Correlation Between Mutation Rate and Genome Size in Riboviruses: Mutation Rate of Bacteriophage Qβ

Bradwell, Katie R.; Combe, Marine; Domingo‐Calap, Pilar; Sanjuán, Rafael

doi:10.1534/genetics.113.154963

Cited by 63 publications

(50 citation statements)

References 52 publications

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“…Higher values increase both standing levels of variation through mutation-selection balance and the supply rate of new beneficial mutations. Mutation rates in turn might correlate with other traits such as genome size, number of cell divisions per generation, or metabolic rates (Bradwell et al 2013). Effects on evolutionary rates are expected to be linear at low values and to saturate as the product of mutation rate and population size, termed θ, increases (Maynard Smith 1976).…”

Section: Evolutionary Dynamics With No Species Interactionsmentioning

confidence: 99%

How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities?

Barraclough

2015

Annu. Rev. Ecol. Evol. Syst.

145

130

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Theories of how species evolve in changing environments mostly consider single species in isolation or pairs of interacting species. Yet all organisms live in diverse communities containing many hundreds of species. This review discusses how species interactions influence the evolution of constituent species across whole communities. When species interactions are weak or inconsistent, evolutionary dynamics should be predictable by factors identified by single-species theory. Stronger species interactions, however, can alter evolutionary outcomes and either dampen or promote evolution of constituent species depending on the number of species and the distribution of interaction strengths across the interaction network. Genetic interactions, such as horizontal gene transfer, might also affect evolutionary outcomes. These evolutionary mechanisms in turn affect whole-community properties, such as the level of ecosystem functioning. Successful management of both ecosystems and focal species requires new understanding of evolutionary interactions across whole communities.

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Section: Evolutionary Dynamics With No Species Interactionsmentioning

confidence: 99%

How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities?

Barraclough

2015

Annu. Rev. Ecol. Evol. Syst.

145

130

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“…In addition to the four proteins covering 95.5% of the whole genome, the secondary and tertiary structures of the Q␤ RNA genome are essential for its amplification (25)(26)(27). The genome is 4,217 bases in length (25) and has a high error rate of 10 Ϫ3 to 10 Ϫ5 per base per replication (28)(29)(30)), thus facilitating genome-level experimental evolution.…”

mentioning

confidence: 99%

Contribution of Silent Mutations to Thermal Adaptation of RNA Bacteriophage Qβ

Kashiwagi

Sugawara

Tsushima

et al. 2014

J Virol

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Changes in protein function and other biological properties, such as RNA structure, are crucial for adaptation of organisms to novel or inhibitory environments. To investigate how mutations that do not alter amino acid sequence may be positively selected, we performed a thermal adaptation experiment using the single-stranded RNA bacteriophage Q␤ in which the culture temperature was increased from 37.2°C to 41.2°C and finally to an inhibitory temperature of 43.6°C in a stepwise manner in three independent lines. Whole-genome analysis revealed 31 mutations, including 14 mutations that did not result in amino acid sequence alterations, in this thermal adaptation. Eight of the 31 mutations were observed in all three lines. Reconstruction and fitness analyses of Q␤ strains containing only mutations observed in all three lines indicated that five mutations that did not result in amino acid sequence changes but increased the amplification ratio appeared in the course of adaptation to growth at 41.2°C. Moreover, these mutations provided a suitable genetic background for subsequent mutations, altering the fitness contribution from deleterious to beneficial. These results clearly showed that mutations that do not alter the amino acid sequence play important roles in adaptation of this single-stranded RNA virus to elevated temperature. IMPORTANCERecent studies using whole-genome analysis technology suggested the importance of mutations that do not alter the amino acid sequence for adaptation of organisms to novel environmental conditions. It is necessary to investigate how these mutations may be positively selected and to determine to what degree such mutations that do not alter amino acid sequences contribute to adaptive evolution. Here, we report the roles of these silent mutations in thermal adaptation of RNA bacteriophage Q␤ based on experimental evolution during which Q␤ showed adaptation to growth at an inhibitory temperature. Intriguingly, four synonymous mutations and one mutation in the untranslated region that spread widely in the Q␤ population during the adaptation process at moderately high temperature provided a suitable genetic background to alter the fitness contribution of subsequent mutations from deleterious to beneficial at a higher temperature.

