期刊论文详细信息
BMC Evolutionary Biology
Evolution at increased error rate leads to the coexistence of multiple adaptive pathways in an RNA virus
Ester Lázaro1  María Arribas1  Laura Cabanillas1 
[1] Centro de Astrobiología (CSIC-INTA) Ctra de Ajalvir Km 4, Torrejón de Ardoz, Madrid, 28850, Spain
关键词: Polymorphisms;    Epistasis;    5-azacytidine;    Mutagenesis;    Beneficial mutations;    Interference;    RNA viruses;   
Others  :  1130256
DOI  :  10.1186/1471-2148-13-11
 received in 2012-08-01, accepted in 2013-01-11,  发布年份 2013
PDF
【 摘 要 】

Background

When beneficial mutations present in different genomes spread simultaneously in an asexual population, their fixation can be delayed due to competition among them. This interference among mutations is mainly determined by the rate of beneficial mutations, which in turn depends on the population size, the total error rate, and the degree of adaptation of the population. RNA viruses, with their large population sizes and high error rates, are good candidates to present a great extent of interference. To test this hypothesis, in the current study we have investigated whether competition among beneficial mutations was responsible for the prolonged presence of polymorphisms in the mutant spectrum of an RNA virus, the bacteriophage Qβ, evolved during a large number of generations in the presence of the mutagenic nucleoside analogue 5-azacytidine.

Results

The analysis of the mutant spectra of bacteriophage Qβ populations evolved at artificially increased error rate shows a large number of polymorphic mutations, some of them with demonstrated selective value. Polymorphisms distributed into several evolutionary lines that can compete among them, making it difficult the emergence of a defined consensus sequence. The presence of accompanying deleterious mutations, the high degree of recurrence of the polymorphic mutations, and the occurrence of epistatic interactions generate a highly complex interference dynamics.

Conclusions

Interference among beneficial mutations in bacteriophage Qβ evolved at increased error rate permits the coexistence of multiple adaptive pathways that can provide selective advantages by different molecular mechanisms. In this way, interference can be seen as a positive factor that allows the exploration of the different local maxima that exist in rugged fitness landscapes.

