. Arquint M, Spencer JH, J Virol 1987 61 12 3694 3700 2824808 (Pubitemid 18011464)
10. φX174 et al. The Microviridae. Fane BA, Brentlinger KL, Burch AD, Chen M, Hafenstein S, Moore E, Novak CR, Uchiyama A, The Bacteriophages New York: Oxford Press, Calendar R, 2 2006 129 145
11. Interaction of morphogenetic genes of bacteriophage T4. Floor E, J Mol Biol 1970 47 3 293 306 10.1016/0022-2836(70)90303-7 4907266
12. Properties of a mutant of Escherichia coli defective in bacteriophage lambda head formation (groE). II. The propagation of phage lambda. Sternberg N, J Mol Biol 1973 76 1 25 44 10.1016/0022-2836(73)90079-X 4578099
13. Biology of the Bacteriophage φX174. Hayashi M, Aoyama A, Richardson DL, Hayashi MN, The Bacteriophages, Volume II New York: Plenum Press, Calendar R, 1988 1 71
14. UCSF Chimera-a visualization system for exploratory research and analysis. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE, J Comput Chem 2004 25 13 1605 1612 10.1002/jcc.20084 15264254
15. Space, time, and host evolution facilitate coexistence of competing bacteriophages: theory and experiment. Coberly LC, Wei W, Sampson KY, Millstein J, Wichman HA, Krone SM, Am Nat 2009 173 4 121 E138 10.1086/597226 19226233
16. Spatial self-organization in a cyclic resource-species model. Krone SM, Guan YT, J Theor Biol 2006 241 1 14 25 10.1016/j.jtbi.2005.11.005 16360180 (Pubitemid 43817985)
17. Spatial invasion by a mutant pathogen. Wei W, Krone SM, J Theor Biol 2005 236 3 335 348 10.1016/j.jtbi.2005.03.016 15899503 (Pubitemid 41008699)
18. The phenotype-fitness map in experimental evolution of phages. Bull JJ, Heineman RH, Wilke CO, PLoS One 2011 6 11 27796 10.1371/journal.pone.0027796 22132144
19. Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Brown CJ, Todd KM, Rosenzweig RF, Mol Biol Evol 1998 15 8 931 942 10.1093/oxfordjournals.molbev.a026009 9718721 (Pubitemid 28364447)
20. Transcription, translation, and the evolution of specialists and generalists. Zhong S, Miller SP, Dykhuizen DE, Dean AM, Mol Biol Evol 2009 26 12 2661 2678 10.1093/molbev/msp187 19706726
21. The cost of expression of Escherichia coli lac operon proteins is in the process, not in the products. Stoebel DM, Dean AM, Dykhuizen DE, Genetics 2008 178 3 1653 1660 10.1534/genetics.107.085399 18245823
22. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. Cooper VS, Schneider D, Blot M, Lenski RE, J Bacteriol 2001 183 9 2834 2841 10.1128/JB.183.9.2834-2841.2001 11292803 (Pubitemid 32319286)
23. Physiological characterization of adaptive clones in evolving populations of the yeast, Saccharomyces cerevisiae. Adams J, Paquin C, Oeller PW, Lee LW, Genetics 1985 110 2 173 185 3891508 (Pubitemid 15116799)
24. Functional and metabolic effects of adaptive glycerol kinase (glpK) mutants in Escherichia coli. Applebee MK, Joyce AR, Conrad T, Pettigrew DW, Palsson BO, J Biol Chem 2011 286 26 23150 23159 10.1074/jbc.M110.195305 21550976
25. Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Fong SS, Joyce AR, Palsson BO, Genome Res 2005 15 10 1365 1372 10.1101/gr.3832305 16204189 (Pubitemid 41400902)
26. Selective pressure causes an RNA virus to trade reproductive fitness for increased structural and thermal stability of a viral enzyme. Dessau M, Goldhill D, McBride RL, Turner PE, Modis Y, PLoS Genet 2012 8 11 1003102 10.1371/journal.pgen.1003102 23209446
27. A negative relationship between mutation pleiotropy and fitness effect in yeast. Cooper TF, Ostrowski EA, Travisano M, Evolution 2007 61 6 1495 1499 10.1111/j.1558-5646.2007.00109.x 17542856 (Pubitemid 46848822)
28. Two steps forward, one step back: the pleiotropic effects of favoured alleles. Otto SP, Proc Biol Sci 2004 271 1540 705 714 10.1098/rspb.2003.2635 15209104 (Pubitemid 38437940)
29. Evolution at two levels: on genes and form. Carroll SB, PLoS Biol 2005 3 7 245 10.1371/journal.pbio.0030245 16000021 (Pubitemid 41032181)