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“…Also, single-stranded viruses tend to show higher mutation rates than double-stranded genomes (6,7). Furthermore, in DNA viruses and, to a lesser extent, RNA viruses mutation rates correlate negatively with genome size, although the causes of this correlation remain poorly understood (8)(9)(10)(11). In theory, mutation rates should be evolutionarily adjusted in response to several factors, including the fitness costs incurred by deleterious mutations (12)(13)(14)(15); the energy costs of encoding replication fidelity mechanisms (15,16); the benefits of increasing adaptability (17,18), population size (19,20), and structure (21); and the topology of the fitness landscape (22).…”

Section: Iral Mutation Rates Vary Amply From 10mentioning

confidence: 99%

Delayed Lysis Confers Resistance to the Nucleoside Analogue 5-Fluorouracil and Alleviates Mutation Accumulation in the Single-Stranded DNA Bacteriophage ϕX174

Pereira-Gómez¹,

Sanjuán²

2014

J Virol

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Rates of spontaneous mutation determine viral fitness and adaptability. In RNA viruses, treatment with mutagenic nucleoside analogues selects for polymerase variants with increased fidelity, showing that viral mutation rates can be adjusted in response to imposed selective pressures. However, this type of resistance is not possible in viruses that do not encode their own polymerases, such as single-stranded DNA viruses. We previously showed that serial passaging of bacteriophage X174 in the presence of the nucleoside analogue 5-fluorouracil (5-FU) favored substitutions in the lysis protein E (P. Domingo-Calap, M. Pereira-Gomez, and R. Sanjuán, J. Virol. 86:9640 -9646, 2012, doi:10.1128/JVI.00613-12). Here, we found that approximately half (6/12) of the amino acid replacements in the N-terminal region of this protein led to delayed lysis, and two of these changes (V2A and D8A) also conferred partial resistance to 5-FU. By delaying lysis, the V2A and D8A substitutions allowed the virus to increase the burst size per cell in the presence of 5-FU. Furthermore, these substitutions tended to alleviate drug-induced mutagenesis by reducing the number of rounds of copying required for population growth, revealing a new mechanism of resistance. This form of mutation rate regulation may also be utilized by other viruses whose replication mode is similar to that of bacteriophage X174. IMPORTANCEMany viruses display high rates of spontaneous mutations due to defects in proofreading or postreplicative repair, allowing them to rapidly adapt to changing environments. Viral mutation rates may have been optimized to achieve high adaptability without incurring an excessive genetic load. Supporting this, RNA viruses subjected to chemical mutagenesis treatments have been shown to evolve higher-fidelity polymerases. However, many viruses cannot modulate replication fidelity because they do not encode their own polymerase. Here, we show a new mechanism for regulating viral mutation rates. We found that, under mutagenic conditions, the single-stranded bacteriophage X174 evolved delayed lysis, and that this allowed the virus to increase the amount of progeny produced per cell. As a result, the viral population was amplified in fewer infection cycles, reducing the chances for mutation appearance. V iral mutation rates vary amply, from 10Ϫ8 to 10 Ϫ4 substitutions per nucleotide per round of copying (s/n/r), and some of the biochemical and genetic determinants of this variability have been elucidated (1). All RNA virus polymerases studied, except those of coronaviruses, lack 3=exonuclease proofreading activity, making replication more error-prone than in DNA viruses (2-5). Also, single-stranded viruses tend to show higher mutation rates than double-stranded genomes (6, 7). Furthermore, in DNA viruses and, to a lesser extent, RNA viruses mutation rates correlate negatively with genome size, although the causes of this correlation remain poorly understood (8-11). In theory, mutation rates should be evolutionarily adjusted in response...

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Correlation Between Mutation Rate and Genome Size in Riboviruses: Mutation Rate of Bacteriophage Qβ

Cited by 63 publications

References 52 publications

How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities?

How Do Species Interactions Affect Evolutionary Dynamics Across Whole Communities?

Contribution of Silent Mutations to Thermal Adaptation of RNA Bacteriophage Qβ

Delayed Lysis Confers Resistance to the Nucleoside Analogue 5-Fluorouracil and Alleviates Mutation Accumulation in the Single-Stranded DNA Bacteriophage ϕX174

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