【 授权许可】

   
2013 Cabanillas et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150226190456692.pdf 548KB PDF download
Figure 3. 61KB Image download
Figure 2. 30KB Image download
Figure 1. 56KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】
  • [1]Muller HJ: Some genetic aspects of sex. Am Nat 1932, 68:118-138.
  • [2]Muller HJ: The relation of recombination to mutational advance. Mutat Res 1964, 106:2-9.
  • [3]Atwood KC, Schneider LK, Ryan FJ: Periodic selection in Escherichia coli. Proc Natl Acad Sci USA 1951, 37:146-155.
  • [4]Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M: Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci USA 1999, 96:3807-3812.
  • [5]Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ: Different trajectories of parallel evolution during viral adaptation. Science 1999, 285:422-424.
  • [6]Holder KK, Bull JJ: Profiles of adaptation in two similar viruses. Genetics 2001, 159:1393-1404.
  • [7]Rozen DE, de Visser JA, Gerrish PJ: Fitness effects of fixed beneficial mutations in microbial populations. Curr Biol 2002, 12:1040-1045.
  • [8]Shaver AC, Dombrowski PG, Sweeney JY, Treis T, Zappala RM, Sniegowski PD: Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 2002, 162:557-566.
  • [9]de Visser JA, Rozen DE: Clonal interference and the periodic selection of new beneficial mutations in Escherichia coli. Genetics 2006, 172:2093-2100.
  • [10]Lang GI, Botstein D, Desai MM: Genetic variation and the fate of beneficial mutations in asexual populations. Genetics 2011, 188:647-661.
  • [11]de Visser JA, Rozen DE: Limits to adaptation in asexual populations. J Evol Biol 2005, 18:779-788.
  • [12]Sniegowski PD, Gerrish PJ: Beneficial mutations and the dynamics of adaptation in asexual populations. Philos Trans R Soc Lond B Biol Sci 2010, 365:1255-1263.
  • [13]Gerrish PJ, Lenski RE: The fate of competing beneficial mutations in an asexual population. Genetica 1998, 102–103:127-144.
  • [14]Wilke CO: The speed of adaptation in large asexual populations. Genetics 2004, 167:2045-2053.
  • [15]Orr HA: The rate of adaptation in asexuals. Genetics 2000, 155:961-968.
  • [16]Orr HA: The distribution of fitness effects among beneficial mutations. Genetics 2003, 163:1519-1526.
  • [17]Desai M, Fisher DS: Beneficial mutation-selection balance and the effect of linkage on positive selection. Genetics 2007, 176:1759-1798.
  • [18]Desai M, Fisher DS, Murray AW: The speed of evolution and maintenance of variation in asexual populations. Curr Biol 2007, 17:385-394.
  • [19]Brunet E, Rouzine IM, Wilke CO: The stochastic edge in adaptive evolution. Genetics 2008, 179:603-620.
  • [20]Hegreness M, Shoresh N, Hartl D, Kishony R: An equivalence principle for the incorporation of favorable mutations in asexual populations. Science 2006, 17(311):1615-1617.
  • [21]Park SC, Krug J: Clonal interference in large populations. Proc Natl Acad Sci USA 2007, 104:18135-18140.
  • [22]de Visser JA, Zeyl CW, Gerrish PJ, Blanchard JL, Lenski RE: Diminishing returns from mutation supply rate in asexual populations. Science 1999, 283:404-406.
  • [23]Barrick JE, Lenski RE: Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 2009, 74:119-29.
  • [24]Miralles R, Gerrish PJ, Moya A, Elena SF: Clonal interference and the evolution of RNA viruses. Science 1999, 285:1745-1747.
  • [25]Kao KC, Sherlock G: Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 2008, 40:1499-1504.
  • [26]Bollback JP, Huelsenbeck JP: Clonal interference is alleviated by high mutation rates in large populations. Mol Biol Evol 2007, 24:1397-1406.
  • [27]Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, Ward A, DeSevo CG, Botstein D, Dunham MJ: The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 2008, 4(12):e1000303.
  • [28]Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF: Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 2009, 461:1243-1247.
  • [29]Betancourt AJ: Genomewide patterns of substitution in adaptively evolving populations of the RNA bacteriophage MS2. Genetics 2009, 181:1535-1544.
  • [30]Miller CR, Joyce P, Wichman HA: Mutational effects and population dynamics during viral adaptation challenge current models. Genetics 2011, 187:185-202.
  • [31]Arribas M, Cabanillas L, Lázaro E: Identification of mutations conferring 5-azacytidine resistance in bacteriophage Qβ. Virology 2011, 417:343-352.
  • [32]Cases-González C, Arribas M, Domingo E, Lázaro E: Beneficial effects of population bottlenecks in an RNA virus evolving at increased error rate. J Mol Biol 2008, 384:1120-1129.
  • [33]Barrera I, Schuppli D, Sogo JM, Weber H: Different mechanisms of recognition of bacteriophage Qβ plus and minus strand RNAs by Qβ replicase. J Mol Biol 1993, 232:512-521.
  • [34]The HIV databases. http://www.hiv.lanl.gov webcite