30. A preliminary analysis of gene pleiotropy estimated from protein sequences. Su Z, Zeng Y, Gu X, J Exp Zool B Mol Dev Evol 2009 314 2 115 122
31. Genomic patterns of pleiotropy and the evolution of complexity. Wang Z, Liao BY, Zhang J, Proc Natl Acad Sci USA 2010 107 42 18034 18039 10.1073/pnas.1004666107 20876104
32. Factors influencing lysis time stochasticity in bacteriophage lambda. Dennehy JJ, Wang IN, BMC Microbiol 2011 11 174 10.1186/1471-2180-11-174 21810267
33. Energy-efficient growth of phage Q Beta in Escherichia coli. Kim H, Yin J, Biotechnol Bioeng 2004 88 2 148 156 10.1002/bit.20226 15449299 (Pubitemid 39422986)
34. Effects of Escherichia coli physiology on growth of phage T7 in vivo and in silico. You L, Suthers PF, Yin J, J Bacteriol 2002 184 7 1888 1894 10.1128/JB.184.7.1888-1894.2002 11889095 (Pubitemid 34275531)
35. Temperature dependence of RNA synthesis parameters in Escherichia coli. Ryals J, Little R, Bremer H, J Bacteriol 1982 151 2 879 887 6178724 (Pubitemid 12027977)
36. Big-benefit mutations in a bacteriophage inhibited with heat. Bull JJ, Badgett MR, Wichman HA, Mol Biol Evol 2000 17 6 942 950 10.1093/oxfordjournals. molbev.a026375 10833201 (Pubitemid 30346554)
37. First-step mutations for adaptation at elevated temperature increase capsid stability in a virus. Lee KH, Miller CR, Nagel AC, Wichman HA, Joyce P, Ytreberg FM, PLoS One 2011 6 9 25640 10.1371/journal.pone.0025640 21980515
38. Nucleation and growth phases in the polymerization of coat and scaffolding subunits into icosahedral procapsid shells. Prevelige PE Jr, Thomas D, King J, Biophys J 1993 64 3 824 835 10.1016/S0006-3495(93)81443-7 8471727 (Pubitemid 23130349)
39. To build a virus capsid. An equilibrium model of the self assembly of polyhedral protein complexes. Zlotnick A, J Mol Biol 1994 241 1 59 67 10.1006/jmbi.1994.1473 8051707 (Pubitemid 24263411)
40. Interaction of the transmembrane domain of lysis protein E from bacteriophage φX174 with bacterial translocase MraY and peptidyl-prolyl isomerase SlyD. Mendel S, Holbourn JM, Schouten JA, Bugg TD, Microbiology 2006 152 Pt 10 2959 2967 17005977 (Pubitemid 44542377)
41. Genetic evidence that the bacteriophage φX174 lysis protein inhibits cell wall synthesis. Bernhardt TG, Roof WD, Young R, Proc Natl Acad Sci USA 2000 97 8 4297 4302 10.1073/pnas.97.8.4297 10760296 (Pubitemid 30226127)
42. Bacteriophage lysis: mechanism and regulation. Young R, Microbiol Rev 1992 56 3 430 481 1406491
43. Noise in timing and precision of gene activities in a genetic cascade. Amir A, Kobiler O, Rokney A, Oppenheim AB, Stavans J, Mol Syst Biol 2007 3 71 17299413
44. Genetic regulatory mechanisms in the synthesis of proteins. Jacob F, Monod J, J Mol Biol 1961 3 318 356 10.1016/S0022-2836(61)80072-7 13718526
45. On the regulation of gene activity. Jacob F, Monod J, Cold Spring Harb Symp Quant Biol 1961 26 193 209 10.1101/SQB.1961.026.01.024
46. φX174 genome-capsid interactions influence the biophysical properties of the virion: evidence for a scaffolding-like function for the genome during the final stages of morphogenesis. Hafenstein S, Fane BA, J Virol 2002 76 11 5350 5356 10.1128/JVI.76.11.5350-5356.2002 11991963 (Pubitemid 34517885)
47. slyD, a host gene required for φX174 lysis, is related to the FK506-binding protein family of peptidyl-prolyl cis-trans-isomerases. Roof WD, Horne SM, Young KD, Young R, J Biol Chem 1994 269 4 2902 2910 8300625
48. The process of infection with bacteriophage φX174. XXXII. Early steps in the infection process: attachment, eclipse and DNA penetration. Newbold JE, Sinsheimer RL, J Mol Biol 1970 49 1 49 66 10.1016/0022-2836(70)90375-X 5450517
49. Characterization and function of putative substrate specificity domain in microvirus external scaffolding proteins. Uchiyama A, Chen M, Fane BA, J Virol 2007 81 16 8587 8592 10.1128/JVI.00301-07 17553892 (Pubitemid 47242832)
50. The growth of bacterial cultures. Monod J, Annu Rev Microbiol 1949 3 371 394 10.1146/annurev.mi.03.100149.002103