  • [35]Korber B: HIV Signature and Sequence Variation Analysis. In Computational Analysis of HIV Molecular Sequences. Edited by Rodrigo AG, Learn GH. Dordrecht, Netherlands: Kluwer Academic Publishers; 2000:55-72.
  • [36]Lynch M, Gabriel W: Mutational load and the survival of small populations. Evolution 1990, 44:1725-1737.
  • [37]Lázaro E, Escarmís C, Pérez-Mercader J, Manrubia SC, Domingo E: Resistance of virus to extinction on bottleneck passages: study of a decaying and fluctuating pattern of fitness loss. Proc Natl Acad Sci USA 2003, 100:10830-10835.
  • [38]Escarmís C, Lázaro E, Manrubia SC: Population bottlenecks in quasispecies dynamics. Curr Top Microbiol Immunol 2006, 299:141-70.
  • [39]Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010, 59:307-321.
  • [40]Drake JW: Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci USA 1993, 90:4171-4175.
  • [41]Drake JW, Charlesworth B, Charlesworth D, Crow JF: Rates of spontaneous mutation. Genetics 1998, 148:1667-1686.
  • [42]Domingo E, Sabo D, Taniguchi T, Weissmann C: Nucleotide sequence heterogeneity of an RNA phage population. Cell 1978, 13:735-744.
  • [43]Pfeiffer JK, Kirkegaard K: Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice. PLoS Pathog 2005, 1(2):e11.
  • [44]Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R: Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 2006, 439:344-348.
  • [45]Holland JJ, Domingo E, de la Torre JC, Steinhauer DA: Mutation frequencies at defined single codon sites in vesicular stomatitis virus and poliovirus can be increased only slightly by chemical mutagenesis. J Virol 1990, 64:3960-3962.
  • [46]Loeb LA, Essigmann JM, Kazazi F, Zhang J, Rose KD, Mullins JI: Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA 1999, 96:1492-1497.
  • [47]Domingo E: Virus entry into error catastrophe as a new antiviral strategy. Virus Res 2005, 107:115-228.
  • [48]Springman R, Keller T, Molineux IJ, Bull JJ: Evolution at a high imposed mutation rate: adaptation obscures the load in phage T7. Genetics 2010, 184:221-232.
  • [49]Mills DR, Priano C, Merz P, Binderow BD: Qβ RNA bacteriophage: mapping cis-acting elements within an RNA genome. J Virol 1990, 64:3872-3881.
  • [50]Klovins J, Berzins V, van Duin J: A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 3′ end is required for replication. RNA 1998, 4:948-957.
  • [51]Klovins J, van Duin J: A long-range pseudoknot in Qbeta RNA is essential for replication. J Mol Biol 1999, 294:875-884.
  • [52]Pybus OG, Rambaut A, Belshaw R, Freckleton RP, Drummond AJ, Holmes EC: Phylogenetic evidence for deleterious mutation load in RNA viruses and its contribution to viral evolution. Mol Biol Evol 2007, 24:845-852.
  • [53]Shao Y, Wang IN: Bacteriophage adsorption rate and optimal lysis time. Genetics 2008, 180:471-482.
  • [54]Sanjuán R, Moya A, Elena SF: The contribution of epistasis to the architecture of fitness in an RNA virus. Proc Natl Acad Sci USA 2004, 101:15376-15379.
  • [55]Sanjuán R, Cuevas JM, Moya A, Elena SF: Epistasis and the adaptability of an RNA virus. Genetics 2005, 170:1001-1008.
  • [56]Sanjuán R, Elena SF: Epistasis correlates to genomic complexity. Proc Natl Acad Sci USA 2006, 103:14402-14405.
  • [57]Weinreich DM, Watson RA, Chao L: Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 2005, 59:1165-1174.
  • [58]Betancourt AJ: Lack of evidence for sign epistasis between beneficial mutations in an RNA bacteriophage. J Mol Evol 2010, 71:437-443.
  • [59]Chetverin AB, Chetverina HV, Demidenko AA, Ugarov VI: Nonhomologous RNA recombination in a cell-free system: evidence for a transesterification mechanism guided by secondary structure. Cell 1997, 88:503-513.
  • [60]Palasingam K, Shaklee PN: Reversion of Q beta RNA phage mutants by homologous RNA recombination. J Virol 1992, 66:2435-2442.
  • [61]Kim Y, Orr HA: Adaptation in sexuals vs. asexuals: clonal interference and the Fisher-Muller model. Genetics 2005, 171:1377-1386.
  • [62]Charlesworth B, Morgan MT, Charlesworth D: The effect of deleterious mutations on neutral molecular variation. Genetics 1993, 134:1289-1303.
  • [63]Elena SF, Sanjuán R: RNA viruses as complex adaptive systems. Biosystems 2005, 81:31-41.
  • [64]Lalić J, Elena SF: Magnitude and sign epistasis among deleterious mutations in a positive-sense plant RNA virus. Heredity 2012, 109:71-7.
  • [65]Eigen M, Schuster P: The hypercycle. A principle of natural self-organization. Berlin: Springer; 1979.
  • [66]Nowak M, Schuster P: Error thresholds of replication in finite populations mutation frequencies and the onset of Muller's ratchet. J Theor Biol 1989, 137:375-395.
  • [67]Biebricher CK, Eigen M: The error threshold. Virus Res 2005, 107:117-127.
  • [68]Eigen M: Error catastrophe and antiviral strategy. Proc Natl Acad Sci USA 2002, 99:13374-13376.
  • [69]Lázaro E: RNA Viruses: Control, Mutagenesis and Extinction. Chichester: John Wiley & Sons, Ltd; [eLS]
  文献评价指标  
  下载次数:49次 浏览次数:28次